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Biotribological Assessment for

Artificial Synovial Joints: The Role

of Boundary Lubrication

Doctorate of Philosophy

in

Biomedical Engineering

by

LORNE R GALE, BE(Mech, Hons)

Thesis submitted for the degree of Doctor of Philosophy,

School of Engineering Systems,

Institute of Health and Biomedical Innovation (IHBI),

Queensland University of Technology, Brisbane

2007

iii

Abstract

Biotribology, the study of lubrication, wear and friction within the body, has

become a topic of high importance in recent times as we continue to encounter

debilitating diseases and trauma that destroy function of the joints. A highly

successful surgical procedure to replace the joint with an artificial equivalent

alleviates dysfunction and pain. However, the wear of the bearing surfaces in

prosthetic joints is a significant clinical problem and more patients are surviving

longer than the life expectancy of the joint replacement. Revision surgery is

associated with increased morbidity and mortality and has a far less successful

outcome than primary joint replacement. As such, it is essential to ensure that

everything possible is done to limit the rate of revision surgery. Past experience

indicates that the survival rate of the implant will be influenced by many

parameters, of primary importance, the material properties of the implant, the

composition of the synovial fluid and the method of lubrication. In prosthetic

joints, effective boundary lubrication is known to take place. The interaction of the

boundary lubricant and the bearing material is of utmost importance. The identity

of the vital active ingredient within synovial fluid (SF) to which we owe the near

frictionless performance of our articulating joints has been the quest of researchers

for many years. Once identified, tribo tests can determine what materials and more

importantly what surfaces this fraction of SF can function most optimally with.

Surface-Active Phospholipids (SAPL) have been implicated as the body’s natural

load bearing lubricant. Studies in this thesis are the first to fully characterise the

adsorbed SAPL detected on the surface of retrieved prostheses and the first to

verify the presence of SAPL on knee prostheses.

Rinsings from the bearing surfaces of both hip and knee prostheses removed from

revision operations were analysed using High Performance Liquid

Chromatography (HPLC) to determine the presence and profile of SAPL. Several

common prosthetic materials along with a novel biomaterial were investigated to

determine their tribological interaction with various SAPLs. A pin-on-flat

tribometer was used to make comparative friction measurements between the

various tribo-pairs. A novel material, Pyrolytic Carbon (PyC) was screened as a

iv

potential candidate as a load bearing prosthetic material. Friction measurements

were also performed on explanted prostheses.

SAPL was detected on all retrieved implant bearing surfaces. As a result of the

study eight different species of phosphatidylcholines were identified. The relative

concentrations of each species were also determined indicating that the unsaturated

species are dominant. Initial tribo tests employed a saturated phosphatidylcholine

(SPC) and the subsequent tests adopted the addition of the newly identified major

constituents of SAPL, unsaturated phosphatidylcholine (USPC), as the test

lubricant. All tribo tests showed a dramatic reduction in friction when synthetic

SAPL was used as the lubricant under boundary lubrication conditions. Some tribo-

pairs showed more of an affinity to SAPL than others. PyC performed superior to

the other prosthetic materials. Friction measurements with explanted prostheses

verified the presence and performance of SAPL.

SAPL, in particular phosphatidylcholine, plays an essential role in the lubrication

of prosthetic joints. Of particular interest was the ability of SAPLs to reduce

friction and ultimately wear of the bearing materials. The identification and

knowledge of the lubricating constituents of SF is invaluable for not only the future

development of artificial joints but also in developing effective cures for several

disease processes where lubrication may play a role. The tribological interaction of

the various tribo-pairs and SAPL is extremely favourable in the context of reducing

friction at the bearing interface. PyC is highly recommended as a future candidate

material for use in load bearing prosthetic joints considering its impressive

tribological performance.

Keywords

SAPL, orthopaedics, biotribology, boundary lubrication, prosthetics, total joint

replacement, PC, USPC, PyC, Pyrolytic Carbon, surfactant, synovial fluid, SF,

arthritis, joint disease, cartilage, artificial joints, BL.

v

List of Abbreviations

SAPL - Surface Active Phospholipid

TJR - Total Joint Replacement

PC - PhosphatdiylCholine

USPC - Unsaturated Phosphatdiylcholine

SPC - Saturated Phosphatdiylcholine

BL - Boundary Lubrication

HPLC - High Performance Liquid Chromatography

SF - Synovial Fluid

GAG - Glycosaminoglycan

HA - Hyaluronic Acid

DPPC - Dipalmitoyl Phosphatidylcholine

DLPC - Dilinoleoyl Phosphatidylcholine

PLPC - Palmitoyl Linoleoyl Phosphatidylcholine

POPC - Palmitoyl Oleoyl Phosphatidylcholine

DOPC - Dioleoyl Phosphatidylcholine

SLPC - Stearoyl Linoleoyl Phosphatidylcholine

PSPC - Palmitoyl Stearoyl Phosphatidylcholine

OSPC - Oleoyl Stearoyl Phosphatidylcholine

BSA - Bovine Serum Albumin

µ - Coefficient of friction

OA - Osteo Arthritis

RA - Rheumatoid Arthritis

PyC - Pyrolytic Carbon

LGP - Lubricating Glyco Protein

LTI carbon - Low Temperature Isotropic carbon

GCS - Glucosamine & Chondroitin Sulfate

NSAIDS - Non-Steroidal Anti-Inflammatory Drugs

VS - Visco Supplementation

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Glossary of Terms

adsorption: A mechanism of attaching to a surface by chemical or

physical bonding.

amphipathic: One end of a molecule has an affinity for the phase in which

it is in, the other end is repelled by the same phase.

arthrocentesis: The surgical puncture and aspiration of a joint.

arthrology: That part of anatomy which treats of joints.

asperities: roughness of a surface , highest points.

boundary lubrication: Lubrication where there is solid-to-solid contact of the

sliding surfaces.

chondrocyte: The cellular component of the cartilage matrix

contact angle: The angle subtended at the edge of a droplet at the triple

point.

colloid: Microscopic particles suspended in some sort of liquid

medium.

cytokine: Mediator of inflammation.

detritus: A mass of substances worn off from solid bodies by

attrition, and reduced to small portions.

esterified: A chemical reaction in which two chemicals (typically an

alcohol and an acid) form an ester as the reaction product.

glycosaminoglycan: Any of a class of polysaccharides derived from hexosamine

that form mucins when complexed with proteins: formerly

called mucopolysaccharide.

HPLC: HPLC is used to separate components of a mixture by using

a variety of chemical interactions between the substance

being analysed and the chromatography column.

hyaluronic acid: A mucopolysaccharide serving as a viscous medium in the

tissues of the body and as a lubricant in joints: a GAG.

hyaluronidase: An enzyme that catalyses the breakdown of hyaluronic acid

in the body, thereby increasing tissue permeability to fluids.

Hydrodynamic Lubrication where the sliding surfaces are separated by

lubrication: a wedge of fluid.

hydrophilic: Highly compatible with the aqueous phase, or “water-

loving”.

hydrophobic: Repels the aqueous phase, or “water-hating “.

lamellar body: Layered structure (A storage form for surfactant).

lipid: Any of a group of organic compounds, including the fats,

oils, waxes, sterols, and triglycerides, that are insoluble in

water but soluble in nonpolar organic solvents, are oily to

the touch, and together with carbohydrates and proteins

constitute the principal structural material of living cells.

lipase: Any of a class of enzymes that break down lipids.

lubricin: A glycoprotein implicated as the boundary lubricant for the

synovial joint.

lyophilic: Characteristic of a material that readily forms a colloidal

suspension.

viii

mucin: Any of a class of glycoproteins found in saliva, gastric juice,

etc., that form viscous solutions and act as lubricants or

protectants on external and internal surfaces of the body.

non-Newtonian: As the rate of shear increases, viscosity decreases; as the

rate of shear decreases, viscosity increases.

osteoarthritis: A degenerative joint disease where the initiating event can

be joint trauma, acute or repetitive.

proteolipid Any of a class of lipid-soluble proteins.

proteoglycan: Any of various mucopolysaccharides that are bound to

protein chains in covalent complexes and occur in the

extracellular matrix of connective tissue.

rheumatoid arthritis: A degenerative disease which is predominantly

inflammatory in nature and origin.

Ringer's solution: An aqueous solution of the chlorides of sodium, potassium,

and calcium that is used topically as a physiological saline.

surfactant: A substance that can effectively modify the surface energy

of an interface.

synoviocyte: The cellular component of the synovial membrane.

synovium: Another term for the synovial membrane.

tribology: The science and technology of surfaces that are in contact

and move in relation to each other.

tribo-pair: The name given to the two materials that slide over each

other in a lubricated system.

triple point: The point where solid, liquid and air all meet.

trypsin: An enzyme capable of breaking down proteins .

turbostratic: A type of crystalline structure where the basal planes have

slipped sideways relative to each other, causing the spacing

between planes to be greater than ideal.

zwitterion: A molecule in which each end carries a different charge

(positive or negative)to produce a charge dipole.

ix

List of Publications and Manuscripts

Refereed Publications

[1] GALE, L.R., R. COLLER, D.J. HARGREAVES, B.A. HILLS, and R.

CRAWFORD (2007): 'The role of SAPL as a boundary lubricant in prosthetic

joints', Tribology International, 40(4), pp. 601-606

[2] GALE, L.R., Y. CHEN, B.A. HILLS, and R.W. CRAWFORD (2006):

'Boundary lubrication of joints: Characterisation of Surface-Active Phospholipids

found on retrieved implants', Acta Orthopaedica, 78(3), pp. 309-314

[3] GALE, L.R., R.W. CRAWFORD, D.J. HARGREAVES and J. KLAWITTER

(2006): 'Boundary lubrication of Pyrolytic Carbon with Surface Active

Phospholipids: Tribological Assessment for Artificial Joints', Acta Orthopaedica,

Under Revision, pp.

[4] L.R. GALE , GUDIMETLA, P., Y. CHEN, R. CRAWFORD and D.J.

HARGREAVES (2007): ' Tribological Testing of Saturated and Unsaturated

Surface Active Phospholipids: Implications for artificial joints', Proceedings of the

Institution of Mechanical Engineers, Part H: Journal of Engineering in Medicine,

Submitted, pp.

Refereed Conference Publications

[1] GALE, L.R., Y. CHEN, B.A. HILLS, and R.W. CRAWFORD (2005):

'Boundary Lubrication of Synovial Joints: Characterisation of the Lubricant', 12th

International Conference on Biomedical Engineering ICBME 2005. Singapore,

2005, pp. 3A4-14.

[2] GALE, L.R., B.A. HILLS, R.W. CRAWFORD, and J. KLAWITTER (2005):

'Tribological Evaluation of Pyrolytic Carbon and Surface Active Phospholipid for

Artificial Joints', 12th International Conference on Biomedical Engineering

ICBME 2005. Singapore, 2005, pp. 3A4-12.

xi

Table of Contents

Abstract ......................................................................................................................... iii

List of Abbreviations.......................................................................................................v

Glossary of Terms ........................................................................................................ vii

List of Publications and Manuscripts .............................................................................ix

Table of Contents ...........................................................................................................xi

Statement of Original Authorship .................................................................................xv

Acknowledgements ......................................................................................................xvi

List of Figures ............................................................................................................ xvii

List of Tables.................................................................................................................xx

Chapter 1 Introduction 1

1.1 Description of Scientific Problems Investigated .......................................................1

1.2 Overall Objectives of the Study ................................................................................3

1.3 Specific Aims of the study ........................................................................................4

1.4 Account of Scientific Contribution Linking the Scientific Papers............................5

Chapter 2 Literature Review - Biotribology 7

2.1 Tribological studies of the performance of natural synovial joints.........................10

2.1.1 Overview - Lubrication of the Diarthrodial Joint: Search for the

Lubricating Factor.......................................................................................................12

2.2 Tribological aspects of prostheses...........................................................................16

2.3 Summary .................................................................................................................18

Chapter 3 Literature Review – Anatomy & Physiology of Diathrodial Joints 19

3.1 Anatomy of the Synovial Joint ................................................................................19

3.2 Articular (Hyaline) Cartilage...................................................................................21

3.2.1 The Articular Surface.........................................................................................22

3.2.2 Articular Cartilage Matrix .................................................................................23

3.2.3 Response to load ................................................................................................27

3.3 Synovial Membrane ................................................................................................28

3.3.1 The Synoviocytes...............................................................................................29

3.3.2 Removal of Substances from the Joint Space....................................................30

xii

3.3.3 The Synovium in Disease ................................................................................. 30

3.4 Synovial Fluid......................................................................................................... 30

3.4.1 Synovial Fluid Composition ............................................................................. 31

3.4.2 Production of Synovial Fluid ............................................................................ 34

3.4.3 Functions of Synovial Fluid .............................................................................. 35

3.4.4 Rheology of Synovial Fluid .............................................................................. 36

3.4.5 Synovial Fluid Lipids........................................................................................ 37

3.4.6 Synovial Fluid in Disease ................................................................................. 38

3.5 Osteoarthritis........................................................................................................... 38

3.5.1 Treatments of Osteoarthritis.............................................................................. 41

3.6 Total Artificial Joint Replacement.......................................................................... 43

3.6.1 Artificial joint failure ........................................................................................ 45

3.6.2 Biomaterials ...................................................................................................... 46

3.6.2.1 Pyrolytic Carbon ..................................................................................... 47

3.7 Summary................................................................................................................. 53

Chapter 4 Literature Review – Lubrication of Joints 55

4.1 Physical Science of Lubrication, Friction and Wear .............................................. 59

4.1.1 Fluid-Film Lubrication...................................................................................... 65

4.1.2 Boundary Lubrication ....................................................................................... 68

4.1.3 Mixed Lubrication............................................................................................. 71

4.1.4 Wear .................................................................................................................. 71

4.2 Natural Joint Lubrication: A Review...................................................................... 73

4.2.1 Experimental techniques and apparatus used to determine the lubrication

of joints ...................................................................................................................... 75

4.2.2 Fluid-Film Models ............................................................................................ 80

4.2.2.1 Hydrodynamic Lubrication ..................................................................... 80

4.2.2.2 Weeping Lubrication............................................................................... 81

4.2.2.3 Elastohydrodynamic Lubrication ............................................................ 83

4.2.3 Mixed Lubrication Models................................................................................ 84

4.2.3.1 Osmotic Lubrication................................................................................ 86

4.2.3.2 Squeeze-Film Lubrication....................................................................... 86

4.2.3.3 Boosted lubrication ................................................................................. 88

4.2.4 Boundary Lubrication Models .......................................................................... 89

xiii

4.2.5 The Search for the Boundary Lubricant ............................................................90

4.2.5.1 Enzyme Studies........................................................................................93

4.2.5.2 Lubricating Glycoprotein.........................................................................94

4.2.5.3 Lipids .......................................................................................................95

4.2.5.4 Surface-active Phospholipid ....................................................................97

4.3 Artificial Joint Lubrication: A Review....................................................................98

4.3.1 Fluid Film Models ...........................................................................................101

4.3.2 Boundary Lubrication Models .........................................................................102

4.3.3 Mixed Lubrication Models ..............................................................................103

4.3.4 Tribological Studies for total joint replacements.............................................104

4.4 Summary ...............................................................................................................107

Chapter 5 Literature Review – Boundary Lubrication for Artificial Joints 109

5.1 Surface Chemistry .................................................................................................111

5.1.1 Surfaces and Surface Energy ...........................................................................111

5.1.2 Hydrophobic vs Hydrophilic ...........................................................................112

5.1.3 Surface Tension and its Measurement .............................................................113

5.1.4 The Young Equation........................................................................................113

5.1.5 The Contact Angle ...........................................................................................115

5.1.6 Surfactants .......................................................................................................115

5.1.7 Electrical Charge..............................................................................................116

5.1.8 Adsorption .......................................................................................................116

5.2 Tribochemistry ......................................................................................................117

5.3 Surfactants for Boundary Lubrication...................................................................118

5.3.1 Lubrication via Surfactants..............................................................................119

5.3.2 Biological Surfactants......................................................................................120

5.3.3 Types of Lipids ................................................................................................122

5.3.4 Phospholipid Analysis .....................................................................................126

5.3.5 Adsorption in Biology .....................................................................................126

5.3.6 Biological Surfactants and Lubrication ...........................................................127

5.4 Boundary Lubrication via SAPL...........................................................................128

5.4.1 SAPL and Wear in artificial joints...................................................................130

5.5 Summary ...............................................................................................................131

xiv

Chapter 6 Scientific Paper I - The Role of SAPL as a Boundary Lubricant in

Prosthetic Joints 133

Chapter 7 Scientific Paper II – Boundary lubrication of Pyrolytic Carbon with

Surface Active Phospholipids: Tribological Assessment for

Artificial Joints 141

Chapter 8 Scientific Paper III – Boundary lubrication of joints:

Characterisation of Surface-Active Phospholipids found on

retrieved implants 149

Chapter 9 Scientific Paper IV - Tribological Testing of Saturated and

Unsaturated Surface Active Phospholipids: Implications for

artificial joints 157

Chapter 10 General Discussion 165

10.1 Conclusions......................................................................................................... 173

10.2 Future Work........................................................................................................ 174

References 177

xv

Statement of Original Authorship

The work contained in this thesis has not been previously submitted for a

degree or diploma at any other tertiary education institution. To the best of my

knowledge this report contains no material previously published or written by

another person except where due reference is made.

Signed:

Date: 24th

Sept 2007

xvi

Acknowledgements

I would like to acknowledge my supervisors Professor Doug Hargreaves, Professor

Ross Crawford and Professor Brian Hills. Doug, thank you for your faith and trust

in me. Ross, thank you for your financial support and exposure to the orthopaedic

world. Brian, rest in peace.

A special thank you to my fellow scholars. Your guidance, help and support has

been highly valued.

A big thank you to my friends and family that actually understood and appreciated

what I was doing. Your interest and enthusiasm provided the essential motivation

required along the way.

Most importantly I am indebted to my wife Michelle for her endless patience and

support throughout. Without her love, care and encouragement the journey would

have never been possible.

My daughter Portia has been the best part of this journey, providing me with

continual entertainment and love that only a child knows how.

xvii

List of Figures

Figure 3.1. Diagram of the structure of the knee. Source: (MowHayes)

Figure 3.2: Schematic of a proteoglycan molecule and schematic of a proteoglycan

aggregate (BaderLee)

Figure 3.3: Schematic of the Hypothetical Layers of Articular Cartilage

(BlackHastings)

Figure 3.4. Various forms of PyC indicating surface finish. (Left to Right) As-

deposited, machined and polished.

Figure 4.1. Amontons' Laws of Friction. Source: (Shi)

Figure 4.2. Range of coefficients of kinetic friction reported in the literature for the

mammalian joint are depicted over a physiological range of sliding velocities and

compared with the a modified classical Stribeck diagram. Source: (Hills)

Figure 4.3. Lubrication regimes Source: (Dowson,Wrightet al April)

Figure 4.4. Molecular Structure of Common Solid Lubricants (a) graphite, and (b)

molybdenum disulfide. (Erdemir 2001)

Figure 4.5: Hydrodynamic Lubrication; Diagram showing the formation of the

pressure generated due to a wedge of fluid that separates the moving bearing

surfaces. (Dinnar)

Figure 4.6: Weeping or Hydrostatic Lubrication; a) as load is applied fluid

flows towards the rubbing surfaces at high pressure, carrying the load with minimal

friction. b) when the load is removed the cartilage expands, drawing in synovial

fluid. (Adapted from (McCutchen))

Figure 4.7: Elastohydrodynamic Lubrication; The top surface in this diagram is

deformable, providing a larger fluid film when load is applied.(Adapted from

(Dowson,Wrightet al April))

Figure 4.8: Microelastohydrodynamic Lubrication; Diagram showing the

deformation of the asperities on the surface of the cartilage under load decreasing

the risk of contact and allowing maintenance of a thinner fluid-film. (Adapted from

(DowsonJin))

Figure 4.9. Mixed lubrication showing that one lubrication regime does not answer

the operating conditions in the joint but a combination of mechanisms. Source:

(PanjabiWhite)

xviii

Figure 4.10: Mixed Lubrication; When the fluid film fails, friction is prevented

by boundary lubrication. (Adapted from (Dowson,Wrightet al April))

Figure 4.11: Squeeze Film Lubrication; The arrows indicate the movement of

fluid away from the load-bearing region leaving an enriched film of synovial fluid

between the surfaces. (Adapted from (Hou,Mowet al March))

Figure 4.12: Boosted Lubrication; a) path of the fluid flow into the cartilage

surfaces while loaded. b) schematic diagram of the pools of enriched synovial fluid

formed on the surface of the cartilage. (Adapted from (McCutchen)

Figure 4.13: Boundary Lubrication; The surface layer prevents the articulating

surfaces from coming into contact.(Adapted from (WrightDowson February))

Figure 4.14. Dependence of the efficiency on the friction coefficient in natural and

artificial joints. Source: (Gavrjushenko)

Figure 4.15. Geometric configurations of various tribometers. Source:

(Dumbleton)

Figure 5.1. The triple point in cross section. Depicting the balance of forces at the

edge of a droplet where the liquid, solid and air all meet to subtend a contact angle

(θ).

Figure 5.2. General structure of phosphoglycerides, emphasizing their amphipathic

nature (Schwarz). Various groups for X are given in Figure 5.3.

Figure 5.3. Various polar head groups for the general phosphoglyceride depicted in

Figure 5.2. Source: (http://en.wikipedia.org/wiki/Membrane_lipids)

Figure 5.4. A molecular model for the adsorption of phospholipid zwitterions to a

negatively charged surface in which cations in the plane of the phosphate ions pull

those ions together, thus enhancing close packing of both polar and non polar

moieties and imparting coherency. (Hills)

Figures within Submitted Papers

Chapter 6

Figure 1: Phospholipid model. This model shows the basic mechanism of

phospholipid adsorption to the cartilage surface, rendering it more hydrophobic,

and how interspersed cations pull the phosphate molecules together enabling high

cohesion (adapted from Hills, 2000).

xix

Figure 2: Oligolamellar structure of a common solid lubricant graphite.

Figure 3: Hounsfield test rig set-up showing horizontal position and custom made

attachments.

Figure 4: Schematic of Hounsfield set-up: (1) Hounsfield control panel and drive;

(2) plate head; (3) UHMWPE pin in pin holder; (4) stainless steel plate; (5) heating

resistors and thermocouple; (6) temperature control unit; and (7) force transducer.

Figure 5: Coeff. of friction at ambient UHMW PE/SS.

Figure 6: Coeff. of friction at 371 UHMW PE/SS.

Figure 7: Coeff. of friction at ambient UHMW PE/PyC.

Chapter 7

Figure 1: Schematic of pin-on-flat tribometer: 1 - control panel and drive, 2 - plate

head, 3 - UHMWPE pin in pin holder, 4 - stainless steel plate, 5 - heating resistors

and thermocouple, 6 - temperature control unit, 7 - force transducer.

Figure 2: Coefficient of friction for the material combinations under the three

lubrication conditions. Dark columns represent dry conditions, light grey columns

represent saline lubrication and light columns represent DPPC lubrication.

Chapter 8

Figure 1: Average proportions of PCs (%). Total average PC profile of the 40

implants analysed (all components included). Error bars represent standard

deviation.

Chapter 9

Figure 1: Friction force exhibited by different surfactants (0.2% concentration)

Figure 2: Effect of Concentration on the Friction Force in USPCs

Figure 3: Comparison of the Behaviour of different combinations of surfactant

species.

xx

List of Tables

Table 4.1. Boundary lubricants within SF suitable for tribo tests. Source: (Brown

& Clarke 2006)

Tables within Submitted Papers

Chapter 7

Table 1: Surface roughness of Samples (Ra – roughness average)

Table 2: Adsorption of DPPC to PyC

Chapter 8

Table 1: Profile of phosphatidylcholine species detected on retrieved implants: (a)

Polymer components (b) Metallic components

Chapter 1: Introduction

1

Chapter 1

Introduction

This thesis seeks to contribute to solving the problems of inadequate artificial joint

design from a tribological perspective. Artificial joints have a limited life time and

this has been traced to wear related issues. By understanding the methods of

lubrication in joints, in particular boundary lubrication which is the dominant

regime in artificial joints, engineers will be better suited to developing longer

lasting implants.

1.1 Description of Scientific Problems Investigated

The “Bone & Joint Decade” (2000-2010) has been dedicated to improving the

quality of life for the millions of sufferers of bone and joint disorders. This thesis

represents a contribution to this ongoing effort. The major offender of bone and

joint disorders is arthritis. Osteoarthritis (OA) has emerged to be one of the most

serious and costly health problems encountered in the last century. Simply OA is a

massive problem. OA accounts for more than half of all chronic conditions in the

elderly and statistics show that 85% of the population will suffer from OA in their

lifetime (American Academy of Orthopaedic Surgeons 2002). Any light that can be

shed on this debilitating disease will be most beneficial to the world at large.

Total joint replacement (TJR) offers a partial solution to this problem but has

problems of its own. At best it is a temporary solution to a much larger problem.

Hip and knee replacement surgery has become a common procedure in recent years

as a method of eliminating pain and discomfort and to improve joint functionality

for patients with end stage arthritis in their lower extremities (Scmalzried &

Callaghan 1999). Although a very successful operation, TJR does not offer the

same performance as the natural joint and suffers from a limited lifetime.

Previously, joint replacement was reserved for the elderly. However, due to the

success of the procedure it is increasingly used in younger individuals. This,


2

combined with an ageing population, has resulted in an increase in the incidence of

primary joint replacement. The rate of revision surgery is also increasing. Revision

surgery is associated with increased morbidity and mortality and has a far less

successful outcome than primary joint replacement. As such, it is essential to

ensure that everything possible is done to limit the rate of revision surgery

(Australian Orthopaedic Association 2002). Because we are living to older ages we

are essentially outliving the lifetime of current joint replacement designs. Research

shows that current implants are surviving to the 15 year mark (Charnley 1982;

Donnelly 1997; Kobayashi 1997) but much beyond that is questionable.

The main problem with TJRs is that they fail.

Past experience indicates that the survival rate of the implant will be influenced by

the micro and macro geometry as well as the material properties of the implant

(Donnelly 1997; Kobayashi 1997; Sumner 1998; Simmons, Shaker et al. 2001).

The reasons for failure of current hip and knee joint replacements are, in order of

proportion; loosening, dislocation and wear (Australian Orthopaedic Association

2002). Dislocation is beyond the scope of this thesis but may lie with a better

education of surgeons and the use of computer guided surgery. With dislocation

aside the other two modes of failure, loosening & wear, account for more than half

of the revision procedures and may be related. Loosening may be caused by the

osteolysis of the bone around the implant which is thought to be due to the body’s

response to foreign wear particles produced in the artificial joint. The loss of

material at the bearing surface not only causes the implant to be worn away but it is

this very wear debris which may cause failure in TJR due to loosening. Essentially

many TJRs are failing because of a tribological problem. Any reduction in wear

will be beneficial to the lifetime of the implant. Wear is reduced by lubrication.

There are considerable political, economic, social and technical reasons to improve

the wear performance of biomaterials used in joint replacements.

The tribology of TJRs is not well understood. Boundary lubrication is the last

defence in lubrication engineering. The conditions suited to boundary lubrication

are low relative surface velocities, like reciprocating motion and high loads which

are conditions matched by the human joint. Boundary lubrication can only occur if


3

there is in fact a boundary lubricant present; if not, a dry bearing will exist and

direct contact will occur leading to high wear. The human synovial joint is not a

dry bearing by any means, even in a diseased, arthritic state. In fact the joint is

filled with synovial fluid, a liquid made mostly of water. It is obvious that this is

nature’s provision for a lubricant, yet it is known in lubrication engineering that

water is a poor lubricant. Even more so, boundary lubrication dictates the

requirement of some surface binding substance that can adsorb to the bearing

surfaces and provide a protecting film. So what else is in synovial fluid that can be

utilised as a lubricant? Synovial fluid also contains small amounts of ‘other’

substances. As yet no consolidation has arisen as to the component of synovial

fluid which provides the effective boundary lubrication that is known to exist. The

problem with artificial joints is that they rely upon boundary lubrication; however,

the boundary lubricant has not yet been completely identified. In order to improve

the lubrication of artificial joints the lubricating component of synovial fluid must

first be completely identified and understood.

In summary, TJR is currently not an entirely sufficient solution to OA. Better

artificial joint design should be instituted which means understanding how joints

are lubricated and designing to suit using materials that complement the boundary

lubricant.

1.2 Overall Objectives of the Study

The overall objective of this research included understanding and defining the

tribological aspects of the artificial synovial joint and in particular, the importance

of the role of boundary lubrication. The identification of the boundary lubricant in

synovial joints was essential to this objective. This knowledge may then be used to

increase our understanding of the relationship between the boundary lubricant and

prosthetic materials, both common and novel. Extending our understanding of

artificial synovial joints and their tribological nature may indeed provide an insight

to the crippling disease, osteoarthritis, and, at the very least, provide a better basis

for joint replacement design.


4

1.3 Specific Aims of the study

Specifically, the aims of the thesis were to:

1) Determine the tribological performance of common prosthetic materials

lubricated in vitro by Surface Active Phospholipid (SAPL), which has been

implicated as the boundary lubricant in the joint.

2) Determine the tribological performance of a novel load-bearing prosthetic

material: Pyrolytic Carbon (PyC).

3) Show evidence of SAPL on the surface of retrieved knee implants.

4) Use High Performance Liquid Chromatography (HPLC) to identify the

composition of SAPL found on the surface of retrieved hip and knee

implants.

5) Provide evidence of boundary lubrication in TJR by measuring the

frictional performance of retrieved implants ex vivo.

6) Use the profile of SAPL identified via HPLC to develop a synthetic

boundary lubricant suitable for laboratory testing.

7) Determine the tribological performance of the synthesised test lubricant and

common prosthetic materials.

8) Provide recommendations for the future of artificial joint design.

9) Provide recommendations for the implementation of a standardised test

lubricant suitable for in vitro laboratory testing for the purpose of

evaluating artificial implants.

Aims 2-7 make up the original features of this thesis and to the best of the author’s

knowledge have not been investigated else where.


5

1.4 Account of Scientific Contribution Linking the

Scientific Papers

This thesis begins with a literature review of biotribology at large. Chapter 2 is an

overview of the science of biotribology with a focus on the lubrication within the

human body. Subsequent chapters 3-5 give an increasing in detail review to the

area of biotribology of interest. Namely, Chapter 3 reviews the structure and

function of the human diarthrodial joint, its failure due to OA and the current

remedy of Total Joint Replacement and its failure. Chapter 4 is an overview of the

lubrication of human joints. Chapter 5 is an in depth look at boundary lubrication.

Chapters 6-9 are scientific papers that have been written by the thesis author

reporting on research into the lubrication of artificial joint materials.

Chapter 6 is the first scientific paper published and was an initial study to

determine the tribological interaction of a synthetic SAPL, dipamitoyl

phosphatidylcholine (DPPC) and a novel load bearing prosthetic material, PyC.

This study was performed to screen a new candidate material for hip and knee

implants with respect to producing a low friction bearing surface and to further

support the notion that effective boundary lubrication exists between SAPL and

prosthetic materials.

Chapter 7 is the second scientific paper submitted for publication and is a more

advanced study that extends the previous work with PyC given the encouraging

results produced in the preliminary study (Chapter 6). This study was a tribological

assay of several types of PyC lubricated with DPPC. In addition a goniometer was

used to determine the interaction of the SAPL with the PyC surface. Adsorption

tests were performed to establish the tenacity of DPPC to the PyC surface. This

study revealed the frictional performance of many forms of PyC and confirmed the

ability of SAPL to act as a boundary lubricant on artificial surfaces.

Previous work by our research group (Purbach, Hills et al. 2002) established the

presence of SAPL on the surface of retrieved hip implants. Ongoing data collection


6

from the implant retrieval studies generated sufficient data so that a further report

could be published. This report, the third scientific paper of the thesis forms

Chapter 8. This study fully characterised the SAPL found on the surface of

retrieved hip and knee implants by HPLC. This knowledge would allow for a more

accurate definition of the boundary lubricant present on the surface of artificial

joints and support for the boundary lubrication of artificial joints. This study

produced a profile of the constituents of SAPL that revealed that DPPC was not in

fact the dominant portion suggesting that future friction testing of artificial joint

materials should utilise a lubricant similar to the profile of SAPL detected on the

artificial joint surface.

Considering the information obtained in the study described in Chapter 8 it

followed that the next study should test again the common and novel artificial joint

materials for their frictional performance using a synthetic copy of the determined

SAPL profile. The aim of this study was to compare the work done previously

using only DPPC as the lubricant to the results achieved using the more accurate

definition of the boundary lubricant. This paper forms Chapter 9 of the thesis.

The four scientific papers (Chapters 6-9) are the thesis author’s original

contribution to this field of research.

The thesis concludes with a general discussion of the outcomes and a summary of

the four papers presented for examination. Nature has provided an effective

boundary lubricant in the form of SAPL as found on retrieved implant surfaces.

Boundary lubrication is instrumental to the reduction of friction between prosthetic

joint materials. Future artificial joint design should incorporate these parameters in

order to improve the currently unsatisfactory lifetime of TJRs. Novel materials,

such as PyC, can interact favourably with SAPL and suggest a tribologically

satisfactory biomaterial suitable for future artificial implants. Better artificial joint

design may be achievable by means of material selection and surface modification

that can capitalise on the nature of the lubricant present. This thesis also promotes

the use of a standardised lubricant for in vitro testing that is similar to what is

found to lubricate artificial joints.

7

Chapter 2

Literature Review - Biotribology

As the thesis author has a background in Mechanical Engineering the following

literature review is broad in order to provide a sound background to the

biotribology field. Biotribology (BT) is a very large field of research indeed. This

thesis will focus on the application of this science, biotribology, to human artificial

synovial joints. This chapter will outline the general topic of BT and the

subsequent literature review chapters will cover further detail of the thesis topic.

The literature review, Chapters 2-5, includes a discussion of the joints themselves,

the fluid within the joint, the disease osteoarthritis (OA) and the current solution of

artificial joint replacement, the bearing materials, a review of the various modes of

lubrication and a focus on boundary lubrication and SAPLs,

BT is a relatively new term introduced in the early 1970’s to describe a group of

sciences that converge on one single topic: the study of friction, wear and

lubrication within biology. In consideration that the invention of this term and the

creation of this field of research would not have occurred if it had not been for the

increasing incidence of OA it is essential that a review be made of the natural

synovial joint itself. This will form part of Chapter 3 which will also include a

review of the degenerative joint disease, OA, the current remedy TJR and the

failure of these replacement joints.

Originally BT was applied to natural synovial joints in an effort to understand the

joints’ mechanical functions and the mechanisms of failure with the hope of

reducing the effects of OA. Physicians, physiologists, biochemists,

rheumatologists, biologists, rheologists and engineers joined forces in an effort to

understand how the natural joint was lubricated and, more importantly, how the

joint was being compromised by OA. This will form part of Chapter 4. OA has not

been cured and the best remedy to alleviate joint dysfunction has been the

invention of TJRs. Artificial joints are prone to failure and the science of BT has

Chapter 2: Literature Review - Biotribology

8

now turned its focus to the artificial joint in an attempt to improve the lifetime of

the prosthesis. The remainder of Chapter 4 discusses the lubrication of artificial

joints.

It is well known that effective boundary lubrication occurs in artificial joints.

Chapter 5 is an in depth look at boundary lubrication.

Biotribo1ogy is a challenging, multidisciplinary field of research, involving

biology, orthopaedics, biomechanics, biomaterials science and tribology.

Tribology, an area of engineering, is the science that studies the lubrication of

interacting surfaces in relative motion. Friction is the resistance to relative sliding

or rolling motion of the surfaces. Overcoming friction dissipates energy and causes

wear of the surfaces. Lubrication provides an effective means of reducing friction

and wear by separating contacting solids with a thin layer of material of low shear

strength. The purpose of tribological research of prosthetic joints is to minimize

friction and wear of the implant, and thereby to increase the lifetime of the joint

(Calonius 2002). So, tribology plays a major role in the effective treatment of one

of the most common medical conditions known in the western world (Unsworth

1991).

Biotribology is nature’s way of turning a science into an art, so amazing is the

ability of biology to lubricate it’s mechanical functions. Engineers may be the only

ones that truly appreciate and marvel at nature’s eloquent yet complex methods of

lubrication. BT applies the principles of lubrication engineering in an attempt to

understand how the body lubricates it’s articulating bearings: the synovial joints. A

mechanical bearing analysis is not a complete analysis of the human joint, as it is a

biological bearing where biochemistry and surface chemistry play a very important

role, potentially far more important than the mechanical part (Dowson 1990). This

requires engineers to call upon the expertise of other disciplines to understand

human joint lubrication and to design suitable replacements. As will be seen by the

diversity of this literature review, biotribology requires skills from the engineer that

far extend beyond traditional engineering principles.


9

‘Novel’ expressions such as ‘biolubrication’ have been introduced by a research

group (Benz, Chen et al. 2005) to describe the dynamic properties of very thin

aqueous films between two biological surfaces in relative motion or for water

flowing through pores or between two stationary surfaces; but more generally this

expression also covers related phenomena such as the adhesion, friction,

deformations, damage, and wear of the surfaces or the lubricating fluid. These

nanoscale phenomena ultimately determine the way biofluids flow through narrow

pores or effectively lubricate a joint.

BT’s large focus is to increase the lifetime of artificial joints. Historically, new

bearing materials were 'tried out' in patients (Charnley 1966; Fisher 2000). The

consequence of incorrect design and material selection and subsequent failure now

means that there are extensive pre-clinical requirements for evaluation of materials

prior to implantation (Fisher 2000). This is by no means a simple problem.

Environmentally (biochemical) conditions in the body are harsh, biomechanical

requirements are complex and variable, and the biological response to wear

particles is largely unknown and dependent on the genetic profile of the recipient

(Fisher 2000). Biotribology is a highly multidisciplinary subject crossing

engineering materials and physical science, biological science and medicine.

Predicting the mechanical and tribological performance of bearing surfaces, and

understanding the biological responses to wear debris and the resulting potential

clinical outcomes, remains a substantial scientific and technological challenge. Key

factors limiting the successful development of improved products are our limited

understanding of biotribological science, the capability and capacity to simulate in

vivo conditions in the laboratory in pre-clinical tests, and a lack of fundamental

understanding of the complex and heterogenous biological reactions and

biocompatibility of wear debris in the body (Fisher 2000).

Tribology is itself an inter-disciplinary subject, being concerned with ". . . the

science and technology of interacting surfaces in relative motion and the practices

related thereto" (Dowson & Wright 1973). It embraces studies of lubrication,

friction, wear, tribochemistry, rheology and surface chemistry each of which calls


10

upon contributions from chemists, physicists, mathematicians, engineers, materials

scientists, and tribologists.

At a 1970 Conference on Rheology in Medicine and Pharmacy, Dr G. W. Scott

Blair, with some justification, referred to "our somewhat precocious sister-science

of tribology" (Ferguson & Nuki 1973). He commented on the interesting link and

that paper was seen as a small attempt to encourage the courtship between the

disciplines.

Dowson & Wright introduced the term "bio-tribology" to mean those aspects of

tribology concerned with biological systems (Dowson & Wright 1973). There is a

growing interest in the relevance of tribology to biological systems, with some of

the main areas of activity being grouped together as follows:

1. The abrasive wear characteristics of human dental tissues.

2. Fluid transport in the body.

3. Locomotion of micro-organisms

4. The motion and lubrication by plasma of red blood cells in narrow

capillaries.

5. The action of saliva.

6. Tribological studies of the performance of natural synovial joints.

7. Tribological aspects of prostheses

This thesis will explore the areas concerned with joints.

2.1 Tribological studies of the performance of natural

synovial joints

It is true that the largest and most successful activity in the field of biotribology has

been the study of human joints.

The human joint is a remarkable bearing. It has a low coefficient of friction (0.002)

(Jones 1934; Charnley 1959; Hills & Crawford 2003) and it is expected to survive

the dynamic loading associated with the normal activities of life for at least 70

years. The bearing material (articular cartilage) is elastic and porous. It has an


11

initial thickness of a few millimeters and, like conventional plain bearing materials,

it is mounted on a hard backing (bone). The lubricant is synovial fluid; a highly

non-Newtonian fluid which is contained within the joint space by the synovial

membrane. It consists of a dialysate of blood plasma with varying amounts of

protein/mucopolysaccharide (hyaluronic acid complex).

Theoretical and experimental studies have suggested that the joint experiences most

of the lubrication modes familiar to tribologists; hydrodynamic,

elastohydrodynamic, mixed, and boundary, together with a unique squeeze film

characteristic. The range of loading experienced by the joint is considerable and

peak loads of more than ten times body weight can be anticipated in some

activities.

In spite of the remarkable characteristics of healthy human joints, many show signs

of wear and general distress during their working life. Osteoarthritis is a process in

which the articular cartilage is roughened and worn away, with consequent

discomfort and loss of mobility. There appear to be certain similarities between the

wear of some engineering bearings and the development of osteoarthritis, and it is

for this reason that physicians, surgeons, biochemists, rheologists and engineers

have joined forces for an attack on the problem.

If an engineering bearing shows signs of distress it can often be cured by

improving the lubricant. This suggests that it might be possible to influence the rate

of development of osteoarthritis by the introduction of synthetic lubricants. The

main problem is that even if the synthetic lubricant could be introduced and

retained within the joint space, we do not have an adequate understanding of the

normal lubrication mechanism to enable us to write a specification for the synthetic

material. In addition, and maybe more importantly, is that consolidation is still

lacking as for the identification of the lubricant in the natural joint.

A large part of BT has focused on the identification of the lubricant within the joint

that facilitates such an engineering feat.


12

2.1.1 Overview - Lubrication of the Diarthrodial Joint: Search for

the Lubricating Factor

The diarthrodial or synovial joint allows relative motion of the bones. The bone

ends meet within a fibrous enclosure termed the joint capsule. The joint cavity is

filled with a pale yellow, viscous fluid known as synovial fluid. The lubricating

factor that allows the relative motion of the bones is believed to be contained

within the synovial fluid. Daily use of the synovial joints of the lower limbs - the

hips, knees and ankles, involves large ranges of relative motion in multiple

directions experiencing loads often as high as six times the body weight during a

normal walking cycle (Mow & Mak 1987). These loads must be sustained by the

biological bearings, the synovial joints, with characteristics of friction, wear and

lubrication that are the envy of modern engineering science. Cartilage rubbing on

cartilage has extremely low coefficients of friction (µ), in the range of 0.003- 0.024

(Jones 1934; Charnley 1959; Linn 1968) this is much lower than the values attained

using any synthetic bearing materials in equivalent situations, the best of which is

Teflon (PTFE) rubbing Teflon which gives a value for µ of 0.04.

The mechanics and biochemistry of synovial joint lubrication has been the subject

of detailed investigation since the early 1900’s. Interest in the biomechanics of the

joint is widespread, extending into the fields of medicine and veterinary science

due to the high incidence of osteoarthritis (OA) or degenerative joint disease (DJD)

in today’s society and the equine industry. Current literature implicates a direct

mechanical cause in the initiation of OA (Lane & Buckwalter 1993; Felson &

Radin 1994), the most commonly affected joints being those that bear load or those

that are likely to be subjected to acute injury (Meachim & Brooke 1984; Wyn-

Jones 1986; Felson 1990; Panush 1990). Deterioration of these joints causes great

pain and loss of mobility for the sufferer. Two of the major aspects in maintaining

joint mobility is lubrication (Cooke, Dowson et al. 1978) and the general

maintenance of a good load bearing surface (Freeman & Meachim 1974). It may be

that the development of OA follows the compromise of the lubricating system of

the synovial joint. What system could act within the joint to enable the exceptional

properties of friction, lubrication and wear seen at the bearing surface?


13

The major theories of joint lubrication are based upon one or a combination of two

main mechanisms: boundary lubrication mechanism, where there is solid-to-solid

contact; or, a fluid-film mechanism, where the two sliding surfaces are separated by

a fluid-film or wedge of liquid which keeps them from touching. Fluid-film

mechanisms typically reach much lower coefficients of friction than boundary

mechanisms (Williams 2005) but require velocities roughly an order of magnitude

higher than typical joint sliding rates in order to maintain the wedge that separates

the two surfaces. Below this velocity, the two surfaces touch and boundary

lubrication is all that remains to facilitate motion.

Initially, the lubrication qualities of synovial fluid were thought to relate to its

characteristic viscosity, a characteristic imparted by the hyaluronic acid component

of the synovial fluid (Ogston & Stanier 1953). It was believed that the greater the

viscosity of the fluid, the better the lubricity. Hyaluronic acid is a high-molecular-

weight polysaccharide which is present in high concentrations in synovial fluid.

Apart from being responsible for the viscosity of synovial fluid, it is also very

slippery. However, it fails to lubricate under any significant load (McCutchen

1967; Linn & Radin 1968; Radin, Swann et al. 1970; Radin, Paul et al. 1970).

Further studies using hyaluronidase (McCutchen 1966) added to synovial fluid

revealed substantially reduced viscosity following hyaluronic acid destruction, but

the lubricating abilities of the synovial fluid were unchanged. Conversely, tryptic

digestion (Wilkins 1968) left viscosity unchanged but severely compromised the

lubricity of synovial fluid. These studies demonstrated two things:

(1) That the lubricating abilities of synovial fluid are independent of its

viscosity and hence, the hyaluronic acid component.

(2) That the lubricating component of the synovial fluid is somehow

associated with a protein.

These experiments were the beginning of the search for the ingredient of synovial

fluid that has the high-load-bearing capabilities necessary for lubrication of the

lower extremity joints.


14

Studies have also been performed to demonstrate the lubricating advantage of

synovial fluid over saline using a system of fresh cartilage rubbing on glass (Jones

1934; Charnley 1959). It was found that synovial fluid had little advantage over

saline in terms of lubricating ability, at least over a short period of time. Over a

longer period, saline ceased to lubricate and the synovial fluid was clearly superior.

The fact that saline lubricated at all was significant. It indicated that there may be a

lubricant attached to the cartilage surface which required replenishing from the

synovial fluid.

Following a rigorous experimental protocol, it was demonstrated that the

lubricating abilities of synovial fluid were completely recovered in the protein

fraction of synovial fluid as opposed to the hyaluronate fraction (Radin, Swann et

al. 1970). Further refinement of the gross protein fraction showed that the

lubricating ability was located in a glycoprotein fraction that could be separated

from the bulk of the synovial proteins. Since serum proteins did not possess similar

lubricating abilities, the glycoprotein was considered unique and termed a

Lubricating Glycoprotein (LGP) or ‘Lubricin” (Swann 1978; Swann, Hendren et al.

1981; Swann, Slayter et al. 1981). Numerous characterisation tests were carried out

in an attempt to identify the glycoprotein; however, only 87—90.8% has been fully

characterised (Swann, Slayter et al. 1981; Swann, Bloch et al. 1984). Another

interesting fact is that the molecular weight (220,500) varied with the analyses used

to identify the protein (McCutchen 1966). The remaining unidentified 9.2—13%

has been shown to be lipidic in nature (Schwarz & Hills 1998) and has been

heralded as the active boundary lubricant in SF and labelled Surface Active

Phospholipid (SAPL). Studies demonstrating that LGP could adsorb or otherwise

bind to the articular cartilage surface have also been performed. These showed that

14% of the LGP molecule could actually adsorb to the cartilage surface (Swann,

Hendren et al. 1981). It would seem rather coincidental that these amounts were

very nearly the same suggesting that LGP (Lubricin) may in fact be a carrier for the

active lubricating ingredient (SAPL) , rather than the lubricant per se (Schwarz &

Hills 1998).


15

Other published works, for example (Tsukamoto, Yamamoto et al. 1983), have

shown that the coefficient of friction does not correlate with the concentration of

the common proteins, globulin and albumin, in synovial fluid. Also there is no

correlation between the coefficient of friction and the concentration of hyaluronic

acid. This means that the lubricating properties of synovial fluid depends upon

other substances (Gavrjushenko 1993). Attention has therefore turned to lipids

which are widely distributed in the body. The lubricating ability of lipids is

attractive because lipids have good solubility in SF and the supply is practically

inexhaustible.

Almost all studies concerning lubrication of the joint have ignored the lipids,

despite the oily nature of the cartilage surface and the presence of lipids in the

synovial fluid in concentrations comparable to that of the polysaccharides and

proteins. One exception to this is the study by (Little, Freeman et al. 1969) who

found that rinsing the cartilage surface with a lipid solvent increased friction, i.e.

the value of µ by 500%. However, the work involving lipids and their role in joint

lubrication appeared to cease at this point. At least a decade later, Hills reignited

interest in the field by suggesting that the surfactant identified in the lung may have

lubricating abilities in many other locations in the body. More recently interest has

grown in the area with several groups researching the role of lipids in lubrication

(Gavrjushenko 1993; Williams III, Powell et al. 1993; Craig & LaBerge 1994;

Higaki, Murakami et al. 1997; Saikko & Ahlroos 1997; Stachowiak & Podsiadlo

1997; Pickard, Fisher et al. 1998; Ethell, Hodgson et al. 1999; Bell, Tipper et al.

2001; Nitzan 2001; Kawano, Miura et al. 2003; Gale, Chen et al. 2006; Gale,

Coller et al. 2007).

Considering the work of Little et al (1969) in light of the work of Radin, Swann

and their co-workers raises the possibility that a form of lipid is involved in the

lubrication of the articular surface and that the glycoprotein is simply the carrier for

the highly insoluble lubricating component. This was confirmed by work done by

(Schwarz & Hills 1998).


16

The equivalent lubrication system used in industry, i.e. solid to solid rubbing, uses

a monolayer of surfactant. Surfactants readily adsorb to surfaces rendering

hydrophilic surfaces more hydrophobic. Interestingly, the articular surface is

hydrophobic, a property readily demonstrated by measuring the contact angle

occurring when a droplet of saline is placed upon the cartilage surface. If a

component of synovial fluid were a surfactant, a surfactant might actually be

responsible for the lubricity under load of synovial fluid and the articular surface.

Indeed, a major portion of the lipid component of synovial fluid is phospholipid

(Rabinowitz, Gregg et al. 1984). Phospholipids are well known for their surface-

activity and have the capability of readily rendering a surface hydrophobic.

Phospholipids also provide values for µ equivalent to the very low values obtained

by rubbing cartilage on cartilage (Hills 2000). Moreover, phospholipids are also

recognised as possessing substantial load bearing abilities.

2.2 Tribological aspects of prostheses

When prostheses are introduced into the human body and relative motion of the

components are involved, the rheological and tribological features of the material,

the prosthesis and the body’s fluids become important. Examples include the wear

of some heart valves, fretting corrosion of plates and screws, and the friction and

wear characteristics of human joints.

The hip joint has received the most attention and it has been estimated that there

are over one million operations each year the world over (Bowsher & Shelton

2001). A variety of materials and designs have been witnessed in the developments

which have led to the present position. There are three major forms of material

combinations; metal-on-metal, ceramic-on-ceramic and metal-on-plastic. The first

is tribologically undesirable under most circumstances and engineering bearings in

which contact and sliding occur usually consist of a soft bearing material and a

relatively hard metal. However, in the environment of the body, corrosion might

readily occur if dissimilar metals are used. Ceramic-on-ceramic has had varied

success and seem to exhibit similar tribological failings as the other combinations

(Jazrawi, Kummer et al. 1998). The metal-on-plastic arrangement is currently most


17

popular, the favourite materials being stainless steel and ultra high molecular

weight polyethylene. In the early stages of development of this form of prosthesis,

the low friction plastic polytetrafluoroethylene (PTFE) or commonly called Teflon

was employed, but the results were disastrous, owing to the high rate of wear of the

softer material. The present combination of materials provides some confidence in

the long-term future of the prosthesis but beyond the 15 year mark is still in

question. It is worth noting that although wear-rate is probably the most significant

tribological feature of artificial joints, friction is fundamentally important to wear.

In engineering a reduction in friction in a bearing will nearly always reduce wear

and guarantee a longer life for the bearing but there are exceptions to the rule, at

least in the body, as mentioned above in regards to the use of PTFE. The short- and

long- term reactions of body tissue to wear particles is also important.

The knee joint probably suffers more from osteoarthritis than the hip, and yet the

development of the knee joint may be still some way behind the development of

the hip joint. The knee lacks the basic stability associated with the hip, the

geometry and motion is more complicated, and the stress levels generally higher.

Hinge joints have been used successfully, but the motion is in many ways an

unsatisfactory substitute for the natural condition, and there are a number of

medical objections to the arrangement. Present designs are more in the form of

replacement linings of the natural bearing materials. In prosthetics, the combination

of metal and Ultra High Molecular Weight Polyethylene (UHMWPE) seem to be

favoured at the present time.

The number of biological subjects in which the science of tribology has made a

contribution to the overall understanding of the problem is extensive and

expanding. Many of the examples are concerned with the common ground between

the sciences of rheology (Ferguson & Nuki 1973), tribology (Nakano, Momozono

et al. 2000) and surface chemistry (Benz, Chen et al. 2005).


18

2.3 Summary

The main aim of biotribology is to understand nature’s treatment of tribology and

use this knowledge to design prosthetic joints with the aim to develop joint

couplings that minimise wear and friction in order to improve the long-term

performance of these prostheses. The lubrication of joints is complex as is the role

of the lubricating factors in synovial fluid and both will receive further discussion

in the subsequent chapters. Three substances have been implicated as the

indigenous lubricating portion of synovial fluid: Hyaluronic acid, Lubricin and

Phospholipids. It has been shown that HA fails to lubricate under any significant

load. Lubricin is a protein and never before has a protein been shown to lubricate.

Lipids in particular phospholipids are known for their lubricating abilities.

Interestingly a portion of Lubricin has been identified as phospholipidic in nature

suggesting that phospholipids are indeed the lubricating fraction of synovial fluid.

Hence, the next stage of research into the lubricating component of the joint

environment would seem to be one of testing for the presence of phospholipids at

the bearing surface. Further evidence supporting a role for phospholipid in the

lubrication of the joint would also open a new avenue of research in the

development of an effective artificial synovial fluid for use in both the natural and

artificial joint.

Chapter 3: Literature Review - Anatomy & Physiology of Diathrodial Joints

19

Chapter 3

Literature Review – Anatomy &

Physiology of Diathrodial Joints

This chapter includes a discussion of the joints themselves, the fluid within the

joint, the disease osteoarthritis and the current remedy, artificial joint replacement.

It will review the materials used in TJRs and discuss the failure of artificial joints.

It should be noted that in an examination of the literature on synovial joints far

more information is available on the natural joint than its replacement. It is an

essential step in engineering to have a sound understanding of the original and the

reasons for failure of the original before designing a replacement.

3.1 Anatomy of the Synovial Joint

Diarthrodial or synovial joints are found at the articulations of the long bones of the

skeleton (hip, knee, shoulder, fingers etc.). Diarthroses refer to the degree of

movement allowed (function) by the joint: freely movable articulations as opposed

to either amphiarthroses (slightly movable articulations) or synarthroses

(immovable articulations). Synovial refers to the structure of the joint: articular

surfaces covered with hyaline cartilage, connected by ligaments and lined by a

synovial membrane to create a joint cavity filled with synovial fluid (Gray 1918).

Synovial joints allow movement between articulating bones. The loads experienced

by synovial joints are complex and variable, exceeding 100 million cycles within a

lifetime without failure. During walking, for example, joints experience high

loading (five to six times body weight) at low surface velocities during heel strike

and toe off and very low loads at maximum surface velocity during swing phase

(Unsworth 1978). This calls for incredible load bearing capacity combined with an

extremely effective lubrication system.


20

The knee is a diarthrodial or synovial joint and the discussion here will detail the

knee even though the proposed study will also include the hip. Essentially, the

following biotribological review applies equally to the majority of synovial joints

including the hip.

The knee consists of three articulations in one: two condyloid joints (Figure 3.1),

one between each condyle of the femur and the corresponding meniscus and

condyles of the tibia (tibiofemoral joint); and a third between the patella and the

femur (patellofemoral joint). (Figure 3.1)

Figure 3.1. Diagram of the structure of the knee. Source: (Mow & Hayes 1997)


21

The articular capsule surrounds the joint, forming the joint cavity, and is a thin but

strong, fibrous membrane. The inner layer of the capsule is the synovial membrane

(Gray 1918). The menisci or semilunar fibrocartilages are found on the articular

surface of the tibia and improve articulation with the condyles of the femur,

enlarging the joint contact area, hence aiding articular cartilage in load transmission

and distribution. When removed, stress in the subchondral bone can be up to 5.2

times higher than when the menisci are present (Fukuda, Takai et al. 2000). A layer

of articular cartilage 1.5 to 3.5 mm thick (Bader & Lee 2000) lines the femoral,

tibial, and patella articulating surfaces.

3.2 Articular (Hyaline) Cartilage

Articular cartilage covers the articulating bone ends of synovial joints forming a

bearing surface that enables the surfaces to resist compression, transmit and

distribute loads and maintain low frictional resistance and wear. Freeman et al

(Freeman, Swanson et al. 1975) stated that the function of articular cartilage is: ‘to

reduce the stresses present in the articulating bone when load is applied to the joint,

to protect the bones from abrasive wear, and to reduce the friction in the joint’.

However, some authors, including Fukuda et al claim that the stress reducing role

of cartilage is only minimal (Fukuda, Takai et al. 2000).

This bearing material has a thickness of between 1 and 5mm, depending upon both

species and location of the joint. It is a porous elastic material with a surface

topography determined largely by the underlying structure of collagen fibres

(Kuettner, Aydelotte et al. 1991). The absence of blood vessels, nerve fibres and

lymphatics as well as basement membranes on either side of the tissue makes adult

articular cartilage unique among connective tissues (Huber, Trattnig et al. 2000). It

is dependent on the diffusion of molecules into the synovial fluid from the well

vascularized synovial membrane for nutrition and the pumping action generated by

the repetitive loading of the joint is essential for sufficient nutrition.

The combination of articular cartilage and synovial fluid provide an almost

friction-free articulation. The biomechanical properties of articular cartilage depend


22

upon the structure of the extracellular matrix, which is composed of collagen fibres

and a well-hydrated ground substance made up of proteoglycans, glycoproteins,

traces of phospholipids and elastin (Kuettner, Aydelotte et al. 1991; Nixon,

Bottomley et al. 1991). The important functional properties of cartilage which

include stiffness, durability and distribution of load, depend on the extracellular

matrix.

3.2.1 The Articular Surface

The articular surface is a thin membrane-like coating of the cartilage matrix. In

electron micrographs it presents as an amorphous, electron-dense layer which at

high magnification shows a particulate and filamentous appearance (Ghadially,

Lalonde et al. 1983) which coats a layer of collagen fibrils. Morphological studies

by Hills have provided visible evidence of oligolamellar phospholipid on the AC

surface (Hills 1989; Hills 1990). Guerra et al reported that the surface of normal

articular cartilage is covered by a discontinuous, mono/multilayered pseudo-

membrane and seems to consist of phospholipids, glycosaminoglycans and proteins

(Guerra, Frizziero et al. 1996). They suggested this membrane-like structure might

have a protecting role in preventing direct contact between the articular cartilage

and toxic agents present in the synovial fluid and/or exert a lubricating effect

within the articular joint. Ballantine also found the same and concluded that a layer

of phospholipids was present on the surface of articular cartilage and that the layer

could clearly be viewed in SEM and OM (Ballantine & Stachowiak 2002). They

suggested that the lipid layer acts as a boundary lubricant and is critically important

to the proper functioning of synovial joints

The surface roughness of the cartilage will be considered briefly from the point of

view of its relevance to lubrication: To the naked eye, the surface appears

glistening, smooth and free from noticeable unevenness, irregularities and

roughness. However, the issue of cartilage surface roughness has been the source of

considerable controversy. Most, if not all observations made with the scanning

electron microscope, whether on cartilage itself (e.g. (Walker, Dowson et al. 1968))

or on cast replicas (e.g. (Dowson, Longfield et al. 1968) show some surface


23

irregularities. Ghadially (1983) explains the presence of surface asperities as

artifacts of tissue preparation; however, there are a number of earlier studies which

describe surface roughness. Davies et al (1962) suggests that the surface is very

smooth, with irregularities in the range of 0.02µm. Dowson et al (1968) and Jones

et al (Jones & Walker 1968) found much greater roughness, which increased with

age. The values ranged from about 1µm for foetal cartilage to about 2.7 µm for

adult cartilage. Further study by Sayles et al reported average roughness between 1

and 6µm (Sayles, Thomas et al. 1979). Today, it is accepted that asperities between

2-6µm are commonly present (Dowson 1990).

3.2.2 Articular Cartilage Matrix

Cartilage is an anisotropic material consisting of cells (chondrocytes) embedded in

an extracellular matrix consisting of water (60 to 80% by weight), proteoglycans

(PGs), collagen, and some glycoproteins (non-collagenous proteins). The

organisation of these constituents varies with depth from the surface within the

same joint and between joints (Broom 1988). The fact that cartilage is aneural,

avascular, and has slow cell turnover rates means it has minimal reparative abilities

(Caplan, Elyaderani et al. 1997). Even when cartilage appears to repair an

osteochondral defect, the repair tissue often has a significantly lower aggregate

modulus and Poisson's ratio and a higher permeability than the surrounding

cartilage. These changes in properties indicate that cartilage repair tissue may not

be hyaline in nature and, therefore, inadequate for long term function in the joint

(Hale, Rudert et al. 1993).

Chondrocytes

Cartilage is maintained by the chondrocytes, the cellular component of the

cartilage, which account for less than 10% of the total volume of the cartilage.

They are responsible for the production of matrix material, hence for growth and

repair of cartilage tissue. Chondrocytes synthesise all of the basic molecular

components of the extracellular cartilage matrix and maintain the tissue via a

balance between anabolism and catabolism of the appropriate molecules. The

surface layers rely on the synovial fluid and matrix water exchange for chondrocyte


24

metabolism and waste exchange. As the joint ages, the population of chondrocytes

depletes and the mitotic activity of the remaining cells decrease. (Ghadially 1978)

Proteoglycans

PGs are large, electronegative macromolecules found within articular cartilage.

These are embedded within the fibrillar network (Figure 3.2) and give articular

cartilage the ability to undergo reversible deformation. They consist of monomers

formed by a protein core with a large number of glycosaminoglycans (GAGs)

attached in a ‘bottlebrush’ fashion (Figure 3.2). These GAG side chains are long,

unbranched carbohydrates and are present within the joint mainly as chondroitin

sulphate and keratin sulphate. Proteoglycans are space-filling within the tissue and

show specific interactions with the extracellular cartilage matrix (Comper &

Laurent 1978; Greenwald, Moy et al. 1978; Neame & Barry 1994).

The GAG side chains are linear polymers composed of repeating dimers

(disaccharides). The disaccharide unit contains one or two negatively charged

groups which, when formed into chains of 50-70 dimeric units as is found in a

proteoglycan molecule, represent strongly repelling chains that extend stiffly from

the protein core (Nixon, Bottomley et al. 1991). As highly negatively charged

macromolecules, proteoglycans attract water creating a “hydration sheet” that gives

the cartilage stiffness and compressibility. Upon loading, the proteoglycan

aggregates are compressed and water is expelled from the tissue thus increasing the

negative charge density which in turn increases the resistance of water flow until

equilibrium between loading forces and swelling pressure is reached. Removal of

the load allows the water to return, with nutrients, and the proteoglycan monomers

swell to their former volume. Swelling is restricted to about 20% of its maximum

by the collagen fibrillar network (Maroudas & Bullough 1968; Maroudas 1976;

Maroudas & Venn 1977; Muller, Pita et al. 1989; Nixon 1991). Damage to the

collagen network restraining the proteoglycan hydration shell allows the cartilage

to swell with water. This is one of the early recognised changes in degenerative

joint disease or osteoarthritis.


25

On one end of the PG is a small hyaluronic acid (HA) binding region. This allows a

large number of PGs to interact with a single HA chain forming PG aggregates

(Figure 3.2). The PG-HA complex is stabilized by link proteins. (Muir 1980)

Figure 3.2: Schematic of a proteoglycan molecule and schematic of a

proteoglycan aggregate (Bader & Lee 2000)

Collagen

Collagen fibres are responsible for the structural element of the matrix, forming a

three dimensional fibrillar network of rope-like molecular aggregates which is

arranged with specific orientation in the various zones related to function of the

bearing surfaces. Trapped in this fibre network are macromolecules formed by

proteoglycan aggregates (fig. 3.2). These consist of proteoglycan sub-units attached

to hyaluronic acid molecules. Collagen provides the cartilage with tensile stiffness

and strength. The property of compressive stiffness is supplied by the

proteoglycans. (Mow, Kuei et al. 1980; Kuettner, Aydelotte et al. 1991; Nixon

1991).

Collagen accounts for approximately half the dry weight of articulate cartilage

(Muir 1980) and about 15 to 20% of the wet weight (Bader & Lee 2000). The

predominant collagen within articular cartilage is type II. Orientation varies

throughout the thickness and over the articular surface.

Collagen type II comprises 90-95% of articular collagen forming cross-banded

fibrils and fibres intertwined throughout the matrix. The remainder is made up of a

combination of at least five other types of collagen (Eyre, Wu et al. 1987; Kuettner,


26

Aydelotte et al. 1991). Collagen fibres show some organisation in the surface

layers of the articular cartilage, tending to be tightly packed and orientated parallel

to the cartilage surface. Those in the deeper layers tend to be roughly perpendicular

but on the whole are reasonably random (Nixon, 1991). The collagen fibrillar

network is essential for maintaining the volume and shape of the tissue. The ability

to provide the cartilage with tensile strength is enhanced by the presence of

crosslinks between the cartilage molecules (Mow, Fithian et al. 1988).

Figure 3.3: Schematic of the Hypothetical Layers of Articular Cartilage

(Black & Hastings 1998)

Structure

Cartilage can be broken down into four hypothetical layers or zones (Glenister

1976) illustrated in Figure 3.3. The superficial or tangential zone (5-20% of full

cartilage thickness) is closest to the joint surface and consists of tightly packed

collagen fibers orientated parallel to the joint surface. The orientation of these

fibers can be determined or mapped using the split-line technique. This entails

pricking the surface of the cartilage with a pin. The cartilage will then split along

the direction of the dominant fiber orientation. The fiber orientations are thought to

be aligned in the direction of the most dominant stress experienced under

physiological loading. (Mow, Fithian et al. 1988) The chondrocytes in the

superficial layer are oval in shape with their long axis parallel to the joint surface.

The superficial layer contains the smallest PG content and the highest water

content. (Meachim & Stockwell 1974)


27

The intermediate or transitional zone makes up about 40-60% of the cartilage

thickness. It contains an interlacing network of collagen fibers which are more

widely spaced and more randomly orientated with respect to the cartilage surface.

The chondrocytes in this zone are spherical and more abundant. This layer has a

higher PG content and lower water content. (Meachim & Stockwell 1974)

The deep or radiate zone is approximately 30% of the cartilage thickness. It has a

tighter meshwork than the intermediate zone with the collagen fibres having a

radial orientation; that is, they run perpendicular to the joint surface (Meachim &

Stockwell 1974). Broom (Broom 1988) has proposed that the fibres are not

straight; rather, each radially aligned fibre has repeating lateral deflections along its

length. This allows neighbouring fibres to overlap or crosslink, forming a three-

dimensional network capable of entrapping the much higher content of PGs. The

chondrocytes in the deep zone are spherical and are arranged in columns. The deep

zone has the lowest water content. (Meachim & Stockwell 1974)

The deep and calcified zone are separated by the ‘tidemark’ (Fig 3.3). The calcified

zone consists of a few cells imbedded in a matrix containing calcium salt crystals.

(Meachim & Stockwell 1974) The bundles of collagen in this zone are radially

aligned and serve to anchor the cartilage to the underlying subchondral bone.

(Meachim & Stockwell 1974)

3.2.3 Response to load

The cartilage matrix has a sponge-like structure and much of the water within this

structure is free to move when under compression. The effective pore size of the

matrix is only small, in the range of 20A to 65A (McCutchen 1962; Dowson,

Wright et al. 1969), and the permeability is low.

Cartilage is poroelastic or porohyperelastic at low rates of loading and viscoelastic

at high rates of loading and under impact load (McCutchen 1982). Under a rapidly

applied load, cartilage shows an initial elastic response followed by a poroelastic,

time-dependent creep response. This creep response is thought to be dependent on


28

the PG content, but unrelated to the collage content as it represents the gradual loss

of fluid which is governed by the strength of the PGs’ resistance to water loss.

After the removal of the compressive load, cartilage displays a recovery phase.

The ability of articular cartilage to carry large loads during physiological activity is

highly attributed to its unique structure. The superficial layer of cartilage serves a

strain-limiting function. As a compressive load is applied, a tensile force is formed

over the surface of the cartilage and is resisted by the tangentially aligned collagen

fibres. The intermediate and deep zones are responsible for the resistance of

compressive forces. The entrapment of PGs within the network of collagen fibres

causes the formation of an osmotic pressure due to the PGs affinity for water and

their repulsion between each other. The collagen fibres resist this pressure,

resulting in a stiff, highly structured gel system. As load is applied, the initial

response is elastic, with the load fully carried by the fluid component as the

pressure within the cartilage increases. Once the pressure reaches a maximum, a

pressure gradient is formed and there is a continuous flow of fluid out of the

cartilage. The pressure, which was carried by the fluid component, gradually

transfers to the deforming collagen network. This process represents the time-

dependent behaviour of articular cartilage. As the pressure is transferred, a new

equilibrium is reached and no fluid flow occurs. The load is fully supported by the

collagen network, displaying viscoelastic behaviour. When the load is released, the

pressure equilibrium is disturbed and there is a fluid influx until the fluid osmotic

pressure balances the constraining pressure of the collagen network; that is, the

cartilage deformation is fully recovered. (Freeman & Meachim 1974)

What an engineer must consider here is the flow of basically water through a filter

with a pore size smaller than 65A.

3.3 Synovial Membrane

Synovial membrane (or synovium) lines the inner surface of the joint capsule and

covers all intra-articular structures with the exception of the articular cartilage and

menisci. Its functions are: (1) the production of synovial fluid and (2) the removal


29

of synovial fluid and debris from the joint space. On gross inspection the

membrane is smooth and shiny, but under the light microscope microvilli are

apparent. These folds permit the expansion of the synovial membrane in response

to joint movement or to changes in intra-articular pressure (Jayson & Dixon 1970;

Nitzan, Mahler et al. 1992; Lu, Levick et al. 2005). It is a metabolically active

tissue and, as such, requires adequate nutrition and removal of waste products. The

synovial membrane is comprised of: (1) a lining layer adjacent to the joint space

which is called the synovial intima and (2) a supportive or backing layer called the

sub-synovial tissue or subintimal tissue. On its external surface the subintimal

tissue merges with the fibrous capsule of the joint (Ghadially, Lalonde et al. 1983).

3.3.1 The Synoviocytes

The cells of the synovial intima are known as synoviocytes. There are two main

types: ‘Type A’ and ‘Type B’ synovial cells. The two main functions of the

synoviocytes are the removal of debris from the joint space and the synthesis of

glycosaminoglycan and hyaluronic acid (3.4.1.) (Henderson & Pettipher 1985).

The Type B cell is well endowed with rough endoplasmic reticulum- an organelle

prominent in cells that produce a protein rich secretion (Ghadially 1983), therefore

it can be argued that the Type B cells must produce a protein rich secretion, the

composition of which has many possibilities as listed below:

(1) the small amount of protein in the synovial fluid which is firmly bound to

hyaluronic acid

(2) procollagen and collagen (in culture Type B cells have been shown to produce

types I and III) (Fox, Lotz et al. 1989)

(3) collagenase and plasminogen activator (Ghadially 1983)

(4) c2 macroglobulin (Glynn 1977)

(5) Lubricating glycoprotein-1 (Lubricin) (Ghadially 1983)

(6) glycosaminoglycans (hyaluronic acid, chondroitin sulfate and dermatan sulfate)

(Fox, Lotz et al. 1989)

(7) Fibronectin (Scott & Walton 1984)


30

3.3.2 Removal of Substances from the Joint Space

Secretion of the synovial fluid cannot continue indefinitely into a cavity of finite

size, like the joint cavity, without a corresponding removal of material. The

presence of micropinocytotic vesicles and pinocytotic vacuoles in the synovial

intimal cells indicates the uptake of fluid from the joint space (Ghadially 1983).

The absence of a basal lamina and the presence of lymphatics and fenestrated

capillaries must all facilitate exchange from the joint cavity. Clearance of

substances injected intra-articularly has also been studied, clearly demonstrating

the exchange between plasma and the joint space (Levick 1987; 1989; Levick

1995). Studies using the electron microscope have demonstrated the uptake of

particulate matter from the synovial fluid by the synovial intimal cells (Ghadially

1983).

3.3.3 The Synovium in Disease

The changes in structure and function of the synoviocytes associated with repeated

trauma, infection, metabolic imbalance or deposition of immune complexes lead to

the production of synovial fluid with altered characteristics. This may contribute to

the development of degenerative and inflammatory joint disease (Tew 1980;

Walker, Boyd et al. 1991; Rorvik & Grondahl 1995). In osteoarthritis and

rheumatoid arthritis, the turnover of the synoviocytes increases and there is both

hypertrophy and hyperplasia of synoviocytes. There may be ulceration of the

synovial surface, proliferating fibroblasts and other histologically-evident changes

(Henderson & Pettipher 1985; Fox, Lotz et al. 1989).

3.4 Synovial Fluid

Synovial fluid is a clear, pale yellow, highly viscous liquid with non-Newtonian

flow properties which occurs in small quantities in normal joints. It occupies a key

position in the function and well-being of the joint and is responsible for the

lubrication and nutrition of the joint tissues. This is nature’s provision of a

lubricant in the joint and must be well understood by the engineer if he is to


31

provide a suitable solution to the failure of the synovial joint. The specific volume

and composition of synovial fluid varies from joint to joint even within the same

species and sometimes within the same animal (Smith, Habermann et al. 1979;

Currey, Unsworth et al. 1981). The volume of normal SF in the knee joint is

estimated to be 0.5 to 2 ml (Yehia & Duncan 1975).

3.4.1 Synovial Fluid Composition

By understanding the constituents of SF, engineers can utilise this information in

designing suitable implants for the joint and the selection of biomaterials that will

function best. It is essential to consider the environment the implant will be

exposed to and that the material selected will not cause an adverse reaction with the

body and conversely that the body does not have an adverse reaction on the

implant. More so to understand what constituents will work with the biomaterial

and what constituents won’t and vice versa.

Synovial fluid is essentially a dialysate of plasma with the addition of hyaluronic

acid which is locally synthesised by the synovial cells. The total protein

concentration of synovial fluid is lower than that in plasma, although some

individual proteins are present in higher quantities than in plasma (Weinberger &

Simkin 1989; Simkin 1991; Prete, Gurakar-Osborne et al. 1993). The protein

content of SF is about 20 mg/ml (2 %) and the proteins of SF are identical with the

proteins of blood plasma. Several of the synovial fluid constituents are unique to

the synovial fluid and are either synthesised in the synovial membrane or are a

result of catabolism within the articular cartilage and other structures associated

with the joint. The constituents of synovial fluid will be considered as groups of

substances based on their origin:

I. Constituents derived from the blood

II. Substances secreted by the synovial membrane

III. Products derived from the catabolism of the joint.

I. Constituents Derived from the Blood


32

The major constituents of the synovial fluid are derived directly from the blood.

The path for direct fluid exchange between plasma and the synovial fluid comprises

the capillary endothelium and interstitial spaces between synoviocytes (Knight &

Levick 1983). The degree of permeability of the capillary walls is believed to limit

the molecular size of components reaching the synovial fluid. Small molecules

such as ions and non-electrolytes diffuse freely between plasma and synovial fluid

via the large vascular network in the synovium. As a result of this direct exchange,

the concentrations of these solutes in both fluids is almost identical.

Glucose is one of the most important nutritional requirements of the chondrocytes

(Simkin 1993; Levick 1995). The concentration of glucose in synovial fluid is

usually close to that of plasma. Between 3 to 4 hours following a meal, levels have

regularly been found to be higher in the joint space than in the perfusing blood

(Ropes, Muller et al. 1960), leading investigators to suggest that there might be a

specific glucose transfer system. Most small molecules move freely in both

directions between plasma and synovial fluid in accord with simple diffusion

kinetics. Glucose, however, enters the joint more rapidly than would be expected

from its size, but its rate of return to the plasma is unaffected (Simkin 1993).

Proteins do not equilibrate between plasma and synovial fluid (Ropes, Rossmeisl et

al. 1939). Their distribution in synovial fluid is primarily due to capillary selective

permeability and the size of the molecules that can permeate the synovial

membrane. The concentration of total proteins in normal synovial fluid varies from

joint to joint and is approximately one-third of the protein concentration in serum

(Weinberger & Simkin 1989). Synovial fluid contains many of the lower molecular

weight proteins such as albumin, globulin, and seromucin (Currey, Unsworth et al.

1981). Proteins with molecular weights exceeding 160 000, such as fibrinogen,

macroglobulins and lipoproteins, are found in trace amounts only (de Medicis,

Reboux et al. 1976).

Fat soluble solutes can diffuse easily both through and between cell membranes, so

they do not face the same restrictions as the hydrophilic molecules. The entire

surface area of the synovium is available for the diffusion of these molecules.


33

Physiologically, the most important of these are the respiratory gases: oxygen and

carbon dioxide (Simkin 1993). Lipophilic molecules tend to accumulate in fatty

tissues and are eluted slowly by the surrounding interstitial water (Prete, Gurakar-

Osborne et al. 1993).

Normal synovial fluid contains few cells and there are no erythrocytes or platelets

present. Mononuclear cells such as modified macrophages and synovial cells are

the predominant cell type. The average number of cells per mm3 is reported to be

63 (Currey, Unsworth et al. 1981). The mononuclear phagocytes are probably

present in order to remove wear debris and particulate matter from the synovial

fluid.

II Constituents derived from the Synovial Membrane

Although the source of these constituents has already been discussed, the structure

and role of hyaluronic acid will be covered further:

Hyaluronic Acid

Hyaluronic acid (HA) is the major secretory product from the synovial membrane.

It is a glycosaminoglycan of high molecular weight which confers the

viscoelasticity and shear thinning behaviour of synovial fluid. The viscosity of the

synovial fluid is directly related to the concentration of HA (Ogston & Stanier

1953) which is about 2 to 3 mg/ml in the normal human living knee (Balazs 1968).

In some inflammatory disease states where the volume of synovial fluid is greatly

increased, the viscosity is correspondingly decreased due to the reduction in HA

concentration. It is suggested that the concentration of HA in synovial fluid is

passively equilibrated with its concentrations in the synovial tissue (Henderson,

Revell et al. 1988). HA is rapidly removed from the joint cavity through the

lymphatic pathways. It is then taken up from circulation and metabolised by

endothelial cells in the liver sinusoids and the lymphatic tissue (Fraser & Laurent

1989). The factors controlling HA synthesis and turnover in the synovial space are

still the subject of investigation (Fraser & Laurent 1989; Momberger, Levick et al.

2005).


34

III Constituents derived from the Catabolism of Joint Tissues

The articular cartilage matrix is basically composed of collagen and proteoglycan.

These two components are constantly being turned over throughout the life of the

cartilage (Mankin & Lippiello 1969; Lohmander 1988). The protein core of the

proteoglycans may be cleaved by proteases and as a result, proteoglycan fragments

may be released into the synovial fluid (Sandy, Brown et al. 1978). These are taken

up by the afore-mentioned phagocytic cells. Chondroitin sulphate, a

glycosaminoglycan, is present in small amounts in normal synovial fluid due to the

turnover of the matrix proteoglycans (Swann 1978).

3.4.2 Production of Synovial Fluid

It has already been noted that most of the components of synovial fluid are derived

from the blood, presumably by a process of simple diffusion through the synovial

membrane, without intervention of cellular activity or active transport mechanisms.

However, the presence of hyaluronic acid and proteins, other than those found in

plasma, (and their degradation products) cannot be explained by the above scheme.

Hyaluronic Acid

Studies including light microscope and histochemical work have been used to try to

identify the source of these ‘extra’ components of the synovial fluid. It would

appear that conclusive evidence supporting the role of Type B cells in the synthesis

of hyaluronic acid is still lacking, although it has been clearly illustrated that the

intact synovium synthesises hyaluronic acid (Yielding, Tomkins et al. 1957; Myers

& Christine 1983).

Protein

Most proteins in synovial fluid are filtered across the synovial membrane directly

from the circulating blood. Normal synovial fluid from the human knee contains

13g of total protein /l00ml (2.9% of wet weight), a large quantity of the protein

being albumin (Rabinowitz, Gregg et al. 1984; Simkin 1993). Between 10% and

30% of the proteins in synovial fluid are loosely associated with hyaluronic acid

(Balazs 1968), these are believed to be derived from the blood. However, 2% of the


35

protein is firmly bound to the hyaluronic acid, is different from plasma protein and

is probably of synovial origin (How, Long et al. 1969).

Another protein apparently unique to the synovial fluid is the lubricating

glycoprotein, proposed to be the boundary lubricant for the cartilage, which

constitutes around 0.5% of the total protein in synovial fluid and is absent in serum

(Swann & Radin 1972). Little is known of the synthesis of this protein, although it

is clear that it is not produced in the articular cartilage. In vitro cultures of cells

from the synovial lining have produced a molecule resembling this glycoprotein

(Ghadially 1983).

3.4.3 Functions of Synovial Fluid

The functions of synovial fluid lie largely in two areas:

I. Nutrition to the avascular cartilage.

II. A role in lubrication of the synovial joint, including load bearing and

shock absorption.

I Nutrition

As previously noted, the articular cartilage is avascular and it must depend largely,

if not entirely, on diffusion from the synovial fluid for nutrition (Maroudas 1976;

O'Hara, Urban et al. 1990). In immature animals, before calcification is complete

and there is closure of the subchondral plate, the deeper parts of the cartilage may

receive some nutrition from blood vessels in the marrow space (McKibbin &

Maroudas 1979; Mankin & Brandt 1984). The transport of nutrients and the

removal of the by-products of metabolism is believed to be assisted by the

movement of fluid in and out of cartilage in response to cyclic loading of the joint

tissues known as ‘pumping” (Mankin & Brandt 1984; O'Hara, Urban et al. 1990).

Joint motion is not considered to be important for the supply of nutrients of low

molecular weight, such as oxygen and glucose to the cartilage. However, as the

molecular weight of solutes increases, simple diffusion of the solute becomes more

difficult and the influence of convection becomes more important. Pumping may


36

assist the transport of substances such as enzyme inhibitors or hormone carrier-

proteins through the matrix. It has also been thought that the value of joint motion

is to stir the bulk liquid and reduce the stagnant “boundary layer” over the cartilage

surface (Maroudas & Bullough 1968).

II. Lubrication

The synovial fluid has a role in maintaining good lubrication between the opposing

cartilage surfaces and also between the soft tissue structures within the joint cavity.

Lubrication of the cartilage surfaces will be dealt with thoroughly in chapter 4 and

will receive no further discussion here. However, soft tissue lubrication warrants

some discussion here. It is generally believed that the hyaluronic acid component

of synovial fluid is responsible for soft tissue lubrication (Radin, Paul et al. 1971;

Swann 1978). In this location, the hyaluronate experiences considerably lower

loads than at the cartilage surface. This enables the polysaccharide to lubricate the

soft tissues, such as the synovium and the tendons, most effectively. Lubrication of

these soft tissues is probably via the boundary mechanism (Radin, Paul et al. 1971;

Swann, Radin et al. 1974). Alternatively Wright et al present evidence for a

hydrodynamic mechanism in the lubrication of the synovial membrane and stress

the importance of the viscous properties of the synovial fluid (Wright & Dowson

1976).

3.4.4 Rheology of Synovial Fluid

When the viscosity of a fluid is independent of the rate of shear to which it is

subjected it is said to be “Newtonian”. Synovial fluid (SF) is highly non-Newtonian

(McCutchen 1966), as the rate of shear increases, the viscosity decreases greatly

(shear thinning) and, as the rate of shear decreases, the viscosity increases.

Hyaluronic acid is responsible for the viscosity of the SF. More precisely, SF is

thixotropic and the viscosity is time-dependent, resulting in different maximum and

steady-state values. Synovial fluid also exhibits an elastic response, producing non-

zero normal force differences under load (Caygill & West 1969). The rheological

properties of both the cartilage, as mentioned earlier, and the synovial fluid are

responsible for optimal lubrication. The viscoelastic properties of the synovial fluid


37

also play an important role in maintaining continual effective lubrication (Schurz &

Ribitsch 1987). These properties facilitate a high rate of motion, but also lead to a

thin film of fluid at high speeds (Hamerman, Rosenberg et al. 1970) and, as

discussed in section 4.2.1., this presents a number of problems in the development

of lubrication theories for the joint, especially with respect to the size of cartilage

asperities.

The viscosity is little more than twice that of water under the same conditions. The

lubricant is more akin to water than to mineral oil or silicone fluid as far as

viscosity is concerned (Dowson 1990).

3.4.5 Synovial Fluid Lipids

This component of synovial fluid will receive specific attention because (1) its

source in the normal healthy joint is not clear and discussion of this component is

frequently omitted from reviews on synovial fluid composition; and (2) lipids,

specifically the phospholipids of the synovial fluid, have been implicated in the

boundary lubrication of the joint (Hills 1988; 1989; Hills 1990; Gavrjushenko

1993; Williams III, Powell et al. 1993; Craig & LaBerge 1994; Higaki, Murakami

et al. 1997; Saikko & Ahlroos 1997; Pickard, Fisher et al. 1998). As discussed,

synovial fluid is considered to be a filtrate of plasma combined with HA which is

synthesised locally and most biochemical investigations of synovial fluid have

focused on the protein and polysaccharide constituents. Because of the

comparatively low concentrations of lipid components in normal synovial fluid and

the general lack of interest in their clinical significance, (Wise, White et al. 1987)

little attention has been devoted to their discussion.

Lipids constitute 2 mg/ml of the wet weight of synovial fluid of a healthy human

knee joint (Rabinowitz, Gregg et al. 1979). Neutral lipids make up 67.5% of the

total synovial lipids and the remainder is phospholipid (Rabinowitz, Gregg et al.

1984). Studies on the lipid content of synovial fluid (Bole & Peltier 1962; Chung,

Shanahan et al. 1962; Rabinowitz, Gregg et al. 1984) clearly show

dipalmitoylphosphatidylcholine (DPPC) to be the predominant phospholipid


38

present (14.8% of total lipid). Phosphatidylethanolamine, phosphatidylserine,

phosphatidylinositol and sphingomyelin are also present in synovial fluid (Hills &

Butler 1984; Rabinowitz, Gregg et al. 1984). Lipoprotein levels in synovial fluid

average 40% of those found in serum (Small, Cohen et al. 1964).

The source of these synovial lipids in the normal healthy joint is not clear (Prete,

Gurakar-Osborne et al. 1993) as lipids (lipoproteins) appear to be prevented from

freely entering the synovial cavity (Bole & Peltier 1962). Following trauma, such

as a fracture or soft tissue damage, the level of lipid droplets (largely triglycerides)

in the synovial cavity increase dramatically (Rabinowitz, Gregg et al. 1984; Wise,

White et al. 1987). Conversely, the levels of phospholipids decrease considerably

(Rabinowitz, Gregg et al. 1984). If phospholipid is the boundary lubricant (4.2.5.3

& 5.6) for the joint this may have implications for the development of osteoarthritis

or degenerative joint disease following trauma.

3.4.6 Synovial Fluid in Disease

As already mentioned, SF shows a reduction in viscosity with disease and the lipid

concentration is also affected. Some diseases reduce the viscosity of the SF and

eventually it becomes independent of the shear rate. This is caused by the reduced

concentration of the hyaluronic acid in the pathological SF (Yehia & Duncan

1975). However, the lubricating ability does not seem to be greatly affected

(Swann, Bloch et al. 1984). Only 20 out of 180 diseased joints showed a reduction

in lubricating ability. SF from OA joints is far more Newtonian in its

characteristics (Dumbleton 1981). The question is raised in respect to joint fluid

lubrication: in what way is the function and nature of the joint fluid altered in the

presence of disease and is the change a cause or effect of the pathological

condition? Essentially, little work has been carried out on the nature of joint fluid

around artificial joints and the role of the synovial fluid in artificial joints.

3.5 Osteoarthritis

There are more than 100 different types of arthritis, and the cause of most is

unknown. Arthritis causes pain, stiffness, and sometimes swelling in or around


39

joints. Arthritis is a complex collection of diseases that may have different causes

but result in the same outcome. Arthritis is a common disorder in all populations

and often results in disability or activity limitation and eventual loss of mobility

(Felson 1998).

Osteoarthritis, or degenerative joint disease (DJD), is one of the oldest and most

common types of arthritis. Osteoarthritis affects the quality of life of hundreds of

millions of people the world over. Osteoarthritis is a disease of the synovial joint.

The term osteoarthritis is the name this disease is well known by, but it is

somewhat technically and pathologically incorrect. Osteoarthritis refers to a

primarily inflammatory problem, which is not the case. The pathogenesis described

below is the end result of multiple injuries to the joint surface with minor

inflammation to the joint capsule also occurring. The more accurate term for this

disease is osteoarthrosis (OA), implying primarily a degeneration of the joint. This

thesis, however, will continue to use the common term of osteoarthritis or OA.

OA can affect all synovial joints of the body either singly or in combination but

most commonly affects the load bearing joints of hips and knees. It is

characterized by the breakdown of the articular cartilage and the eventual loss of

articular cartilage from all or a portion of the joint surface. The disease not only

affects the cartilage, but also has ruinous influence on the subchondral bone, joint

capsule, synovial membrane, and even surrounding ligaments and muscle. (Flores

& Hochberg 1998). The cartilage breakdown causes bones to rub against each

other, causing pain and loss of movement. As the cartilage continues to degenerate,

changes occur in the underlying bone, which becomes thickened with the formation

of bony growths from the bone surface called bone spurs. Fluid-filled cysts may

form in the bone near the joint. Bits of bone or cartilage can break off into the joint

space and irritate soft tissues, such as muscles, and cause problems with movement.

Much of the pain is a result of the increased load on muscles and the other tissues

that help joints move, which is a result of the damage to the cartilage. Cartilage

itself does not have nerve cells, and therefore cannot sense pain (inflammatory), but

the muscles, tendons, ligaments and bones do. The synovium becomes inflamed as

a result of the arthritic cartilage. This inflammation leads to the production of


40

cytokines (inflammatory proteins) and enzymes that may damage the cartilage

further.

While it is widely accepted that end stage OA is represented by full thickness loss

of articular cartilage, early OA is much more ambiguous. Osteoarthritic

degeneration progresses through four phases as the cartilage damage becomes more

severe; these grades of degradation are explained by Marcinko (Marcinko &

Dollard 1986). In Grade I, surface and subsurface damage are minor, and limited to

small fissures and pits. The damage can be observed only at points of highest stress

and the rest of the joint functions normally. In Grade II, more severe cartilage

damage can be seen, though the damage is still confined to the areas of greatest

loading. Some cartilage loss can occur in this stage. Grade III of the degradation

marks the complete loss of cartilage in heavily loaded areas and possibly the

formation of bony growths. Pain in the joint would typically begin during this

stage. Grade IV is the most severe level of degradation; in this end stage, large

areas of bone may be completely exposed. The surfaces of the bone can become

misshapen and the articular surfaces become irregular (Marcinko & Dollard 1986).

The causes of osteoarthritis have been subject to a number of theories. Several

theories are related to trauma in the joint resulting from injury (Panush 1990;

Buckwalter & Lane 1997; Jay, Elsaid et al. 2004). Other theories suggest that OA

is just a ‘wear and tear’ form of arthritis. Yet other theories point to genetic factors

involved in OA that can predispose the patient to or produce osteoarthritic lesions

(Neame, Muir et al. 2004). Risk factors for OA are many and varied, single or

multiple, and include: age, sex, obesity, height, genetic influences, socio-cultural

influences (nutrition, sitting habits etc.), exercise levels, joint injury, existing

diseases (for example, osteoporosis), congenital factors etc. (Felson 1998; Wildner

& Sangha 2000)

It has not yet been determined exactly which mechanism causes OA or what is the

initial trigger. It is likely that there are multiple pathways. Continuing efforts of

research are being made to gather more information about the early stages of OA

and the chain of events that occur during the progression of the disease.


41

From an engineering perspective, when considering the failure of bearings, with

failure due to overload (i.e. trauma) aside, nearly all bearing failures can be traced

to a lubrication deficiency. Indeed, one of the models proposed for the pathogenesis

of OA is that the joint fails because of a lubrication related issue (Davis, Lee et al.

1978; Marcinko & Dollard 1986; Batchelor & Stachowiak 1996).

3.5.1 Treatments of Osteoarthritis

Few treatments exist for osteoarthritis patients. Part of the difficulty in treating

OA results from the difficulty in diagnosing the disease early; the pain and stiffness

associated with later stages (Grades III and IV) of the disease are not generally

evident until much cartilage damage has occurred. Attempts to slow the

progression of osteoarthritis have been made using nutritional and pharmaceutical

supplements, physical therapy, and other approaches. Some common treatments are

weight control, pain-control medicine, and hot/cold therapy. These treatments have

been shown to reduce pain, but do little to stop the progression of the disease and

cannot reverse its effects (Furey & Burkhardt 1997).

Weight loss and physical therapy are generally prescribed to treat mild OA.

Traditionally more advanced OA is treated with non-steroidal anti-inflammatory

drugs (NSAIDS) until the drugs no longer provide relief from pain at which point

the treatment usually progresses to surgery. While NSAIDS are the most

commonly prescribed medications for OA, they do not seem to alter the natural

course of the disease and they produce significant gastrointestinal side effects.

There are a growing number of non-traditional approaches being used throughout

the world. In Europe and Asia, glucosamine and chondroitin sulfate (GCS) have

long been used to treat arthritis. Glucosamine is a constituent of

glycosaminoglycans (GAGs) and proteoglycans that are naturally found in cartilage

and synovium. It is also a building block for hyaluronic acid, which forms the

backbone of the proteoglycans embedded in the articular cartilage. Chondroitin 4-

and 6-sulfates are the main GAGs of articular cartilage (Buckwalter 1983). In


42

theory, by providing the building blocks for healthy articular cartilage, the joint

will be able to repair and regenerate cartilage, but this ability of chondroprotection

is unproven. It is worth noting that there is no single treatment that works for the

entire affected population but that certain treatments do seem to help some

individuals.

Another non-surgical treatment for OA is intraarticular injections of hyaluronic

acid (HA) known as viscosupplementation (VS). Balazs (Balazs 1968) has

advocated the use of artificial synovial fluid since the 1960’s and is truly a pioneer

in the field. VS is a procedure in which a hyaluronic acid derivative is injected

directly into the affected joint. The goal of viscosupplementation is to recreate the

environment of a healthy joint in an effort to encourage the joint to escape the

negative feedback cycle of OA progression. Once normal viscoelastic properties

are returned to the joint fluid, the joint will increase production of healthy synovial

fluid. Initially the mode of action is mainly mechanical, but it is suspected that

additional biologic benefits are eventually levied. The half-life of the injected fluid

is only a few days. Therefore after one week there is no longer a significant amount

of artificial fluid in the joint. However, clinical studies have shown that the benefits

of viscosupplementation can last from 6 months up to a year after the last injection

(Wobig, Dickhut et al. 1998). It is believed that because of the transient nature of

the HA within the joint, it is not actually the restoration of joint viscosity that is the

cause of the noted changes (Brandt, Smith et al. 2000). More likely, the benefits

observed in VS are due to interactions on the molecular level between the HA and

pain receptors in the joint. However, since the cause for the initial onset of arthritis

is not addressed (subchondral sclerosis, varus/valgus deformity, obesity etc.) the

benefits of viscosupplementation are not and may never be long term. From an

engineering perspective the idea is good; renewal of the lubricant will increase the

lifetime of the component. However without fully understanding the nature of the

bearing and how it is lubricated it is foolhardy to suggest a suitable replacement

lubricant.

When these treatments do not work or the situation is continually getting worse,

surgery is needed to relieve chronic pain (Australian Orthopaedic Association


43

2002). Joint replacement is a treatment typically reserved for patients over 55 years

of age, and is undertaken when no other measures can be used to save or prolong

the life of the joint.

Although new research continues to provide more information about the causes and

mechanisms of osteoarthritis, the roles of tribology and biochemistry in the process

of joint degradation must be more clearly understood before the disease can be

adequately prevented or cured. Ultimately, preventative measures could become

available that may force joint replacements and other such radical procedures into

obsolescence.

3.6 Total Artificial Joint Replacement

Total joint replacement (TJR), also called arthroplasty and referred to commonly as

hip/knee surgery or a hip/knee replacement, is a surgical procedure that removes

the diseased components of the natural joint and replaces them with an artificial

equivalent.

In a partial joint replacement, one of the articulating surfaces of the joint is

surgically removed and replaced with an approximate artificial replica. In total joint

replacements, both articulating surfaces are removed. The prosthesis design is

usually chosen from a library of geometries, then modified by a varying selection

of ball sizes, in the case of the hip, to fit the specific patient. When all or a portion

of a joint is replaced, a portion of the patient’s bone must be cut away and

removed; the prosthesis is then mounted or cemented in place on the truncated end

of the bone.

The earliest successful implants were bone plates, introduced in the early 1900s to

stabilize bone fractures and accelerate their healing. In 1925, a surgeon in Boston,

Massachusetts, M.N. Smith-Petersen, M.D., moulded a piece of glass into the

shape of a hollow hemisphere which could fit over the ball of the hip joint and

provide a new smooth surface for movement. In the 1930s PhiIlip Wiles from the

Middlesex Hospital, London, UK designed and inserted the first total hip


44

replacements. G.K.McKee, who was following Wiles, introduced metal-on-metal

hip prostheses. He developed various uncemented prototype total hip replacements

in the 1940's and 1950's. Dental cement brought about a new era in fixation

techniques and the McKee-Farrar Total Hip Replacement (THR) was the first

widely used and successful THR. In the late 1950s, the first total hip replacement

was introduced using PTFE as the cup-bearing surface (Blanchard 1995). However,

since the PTFE undergoes aseptic loosening, PTFE did not proved to be an

appropriate material to use as a load-bearing surface in the body. In the late 1960s

Sir John Charnley, a British Orthopaedic surgeon, developed the fundamental

principles of the artificial hip that still sees widespread use today. Frank Gunston

developed one of the first artificial knee joints in 1969. Since then, joint

replacement surgery has become one of the most successful orthopaedic treatments

(http://www.utahhipandknee.com/history.htm 2004).

It is now accepted that a Charnley-type total hip replacement can give satisfactory

results in an elderly sub-active population. Several metals are used including

stainless steel, alloys of cobalt and chrome, and titanium, and the plastic material

used is the durable and wear resistant UHMWPE. Recent research on hip and knee

replacement prostheses covers areas such as tribology of metal-on-metal hip joints,

coatings for enhanced tribological performance, soft layer and hard-bearing

surfaces in hip replacements, generation and biological activity of wear debris,

wear measurement and component geometry, wear of ceramic-on-ceramic joint

replacements, validation of knee simulator wear, wear measurement on knee

prostheses, lubricating film thickness in hip prostheses, and advances in simulator

testing (Hutchings 2002).

Current artificial joints made with UHMWPE and metals undergo degradation after

10- 15 years (Spector 1992; Shi et al. 2001). The research on how to improve the

design and materials to improve the durability of the artificial joints is the key for

the most recent research.

Total artificial joints must not only survive the rigorous loading pattern of the

human synovial joint, but must do so under extreme biological conditions. Low


45

coefficients of friction are essential in order to minimise the torque transmitted to

the surrounding bone. They must be long lasting, requiring an implantation life of

up to, and sometimes over 20 years depending on the age of the patient. They must

also exhibit very low wear rates, with the wear particles not causing adverse

cellular reactions that lead to loosening and failure. (Fisher & Dowson 1991)

For forty years, the basic tribological design of hip joints has not changed. There

have been many innovations regarding the strength, shape, function and behaviour

of the femoral stem which holds the prosthesis into the bone, but the surfaces have

changed very little indeed since Charnley first moved from PTFE to UHMWPE

(Maroudas 1967).

3.6.1 Artificial joint failure

The reasons for failure of current hip and knee joint replacements are, in order of

proportion, loosening, dislocation and wear (Australian Orthopaedic Association

2002). Failure due to dislocation is beyond the scope of this thesis but lies with a

better education of surgeons and the use of computer guided surgery. The other two

main modes of failure for implants are loosening and wear, and account for more

than half of revision procedures. Considering the nature of two articulating surfaces

and with wear (directly and indirectly through loosening) being the biggest mode

of failure of joint replacements, it is clear that the failure of many artificial joints is

a tribological issue. Hence tribology plays a major role in the effective treatment of

one of the most common medical conditions known in the western world

(Unsworth 1991).

Wear particles of UHMWPE are known to cause adverse cellular reactions

resulting in loosening and eventual failure of the prosthesis. The wear particles are

released into surrounding tissues and fluids where they initiate macrophage

activity. Since the wear particles cannot be broken down, the macrophages secrete

cytokines and other inflammation mediators that cause necrosis (death) and

resorption of the bone near the joint replacement. This reaction is a major cause of

prosthetic loosening and failure (Fisher & Dowson 1991) and (Ingham & Fisher


46

2000). Other causes of loosening include the response of the bone to stress

shielding and micromotion between the bone and prosthesis (Ingham & Fisher

2000).

High friction in the artificial joint cause’s high torque loads to be transmitted to the

bone-implant interface which may accelerate the loosening of the implant in light

of loosening being the primary reason for failure. Combine this with the immune

reaction to wear debris and friction in the joint is very important. It is therefore

important to improve lubrication mechanisms in order to reduce friction and hence,

wear.

It is obvious there is still a need for a better solution for TJR and one way to offer

this is to consider the tribological aspects of the joint and provide materials that

better suit the indigenous lubricant.

3.6.2 Biomaterials

Well over a century ago a great search was already under way for some material

which could be utilised to resurface or even replace diseased hips. Several

proposals and trials were made including the use of muscles, fat, chromatized pig

bladder, gold, magnesium and zinc. All met with failure. Surgeons and scientists

were unable to find a material which was biocompatible with the body, and yet

strong enough to withstand the tremendous forces placed on the hip joint. Stainless

steel was trialled in the late 1920’s but the poor steel processing techniques of the

day led to corrosion in the body. A break through occurred in the 1930s when

scientists manufactured a cobalt-chromium alloy that was almost immediately

applied to the orthopaedic problem. This new alloy was both very strong and

resistant to corrosion, and has continued to be employed in various prostheses since

that time. The next hurdle in the treatment of the arthritic hip was to replace the

pelvic component, the acetabulum cup, with a suitable biomaterial. An attempt was

made in the late 1950s by John Charnley when he replaced the arthritic socket with

a polytetrafluoroethylene (PTFE or Teflon) implant. Although PTFE is one of the

most ‘slippery’ materials know to man in the engineering world, it had disastrous


47

results in the body. Undeterred, Charnley went on to try polyethylene (PE) with

great success. Over a very short time, this became the 'gold standard' for joint

replacement, starting with total hip replacement and quickly spilling over to total

knee replacement.

The most common combination of materials used for artificial joints today is ultra

high molecular weight polyethylene (UHMWPE) cups sliding on hard metallic or

ceramic heads (Fisher & Dowson 1991), (Ingham & Fisher 2000). Typical

materials used for the heads include: stainless steel (316L), titanium alloy (Ti 6Al

4V), cobalt chrome molybdenum alloy (Co 28Cr 6Mo), and aluminium oxide

ceramic (alumina Al2O3). This combination of UHMWPE on metallic or ceramic

heads has been found to be quite successful in providing both low coefficients of

friction and wear rates.

However, considering the previous section, it is clearly evident that the optimal

material has not yet been found for use in prosthetics. Research is ongoing in

search of materials that will allow for a longer lasting implant.

3.6.2.1 Pyrolytic Carbon

A search is underway for new implant materials that have low friction and are

highly wear-resistant and biocompatible. The friction and wear properties are only

pertinent to the bearing surfaces themselves rather than to the bulk material. In

tribology, various methods are used to modify the friction and wear behaviour of

the contacting surfaces. A common method for modifying surface properties for

tribological applications is through deposition of a distinctive surface layer in the

form of a coating. One such coating is Pyrolytic carbon, a very successful

biomaterial (More, Haubold et al. 2000) already used for prostheses in the heart

and the upper limbs. This low friction and wear resistant thin film coating may be a

candidate material for articulating surfaces of total joint prostheses.

While many engineering materials and biomaterials are based on carbon or contain

carbon in some form, elemental carbon itself is also an important and very

successful biomaterial. Elemental carbon is found in nature as two crystalline


48

allotrophic forms: graphite and diamond. Elemental carbon also occurs as a

spectrum of imperfect, turbostratic crystalline forms that range in degree of

crystallinity from amorphous to the perfectly crystalline allotropes (More, Haubold

et al. 2000). Recently a third crystalline form of elemental carbon, the fullerene

structure, has been discovered. There exist many possible forms of elemental

carbon that are intermediate in structure and properties between those of the

allotropes diamond and graphite. Such 'turbostratic' carbons occur as a spectrum of

amorphous through mixed amorphous, graphite-like and diamond-like to the

perfectly crystalline allotropes. Because of the dependence of properties upon

structure, there can be considerable variability in properties for the turbostratic

carbons. Properties found in one type of carbon structure can be totally different in

another type of structure.

The biomaterial known as Pyrolytic Carbon (PyC) is not found in nature—it is

manmade. Pure carbon was the original objective of the development of PyC

because of the potential for superior biocompatibility (LaGrange, Gott et al. 1969).

The successful pyrolytic carbon biomaterial was developed at General Atomic

during the late 1960s using a fluidized bed reactor (Bokros 1969). In the original

terminology, this material was considered a low temperature isotropic carbon (LTI

carbon). Pyrolytic carbon components have been used in more than 25 different

prosthetic heart valve designs since the late 1960's and have accumulated a clinical

experience on the order of 16 million patient-years (More, Haubold et al. 2000).

Clearly, pyrolytic carbon is one of the most successful and critical biomaterials

both in function and application. Among the materials available for mechanical

heart valve prostheses, pyrolytic carbon has the best combination of blood

compatibility, physical and mechanical properties and durability.

The term ‘‘pyrolytic’’ is derived from ‘‘pyrolysis’’ which means thermal

decomposition. PyC is formed from the thermal decomposition of hydrocarbons

such as propane, propylene, acetylene and methane, in the absence of oxygen.

Without oxygen, the typical decomposition of the hydrocarbon to carbon dioxide

and water cannot take place; instead, a more complex cascade of decomposition

products occurs that ultimately results in a ‘polymerization’ of the individual


49

carbon atoms into large macroatomic arrays (More, Haubold et al. 2000).

Decomposition products, under the appropriate conditions, can form gas-phase

nucleated droplets of carbon/hydrogen, which condense and deposit on the surfaces

of items within the reactor (Bokros 1969). This pyrolytic carbon coating can be

produced in a variety of structures such as laminar or isotropic, granular or

columnar. The structure of the coating is controlled by the gas flow rate (residence

time in the bed), hydrocarbon species, temperature and bed surface area. This

control allows for a tailor made material, inasmuch that the structure can be

controlled to provide required mechanical properties and the surface can be

modified to give the desired surface properties.

Since pyrolytic carbon is a coating, it must be deposited on an appropriately

shaped, pre-formed substrate (preform). Because the pyrolysis process takes place

at high temperatures, the choice of substrates is severely limited. Only a few of the

refractory materials such as tantalum or molybdenum/rhenium alloys and graphite

can withstand the conditions at which the pyrolytic carbon coating is produced. It

is important for the thermal expansion characteristics of the substrate to closely

match those of the applied coating: otherwise, upon cooling of the coated part to

room temperature, the coating will be highly stressed and can spontaneously crack.

For contemporary heart valve applications, fine-grained isotropic graphite is the

most commonly used substrate. The graphite substrate does not impart structural

strength; rather, it provides a dimensionally stable platform for the pyrolytic carbon

coating at both the reaction temperature and at room temperature.

PyC was found to have not only remarkable blood compatibility but also the

structural properties needed for long-term use in artificial heart valves (LaGrange,

Gott et al. 1969). PyC flexural strength is high enough to provide the necessary

structural stability for a variety of implant applications, and the density is low

enough to allow for components to move easily under the applied forces of

circulating blood. With respect to orthopaedic applications, Young’s modulus is in

the range reported for bone (Reilly & Burstein 1974; Reilly, Burstein et al. 1974),

which allows for compliance matching. Relative to metals and polymers, the


50

pyrolytic carbon strain-to-failure is low; it is a nearly ideal linear elastic material

and requires consideration of brittle material principles in component design.

Wear resistance of the pyrolytic carbon is excellent. The strength, stability and

durability of pyrolytic carbon are responsible for the extension of mechanical valve

lifetimes from less than 20 years to more than the recipient’s expected lifetime

(More, Haubold et al. 2000). This property alone makes PyC attractive for use in

the body where wear is known to be an issue. It is interesting to note that some PyC

heart valves have PyC/PyC hinge joints that allow the valve leaflets to open and

close about 40 million times a year and have shown very little wear after 10 – 20

years of service. Contact pressures at the PyC/PyC hinge joint are high due to the

“water hammer” effect at valve closure.

The surface of as-deposited, machined and polished components is shown in Figure

3.4. It was found early on in experiments (LaGrange, Gott et al. 1969) that clean

polished pyrolytic carbon surfaces of tubes, when placed within the vasculature of

experimental animals, accumulated minimal if any thrombus and certainly less than

pyrolytic carbon tubes with the as-deposited surface. Consequently, the surfaces of

pyrolytic carbon have historically been polished, either manually or mechanically,

using fine diamond or aluminium oxide pastes and slurries. The surface finish

achieved has roughness measured on the scale of nanometers. The surfaces of

polished pyrolytic carbon (30-50nm) are an order of magnitude smoother than the

as-deposited surfaces (300-500nm).


51

Figure 3.4. Various forms of PyC indicating surface finish. (Left to Right) As-

deposited, machined and polished.

Pyrolytic carbon surface chemistry is important because the manufacturing and

cleaning operations to which a component is subjected can change and redefine the

surface that is presented to the body’s fluids. For example, oxidation of carbon

surfaces can produce surface contamination that detracts from blood compatibility

(LaGrange, Gott et al. 1969). The effect of modified surface chemistry on blood

compatibility is not well characterised.

It is believed that pyrolytic carbon owes its demonstrated blood compatibility to its

inertness, and to its ability to quickly absorb proteins from blood without triggering

a protein denaturing reaction. Ultimately, the blood compatibility is thought to be a

result of the protein layer formed upon the carbon surface. Baier observed that

pyrolytic carbon surfaces have a relatively high critical surface tension of 50

dyne/cm, which immediately drops to 28 to 30 dyne/cm following exposure to

blood (Baier, Gott et al. 1970). A more contemporary version of the mechanism of

pyrolytic carbon blood compatibility might be to reject the assumption that the

surface is inert, as it is now thought by some that no material is totally inert in the

body (Williams 1998) and accept that the blood-material interaction is preceded by


52

a complex, interdependent and time-dependent series of interactions between the

plasma proteins and the surface (Hanson 1998) that is as yet poorly understood.

The suitability of a material for use in an implant is a complex issue. The merit of

success of PyC in heart valves can not be simply passed onto other potential

applications for PyC in the body. The suitability of carbon materials for long-term

implants is not assured simply because the material is carbon. Elemental carbon

encompasses a broad spectrum of possible structures, mechanical properties and

surface characteristics. Each new candidate carbon material requires a specific

assessment of biocompatibility.

Cook et al have researched the application of PyC in a hip implant as trialled in

canines (Cook, Thomas et al. 1989). They compared the effect of common

prosthetic metallic surfaces versus the PyC articulating against the cartilaginous

acetabulum. They found that PyC resulted in significantly less damage to the

cartilage surface than with either the CoCr or Ti alloys. Survivorship analysis

indicated a 92% probability of survival for cartilage articulating with PyC as

compared to only a 20% probability of survival for cartilage articulating with either

of the metallic alloys. The reason for this far superior performance was unknown.

It is clear that PyC has some very interesting surface properties. The research to

date seems to indicate that the PyC surface is active and binds biologic molecules

that result in blood compatibility and possibly a very slippery, wear resistant

surface. The tribology, and more accurately the tribochemistry, of this coating is of

keen interest as a material that may be suitable for load bearing implants such as

the hip and knee where wear is known the be a problem. Modification of the

activity of the PyC surface by both chemical and thermal treatments is possible to

enhance the attachment of bio macro-molecules, for example SAPL. Knowledge

gained from tribological studies of PyC and the body’s fluids will be invaluable to

the future use of PyC in the human body.


53

This chapter describes the natural bearing - the synovial joint and its failure due to

OA and the replacement bearing - the artificial joint and its failure due to

tribological reasons, establishing the need to provide a more satisfactory solution to

the problem of joint failure.

3.7 Summary

The synovial joint is an amazing machine element from the engineer’s perspective.

The ability to provide such effortless motion over a large range of loads for the

lifetime of the individual is astounding. A large amount of this feat is thought to be

due to the synergy between the unique properties of both the articular cartilage and

the synovial fluid. Surface active phospholipids have been identified in both the

synovial fluid and the articular cartilage and are thought to play an important role

in the lubrication of the joint. DPPC has been identified in the natural joint. DPPC

has been identified in the artificial joint. DPPC has been shown to reduce friction

and wear between prosthetic materials (Sect 4.4.). The presence of not only DPPC

but all PCs (SAPLs), essentially all surface active molecules (that may be

beneficial in lubrication) need to be qualified in the joint environment. Part of this

dissertation seeks to identify the surfactants present in the artificial joint.

As amazing as this natural bearing is it still fails in a large number of cases due to

primarily osteoarthritis. Few treatments exist for these failures, none of which offer

a long term solution. Viscosupplementation receives some credit from the

engineer’s standpoint as the idea of renewing the lubricant in the bearing has merit.

However until the nature of the joint and it’s lubrication is fully understood it

would be unwise to suggest such a replacement lubricant. The long term solution to

OA is the removal of the diseased joint and replacement with an artificial

equivalent in as procedure called a total joint replacement. This equivalent is not a

true equivalent and suffers from a limited lifetime. There is evidence that suggests

that many artificial joints fail due to a tribological situation in vivo.

It has been shown that the lubricating ability of pathologic synovial fluid remains

largely unaffected therefore it is the radical replacement of the natural bearing

surface with man-made materials that may be the source of the problem in TJR


54

failures. Most of the research to date attempting to solve this problem of wear-

related failure in TJRs has been divided into two areas; developing materials that

mimic the properties of AC and the development of more wear resistant

biocompatible material pairs. The thesis considered the latter and investigated the

tribological performance of pyrolytic carbon a highly successful biomaterial used

in non-load bearing locations in the body.

Chapter 4: Literature Review – Lubrication of Joints

55

Chapter 4

Literature Review – Lubrication of Joints

This chapter includes a discussion of tribology in general with a focus on the

lubrication of synovial joints, both natural and artificial. It should be noted that in

an examination of the literature on synovial joint lubrication far more research has

occurred and hence considerably more information is available for the natural joint

as compared to its replacement. As previously stated it is a crucial step in

engineering to have a sound understanding of the function of the original

component before designing a replacement component.

The major load bearing joints, the joints of the lower extremities such as the hip,

are essentially ball and socket joints. Human joints are required to maintain

efficient and painless function for at least 7 to 8 decades under normal conditions.

In order for two opposing surfaces to be continually rubbing against one another

for such a period without major functional deterioration, i.e. wear and tear, a

remarkable system of regeneration and/or lubrication is required within the joint

capsule. It is accepted that the joint itself has a relatively low level of metabolic

turnover (Mankin & Lippiello 1969; Mankin & Brandt 1984; McIlwraith &

Vachon 1988) and, as a result, has a slow rate of repair following injury. This

would tend to negate the argument that the joints maintain their function through

regeneration. Hence, it would seem clear that it is the role of a lubricant present in

the joint capsule to keep the joint mobile through a lifetime of normal wear and

tear. Over the last century, lubrication mechanisms ranging from the simple to the

complex have been examined with reference to their possible function at the

synovial joint surface. There is still no clear agreement on which mechanism acts

within the joint. However, it is clear that either of the two fundamental mechanisms

of lubrication, as described in the physical sciences; fluid-film lubrication or

boundary lubrication, are responsible. Further, it is probable that combinations or

modifications of these mechanisms play a role in the lubrication of the joint.


56

Today our knowledge of diarthrodial joint lubrication is based not only upon these

basic lubrication mechanisms, but also upon our knowledge of the structural and

deformational characteristics of the articular cartilage; the biochemical and

biorheological (flow) properties of synovial fluid; the roughness of the articular

surface; the kinematics associated with each particular joint and the nature of the

loads applied to the articular surface (Mow & Mak 1987). It may be stated at this

stage that the unique lubricating properties of synovial joints are not solely due to

either synovial fluid or to the articular cartilage but to some complex synergistic

interaction of both (Dintenfass 1963). Understandably this situation/system is

radically changed when the cartilaginous bearing surfaces are replaced with an

artificial/man-made material.

“It is interesting to consider that the development of ideas on human joint

lubrication has followed a very similar pattern to the general development of the

understanding of highly loaded lubricated components in engineering” (Dowson,

Wright et al. 1969). It may be oversimplified to consider such a complex creation

with engineering principles but it is the engineer that has been called upon to help

elucidate the mystery of synovial joint lubrication.

Essentially the synovial joint can be likened to a mechanical bearing, by

description, a plain bearing. A bearing is made up of two bearing surfaces

(cartilage on cartilage for the original joint and several different man made

materials for the replacement joint), a load and/or motion (ambulation) and a

lubricant (synovial fluid). It must be noted here that in the case of a replacement

joint the only change to the system is the bearing surfaces and consideration must

be given to the interaction of the lubricant (which may also be affected by the

condition that brought about the failure of the original bearing surfaces) with the

new bearing surfaces. The original bearing surfaces and the lubrication of cartilage

are considerably different to the replacement bearing surfaces and their lubrication.

Articular cartilage, which covers the ends of the bones in the joint as a thin layer, is

not a rigid structure like the replacement material; it is flexible and compliant,

almost a gelatinous substance which shares with synovial fluid the fact that in its

composition there is more water than solid substance (Charnley 1959).


57

The natural joint is a remarkable bearing. It is expected to operate in the human

machine for a lifetime while transmitting varying loads and yet accommodating a

wide range of movement. It normally performs these functions with high efficiency

and coefficients of friction as low as 0.002 have been recorded. In engineering

situations bearing life is sometimes measured in minutes, often in hours and

sometimes in years, but it is rare indeed for the bearing designer to be asked to

provide a bearing with an estimated life of 70 years or more! It is fair to say that the

engineer would find it extremely difficult to provide a bearing which would operate

within the environment of the body, in the same space as the natural bearing, under

the same loads, with the same degree of movement, with similar friction and

comparable mean life to the natural bearing (Dowson 1973).

The influence of lubrication, friction, wear and good bearing design upon the

efficiency and general economic performance of the machinery in our

technological society was recognised in 1966 by the introduction of a new word,

'tribology', meaning 'the science and technology of interacting surfaces in relative

motion and practices related thereto'. In recent years tribologists have worked with

rheumatologists, orthopaedic surgeons, and biochemists in an effort to understand

the remarkable characteristics of healthy joints and, perhaps more importantly, the

reasons why some human bearings wear out more rapidly than others. Engineers

tend to classify forms of lubrication into a few well known physical and chemical

mechanisms, and a good deal of progress has now been made towards an

understanding of the performance of the natural joint. Attempts have also been

made to develop synthetic lubricants which might be introduced into the joints

which start to show signs of failure in the same way that an engineer might prolong

the life of a bearing in a machine by introducing an improved lubricant (Dowson

1973). However it would seem pointless to design such pseudo-synovial fluids

until the lubrication of the human bearing is clearly understood and the indigenous

lubricant is fully defined.

Relative motion between two surfaces is characterised by frictional forces and wear

of the rubbing surfaces. In general, the purpose of a lubricant is to reduce friction


58

and prevent the wear of the surfaces. The ability of synovial joints to function with

almost negligible frictional resistance with a coefficient of kinetic friction (µ)

ranging from 0.001- 0.03 (Jones 1934; Charnley 1959; Dintenfass 1963; Linn

1968), and to do so under appreciable stress, up to l3kg/cm2 or 1.3MPa indicates a

superior system of lubrication which has not been matched in non-biological

systems (Hills 1989).

The lubrication of synovial joints has received comparatively little attention from

physiologists from a point of view which might seem rather obvious to engineers.

The possibility that the lubrication of synovial joints might be a more subtle

problem than had been suspected presented itself when investigating certain

disappointing results (Hall, Unsworth et al. 1997) encountered after attempts to

construct artificial joints by existing surgical techniques. The hip joint, which in

form is an almost perfect ball and socket, is frequently affected by types of arthritis

which destroy the polished rubbing surfaces and which distort the geometry of the

concentric spherical surfaces, with the result that motion is restricted and pain

develops. Early artificial joints designed on accepted ideas of joint lubrication at

the time seemed adequate to replace the distorted and destroyed ball (the head of

the femur) by a sphere of any substance which could be tolerated without adverse

reaction of the body tissues, such as stainless steel, cobalt-chromium alloy or

plastic. Provided that the surface of the sphere was highly polished it has been

assumed without question that its 'slipperiness' when bathed in tissue fluids would

be adequate to function as a weight-bearing joint (Charnley 1959). Even if the

coefficient of friction of this artificial joint was not quite as favourable as the

normal joint, it has been accepted that from a mechanical standpoint a polished

steel sphere would be an improvement on the diseased and distorted head which it

was used to replace. The early results of many of these operations, often quite

dramatically successful in the early months after operation, suggest that surgical

research is very close to success; but, the later results, with return of pain and

disability in many cases, showed that important details still eluded discovery. The

suspicion was aroused that accepted ideas of joint lubrication at that time might be

too simple, and it was necessary re- investigate the subject of normal joint


59

lubrication before investigating the frictional properties of substances suitable for

making an artificial joint.

4.1 Physical Science of Lubrication, Friction and Wear

The word “Tribology” comes from the Greek word Tριβω or ‘tribos’, meaning “to

rub.” It is concerned with surface interactions between two bodies moving relative

to one another. Tribology is generally defined as the study of three areas: friction,

wear, and lubrication of interacting surfaces. The three are highly related, although

in the case of friction and wear their relationship is not well understood. Generally

speaking, wear is friction-related, but there are exceptions to the rule. These

exceptions relate to when wear is regarded as phenomena. Basically, friction is

produced when two sliding surfaces come into contact and inevitably wear will

occur. The defence against wear is achieved by lubrication; the separation of the

two surfaces by a lubricant that will result in a reduction of friction.

Friction

Friction can be defined as the force that acts at the surfaces of two articulating solid

bodies so as to resist sliding on one another. Simply, it is the resistance to motion

of surfaces in relative motion. This force which tends to prevent one surface sliding

over another is caused by shearing of local adhesions that occur at the regions of

real contact between asperities and is very conveniently quantified by a simple

index - the coefficient of friction (µ). The first published study of friction was by

Amonton in 1699 (Shi 2004) who revealed certain ‘laws’ of friction which still

form the basis for the analysis of many sliding contacts today. For dry friction, 1)

the frictional force is directly proportional to the applied load (Amontons 1st Law);

2) the force of friction is independent of the apparent area (A) of contact

(Amontons 2nd

Law); and 3) kinetic friction is independent of the sliding velocity

(Coulombs Law). When a block is placed on a dry surface as illustrated in Figure

4.1, the force (F) needed to be applied in the plane of the interface in order to cause

motion is found to be proportional to the weight (W) or other force pressing the

two surfaces together (Adamson, 1967).


60

Figure 4.1. Amontons' Laws of Friction. Source: (Shi 2004)

The proportionality constant (µ) is termed the coefficient of friction and tends to be

lower after motion is established (Stachowiak & Batchelor 2005), so it is more

appropriate to use the coefficient of kinetic friction in the physiological context. In

order to determine the coefficient of friction, two measurements are needed: the

force (F) required to initiate and/or sustain sliding and the normal force (W)

holding the two surfaces together. The coefficient of friction is then equal to the

initiation/sustaining force divided by the normal force. Since a lubricant reduces

friction, µ provides a very convenient index for quantifying the lubricating ability

of any system. It should be noted that µ must be considered with care as it is

subjective to the lubricated conditions and type of tribometer used. Comparisons

between µ values generated by the apparatus under the same conditions is

acceptable but the comparison of friction coefficient values from differing

apparatus and dissimilar conditions need to be treated with care. This is especially

true for boundary lubrication where many variables play a role in lubrication

(4.1.2).

Lubrication

'Lubrication may be defined as any means capable of controlling friction and wear

of interacting surfaces in relative motion.' (Hsu & Gates 2001). From this definition

it is clear that an effective lubricant is one which minimises both the coefficient of

friction and the amount of wear particles produced. Essentially, effective

lubrication can almost entirely eliminate the friction force by keeping the two

interacting surfaces apart. This is made possible by some ‘substance’ that keeps the

bearing surfaces from touching. This ‘substance’ is referred to as the ‘lubricant’

and can be a liquid, a solid, a mixture of the two or even a gas.


61

There are basically two types of lubrication - one in which there is solid-to-solid

contact of the sliding surfaces known as boundary lubrication and the other where a

thin layer of fluid is either pumped into the intervening space (hydrostatic

lubrication) or the motion itself produces a wedge of fluid on which the moving

surface planes over the counterface (hydrodynamic lubrication). In most

engineering applications, hydrodynamic lubrication is much more effective than

boundary lubrication, but requires high velocities for the wedge of fluid to generate

enough pressure to overcome the load and keep the surfaces separated. In starting

up machinery, the friction and wear are much higher as boundary lubrication gives

way to hydrodynamic lubrication as the fluid film is established and the same

applies in the opposite sense at shutdown. The transition between these modes is

very important, as originally recognised by Stribeck in his classical diagram

(similar to Figure 4.2) demonstrating the change in friction as one mode supplants

the other.

Figure 4.2. Range of coefficients of kinetic friction reported in the literature

for the mammalian joint are depicted over a physiological range of sliding

velocities and compared with the a modified classical Stribeck diagram. Source: (Hills 2000)


62

The Stribeck diagram clearly indicates the drop in the coefficient of friction as the

velocity increases and the transition occurs from solid-to-solid contact to the

establishment of a fluid-film. The friction of fluid film lubrication is proportional to

both the sliding velocity and the bulk fluid viscosity and inversely proportional to

the film lubricant thickness. Therefore as the velocity reduces the fluid film

thickness diminishes and the friction increases. There are three regions in the

Stribeck-Curve: boundary lubrication, a transition region which refers to mixed

lubrication and hydrodynamic lubrication (which includes elasto-hydrodynamic

lubrication (EHL)). Boundary lubrication is characterised by the absence of

hydrodynamic pressure or fluid pressure. One hundred percent of the loading is

carried by the asperities in the contact area, protected by adsorbed molecules of the

lubricant. Mixed lubrication is the intermediate region between boundary

lubrication and hydrodynamic lubrication. Hydrodynamic lubrication is

characterised by the presence of a pressurised fluid that keeps the surfaces apart.

The lubrication regimes are shown schematically below in Figure 4.3. where h is

referred to as the film thickness that separates the bearing surfaces.


63

Figure 4.3. Lubrication regimes Source: (Dowson, Wright et al. 1969)

In systems where both static and kinetic friction occur at some stage (eg most

engines) a force known as the “break-out” or “start-up” force must be overcome.

The coefficient of friction associated with static friction is generally much higher

than that associated with kinetic friction and it is a known fact that the majority of

wear in engines occurs at these times of start-up and shut-down. It is well

established in the physical sciences that, to overcome the problem of the break-out

force, it is necessary to use additives in oils designed for use in systems where


64

there will be components of both static and dynamic friction. The role of the

tribologist is to define a lubricant that can cater to all operating conditions.

When an engineer investigates the performance of bearings he tries to determine

the mode of lubrication and to classify the system as "fluid-film" or "boundary" or

some combination of the two. As mentioned, in fluid-film lubrication the bearing

surfaces are completely separated by a film of fluid for most of their working life

and the frictional characteristics of the bearing can be explained in terms of the

rheological properties of the bulk fluid. In boundary lubrication the bearing

surfaces come much closer together and the frictional characteristics of the bearing

are determined by the properties of the surface materials. The predominant surface

properties are rarely related to the bulk properties of the fluid or the solid and are

usually determined by thin layers of molecular proportions which might take the

form of material arising from chemical reaction between the bearing material and

its immediate environment of thin layers formed by physical or chemical

adsorption (Dowson, Wright et al. 1969).

Wear

Wear can be defined as the progressive loss of substance from articulating surfaces

in relative motion. Mechanisms of wear are many and varied and include abrasion,

adhesion, surface fatigue, corrosion etc. These mechanisms may occur singly or at

the same time. They may also operate independently or interact (Axén, Hogmark et

al. 2001). Friction is caused by the two surfaces coming into contact and this

contact eventually causes wear. It is a simple conclusion to presume that this would

logically mean the lower the friction the lower the wear, however this is not always

the case. Low friction does not always result in low wear and high friction does not

always result in high wear. But generally in bearing design the lower the friction

the lower the wear (Bhushan 2001). There is also evidence (Williams 2005) where

a small increase in friction has led to a large increase in wear and conversely a

decrease in friction has lead to a reduction in wear. The engineering tribologists

must consider the laws of friction and the exceptions to the laws when designing

bearings.


65

4.1.1 Fluid-Film Lubrication

Fluid-film lubrication is a class of lubrication mechanisms having in common a

film of fluid that completely separates the opposing surfaces. This layer of fluid is

thicker than the sum of the surface roughness of the two surfaces. The development

of a film between the opposing surfaces may be achieved in various ways

depending on the properties of the fluid and the surface motion. The load on the

surface is supported by the pressure in the fluid film. The fluid film thickness is

usually less than 10µm according to (Dowson, Wright et al. 1969). The resistance

to motion arises entirely from the shearing of the viscous layer, and in general the

friction force can be represented by an equation of the form:

Equation 4.1. Ah

VF η=

where F = friction force;

V = relative sliding velocity

h = lubricant film thickness

A = effective area of bearing

η = coefficient of viscosity

The coefficient of viscosity is the most important property of a lubricant in fluid-

film bearings since it governs not only the resistance to motion but also the ability

of the bearing to develop adequate load-bearing pressures in the fluid.

The lubricating films in fluid-film bearings are themselves quite thin in physical

terms, normally between 1µm and 25µm. (Dowson, Wright et al. 1969) This

magnitude is normally adequate to separate the opposing bearing surfaces which

are, of course, manufactured with a high degree of precision. Surface roughness of

typical engineering bearings usually range from 0.1µm to 1µm Ra.

If the opposing bearing surfaces can be prevented from touching each other by

interposing a layer of fluid, wear is almost totally prevented and the resistance to

sliding is low. It is for this reason that 'fluid film' is often described as the ideal

mode of lubrication. If the load-carrying pressures are generated by the sliding


66

motion of the surfaces the mechanism is known as 'hydrodynamic lubrication', but

if the pressure is generated in a pump outside the bearing the action is known as

'hydrostatic lubrication'.

Hydrodynamic Lubrication

In the last decades of the 19th century engineers began to understand the manner in

which industrial bearings worked. The fact that they worked had long been

accepted but no-one could explain why oils and greases, which were obviously

essential to the continued running of bearings, could make things slippery. In 1883,

Beauchamp Tower (cited by (McCutchen 1978)) was experimenting with a bearing

shell that sat on an oiled rotating shaft when he noticed that oil flowed out of a hole

that was in the centre of the shell. A wooden plug was driven into the hole but was

slowly forced out by the oil. By mapping the pressure in the lubricating oil, Tower

found that the total force it exerted equalled the bearing load. The shell was

supported by liquid and did not touch the shaft at all so long as the shaft turned fast

enough. Lord Rayleigh (1884) and Sir Osborne Reynolds (1886) (both cited by

(McCutchen 1978)) independently realised that the bearing shell sets itself slightly

off centre horizontally relative to the shaft, forming a thin, curving wedge-shaped

space between itself and the shaft that converges in the direction of shaft motion.

Because the oil is viscous, the moving shaft drags it towards the thin edge of the

wedge where there is less and less room for it. A high pressure results which keeps

the surfaces apart. This was probably the first description of hydrodynamic

lubrication.

Hydrodynamic lubrication is essentially the classical model of fluid-film

lubrication. It occurs when the relative motion of two bearing surfaces draws fluid

into the space between them, keeping them apart, the height of the fluid decreasing

in the direction of motion (wedge action). This mechanism requires uninterrupted

motion in the same direction to maintain the integrity of the fluid wedge and is

especially efficient in high speed bearings.


67

The thickness (h) of the fluid layer in a hydrodynamic bearing in which the

viscosity of the fluid remains constant increases as the sliding speed (U) increases

and decreases as the load (W) increases, or

Equation 4.2. W

Uh ∝

Another important feature of hydrodynamic bearings is that the film thickness

decreases in the direction of sliding (Figure 4.3b).

Elastohydrodynamic Lubrication

Elastohydrodynamic lubrication (EHL) is defined as hydrodynamic lubrication

when applied to solid surfaces of low geometric conformity that deform elastically

(Szeri 2001). In bearings utilizing this mode of lubrication, the pressure and film

thickness are of order 1 GPa and 1 µm, respectively — under such conditions,

conventional lubricants exhibit behaviour distinctly different from their bulk

properties at normal pressure. In fact, without taking into account the viscosity–

pressure characteristics of the liquid lubricant and the elastic deformation of the

bounding solids, hydrodynamic theory is incapable of explaining the existence of

continuous lubricant films in highly loaded gears and rolling contact bearings. The

principal feature of EHL contacts is the film thickness is nearly uniform over the

contact zone, but displays a sudden decrease just upstream of the trailing edge

(Figure 4.3). EHL is a complex regime whereby large pressures are generated in

the fluid film separating the surfaces, large enough that one or both of the bearing

surfaces will elastically deform actually increasing the fluid film thickness between

the surfaces.

Hydrostatic Lubrication

This mechanism also falls under the general heading of fluid lubrication. Bearing

surfaces are held apart by a film of lubricant which is maintained under pressure

and usually supplied by an external pump. The load is completely supported by the

pressure supplied from an external source. This mechanism is especially suited to

oscillating bearings in low-speed applications when loads are high.


68

4.1.2 Boundary Lubrication

Boundary lubrication is a science on its own and it will receive further discussion

in Chapter 5.

“Boundary lubrication is perhaps the most confusing and complex aspect of the

subject of friction and wear prevention” (Ling, Klaus et al. 1969). Confusing in

part by the fact that the boundary is not always well defined and complex in part by

the large number of variables involved. In reference (Larsen & Perry 1950), twenty

nine variables are listed and the list is not by any means complete.

It is clear from Equation 4.1 that the thickness of the lubricant layer will decrease at

low speeds and high loads and in due course the opposing bearing surfaces will

come into contact at high spots or asperities. As the severity of this condition

increases, the effectiveness of the lubricant layer diminishes, friction rises, and the

bearing surfaces start to wear.

It is found that friction and resistance to wear are no longer governed by the

viscosity of the bulk fluid but by the properties of thin surface layers formed by

physical and chemical action on the surfaces of the solids; hence the term

'boundary lubrication' (Dowson, Wright et al. 1969).

Boundary lubrication has developed from experience from very early times. The

first crude wheel could not have been supported by an elegant hydrodynamic

bearing, so some system of boundary lubrication must have been used (Ling, Klaus

et al. 1969).

In engineering, boundary lubrication is known to occur during start, stop and under

severe operating conditions of mechanical machinery. During these conditions,

high loads and/or low speed cause the breakdown of the fluid film causing the

bearing surfaces to come into contact at their asperities. Effective boundary

lubrication depends on the properties of an anti-wear film which must be adsorbed

to the surfaces of the bearing materials and have high cohesion. This film may

operate to prevent wear in many ways. A sacrificial layer prevents wear by being


69

removed instead of the asperities of the bearing surfaces. In order for the surfaces

to remain protected, the rate of formation of the sacrificial layer must be greater

than the rate at which it is being removed. Many solid lubricants work using this

mechanism. Other mechanisms of boundary lubrication include shear resistant

layer, low shear interlayer, friction modifying layer, and load bearing glasses (Hsu

& Gates 2001).

Solid lubricants are a thin film of solid interposed between two rubbing surfaces.

They provide effective lubrication by shearing easily to prevent wear and

maintaining low coefficients of friction. Most solid lubricants can shear easily due

to their lamellar crystaline structure allowing ease of sliding between layers. They

contain close, strongly bonded layers connected by only weak forces between each

layer. It is thought that the strong bonding within the layer helps reduce wear

damage. Common examples of lamellar solid lubricants are graphite and

molybdenum disulfide (Erdemir 2001). Figure 4.4 shows the structure of these

solid lubricants. Evidence has been presented which suggests that surfactant found

in synovial fluid acts in the same way as lamellar solid lubricants, such as graphite,

in joint prosthesis. (Purbach, Hills et al. 2002)

Figure 4.4. Molecular Structure of Common Solid Lubricants (a) graphite,

and (b) molybdenum disulfide. (Erdemir 2001)


70

In commercial situations where surface contact between mating parts is known to

occur, substances are often added to the lubricant (for example engine oils) to

enhance its efficiency. Additives that improve lubricity are often commercial

surfactants. (Larson & Larson 1969) Surfactants adsorb to the bearing surfaces to

form a protective coating that prevents wear and decreases static friction when

contact occurs. They are also an effective anti-stick agent. Although these

surfactants are capable of producing extremely low levels of friction they are too

toxic to be used in clinical situations (Hills 2002).

When two surfaces touch, asperities from one surface make direct physical contact

with the other thus generating friction and possibly adhesion and abrasion if sliding

is attempted. On bearing surfaces these asperities are minimised by making them

macroscopically smooth, but friction can be further reduced if the material at the

interface shears. This could be done within the substance of the bearing, e.g.

Teflon, or within a layer of foreign substance physically adsorbed to the surface

(Figure 4.3.). Substances which are ideal for adsorption to the surface are

surfactants where the polar group bonds the molecule by strong chemisorption to

form an adsorbed monolayer. An example in everyday life is experienced in

touching a bar of wet soap when one’s fingers remain slippery, even after

squeezing out the water. Boundary lubricants are described in terms of their

chemistry and the chemistry of the surfaces they are to protect (Ling, Klaus et al.

1969).

Boundary lubrication is then highly dependent on maintaining strong cohesion of

the adsorbed monolayer in order to avoid its penetration by asperities on the

counterface. The basic molecular requirements for surfactant monolayers to act as

efficient boundary lubricants are described later (5.4.4.). An interesting sub-section

is lamellated-solid lubricants (Erdemir 2001) where sliding surfaces are separated

by multiple layers of the lubricant which are readily sheared, leaving the material

on both surfaces as determined by the cleavage plane. An everyday example is the

graphite pencil, which has the ability to withstand a perpendicularly applied load

while shearing. Thus graphite and molybdenum disulphide (MoS2) are much used

lubricants on their own or as additives in oils (Ling, Klaus et al. 1969).


71

Boundary lubrication is essentially independent of the physical properties of either

the lubricant (e.g. viscosity) or the contacting bodies (e.g. stiffness). The best

values for the coefficient of friction obtained in the non-biological field using

boundary mechanisms, is that of Teflon (polytetrafluroethylene PTFE) rubbing

upon Teflon providing a value for µ of 0.04. Boundary lubrication is generally

implicated under conditions where the load is very high, or the surface motion is

very small and continuous motion is not possible. It must act when the surface

asperities come into contact or when, under prolonged and possibly severe load, the

fluid film is depleted.

4.1.3 Mixed Lubrication

In many bearings there is a combination of both boundary and fluid film regimes, a

situation broadly termed as “mixed lubrication”. This lubrication condition is of

importance especially in systems where movement is intermittent; hence, there is

continual changing from boundary to fluid-film regimes.

4.1.4 Wear

Wear is defined as the damage to a surface that generally involves progressive loss

of material and is due to relative motion between that surface and a contacting

surface or substance(s) (Shi 2004).

Although practically everything which an engineer makes will ultimately wear out,

this aspect of tribology may be the least explored. The physical and chemical

actions involved in the wear process are complex and much current research is

devoted to their elucidation.

Well-known forms of wear include abrasion, adhesion, fatigue, erosion, fretting

and corrosive wear. Abrasive wear occurs when asperities of a rough, hard surface

slide over a softer one (e.g. steel over plastic) and damage the interface by plastic

deformation of fracture. Abrasive wear may also occur when hard particles are


72

trapped between rubbing surfaces. In the latter case, the abrasive material may

enter the system from the environment or it may be debris resulting from the wear

process (Bhushan 2001).

Adhesive wear, which occurs as a result of local welding at asperity junctions, is by

far the most common wear mechanism (Stachowiak 2005). In many cases the

volume of material removed in the adhesive wear process satisfies the following

relationship:

Equation 4.3. mp

WxkV

3=

where

V = volume of material worn away

W = applied load

x = total sliding distance

pm = hardness of softer material

k = wear coefficient

This equation enables the bearing designer to estimate the useful life of a bearing or

prosthesis under given operating conditions. It also enables the wear resistance of

different materials to be evaluated if the hardness can be measured and the

dimensionless wear coefficient evaluated (Dowson, Wright et al. 1969).

Fatigue wear occurs when repeated loading and unloading cycles are applied to the

materials and induce the formation of sub-face or surface cracks, which finally will

result in the break-up of the surface (Axén, Hogmark et al. 2001). Chemical and

corrosive wear occurs when sliding takes place in a corrosive environment. Impact

wear by erosion occurs due to jets and streams of solid particles, liquid droplets,

and implosion of bubbles formed in the liquid and by percussion from repetitive

solid body impacts. Fretting wear and fretting corrosion occur where low-

amplitude oscillatory motion in the tangential direction takes place between

contacting surfaces which are nominally at rest (Bhushan 2001; Ludema 2001).


73

Combinations of these mechanisms can be involved in the wear of biological

bearings and their replacements (Furey 2000).

Wear is related to friction, although in some cases the extent of this relationship is

not well understood. Effectively, high friction will lead to wear in bearings and low

friction is regarded as high wear resistance in most practical situations (Axén,

Hogmark et al. 2001).

4.2 Natural Joint Lubrication: A Review

The human joint is an extraordinary bearing and the engineer would find it difficult

to produce a simple bearing system of the same efficiency for similar operating

conditions. The friction forces in healthy joints are extremely low and coefficients

of friction as low as 0.002 have been recorded. However, in spite of the

extraordinarily low friction, weight-bearing human joints sometimes fail in the

mechanical sense and it is important to establish an understanding of the

lubrication mechanism in healthy joints if the reasons for these failures are to be

examined and understood (Dowson, Wright et al. 1969).

Under normal conditions the combined modifications of the various lubrication

mechanisms are more than adequate to keep the cartilage lubricating effectively

and keep wear minimal for what is essentially a lifetime. However, the failure of

lubrication would be expected to lead to increased cartilage wear and the process of

degeneration could begin (Cooke, Dowson et al. 1978). Indeed, this is one of the

models presented for the pathogenesis of osteoarthritis and other degenerative joint

diseases.

How extraordinarily low is a coefficient of friction of even 0.01 can be appreciated

only if it is realised that it is approximately three times better than the coefficient

for ice sliding on ice (which is approximately 0.03) and between ten and twenty

times better than that for a polished steel surface moving on a lubricated brass

bearing (which is within the range of 0.1 to 0.2). The extraordinary fact of this very

low coefficient of friction in a synovial joint may not be appreciated by all


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scientists. A coefficient of 0.01 means that a load of 50kg (the weight of a small

adult) could be made to slide by applying a force of only 500g. If articular cartilage

were to be no more slippery than a plain engine bearing the same load would need

a force of 5-10kg to make it slide. If we consider that in the lower extremity of a

human being four sliding surfaces are used simultaneously in each limb when

walking or running (hip, knee, knee-cap, and ankle) we see that for an adult

weighing 50kg, 2kg would be needed to move all these joints, but, if in place of

articular cartilage lubricated metal bearings were substituted, a total force of 20-

40kg would be needed to overcome frictional resistance. As Charnley said it best,

“The remarkable way in which nature has solved this friction problem will be

appreciated when it is realised that to equal it an engineer would have to discard

plain bearings and employ a so called 'frictionless' bearing where the rolling

mechanism of a ball-race takes the place of sliding friction” (Charnley 1959).

In the efforts to elucidate how the synovial joint maintains its remarkable

capabilities, showing almost negligible frictional resistance and wear rates, the

engineering analyses of lubrication were soon applied to the joint. This, however,

created an apparent conflict between support for the role of fluid-film lubrication

and support for the role of boundary lubrication. The very low values of 0.003-0.02

that were obtained with the joint would seem to indicate that lubrication had to be

hydrodynamic, as values obtained for solid- to-solid contact (boundary lubrication

mechanism) were typically at least an order of magnitude higher than these.

However, as clearly demonstrated by the Stribeck diagram (Figure 4.2), it is

necessary to reach a certain velocity (of at least 5cm/s) to attain and maintain a

fluid-film, yet the articular joint frequently performs many actions at extremely low

velocity, insufficient to maintain a system of hydrodynamic (fluid-film) lubrication.

Also, although joints are often stationary under load, there is no evidence of a

break-out (start-up) force when movement is resumed i.e., there is no obvious

transition from static to kinetic friction. Because of these complications, engineers

have been postulating models of joint lubrication that would enable fluid-film

lubrication to function at low velocities (certainly lower than that predicted by

Stribeck).


75

In hydrodynamic, or full-film lubrication, the nature of the substances composing

the sliding surfaces, and the nature of the fluid used as a lubricant, are theoretically

unimportant; the essentials are the geometry of the surfaces and the viscosity of the

fluid. In this type of lubrication it is not necessary for the fluid to possess the

property of 'oiliness'. If the hydrodynamic theory were to be the basis of joint

lubrication as it was thought to be in the pioneering years of the development of

TJRs it would be quite logical to expect success by replacing one, or even both, of

the spherical joint surfaces with polished surfaces of stainless steel or plastic of the

correct dimensions. Surgical experience at that time showed that this was not borne

out in practice and it is was the scientists of the time that deemed it necessary to

examine the other forms of lubrication that might be have present (Charnley 1959).

Since that time some thirty or more theories have been proposed for joint

lubrication (Furey & Burkhardt 1997) and several more have been hypothesised

since 1997 (Murakami, Higaki et al. 1998; Skotheim & Mahadevan 2004). The

sheer number of models shows the lack of complete understanding of joint

lubrication. It is difficult for those working on replacement bearings to design

suitable replacements when the lubrication of the original is not fully understood.

4.2.1 Experimental techniques and apparatus used to determine

the lubrication of joints

Generally, two types of frictional measurements have been conducted on joints. In

the first type, the frictional properties of entire joints have been tested using joint

testers or ‘arthrotripsometers’. All of these studies are of the pendulum or

reciprocating motion type, where one bone of the joint swings relative to the other,

either freely or through forced motion. In the second type of experiments, cartilage

explants have been rubbed against each other or against other materials.

Pendulums

Pendulums have been used by many research groups to attempt to identify the

mode of lubrication acting at a surface. In boundary lubrication, friction is

independent of speed so the amplitude of pendulum oscillation drops by an equal


76

amount with successive swings. With hydrodynamic lubrication, however, the loss

between swings falls as the amplitude falls, so long as the fluid film is complete. A

pendulum used in this way to assess friction by measuring the energy loss per cycle

is called a Stanton pendulum after T.E. Stanton (1923, cited by (McCutchen 1978))

In 1934, Jones measured the friction coefficient of cartilage against cartilage (using

a horse stifle joint) at very low rubbing speed and found a value of 0.02 regardless

of whether he used synovial fluid or Ringers solution as the lubricant. Later (Jones

1936), he measured friction using a pendulum with a human interphalangeal

(finger) joint as the pivot and observed how the oscillations decreased over time.

The behaviour of Jones’s pendulum fell between the expectations for boundary and

for hydrodynamic lubrication and, from this, Jones concluded that hydrodynamic

lubrication acted at high rubbing speeds, switching to boundary lubrication as the

rubbing-speed fell. This was the first suggestion of a mixed lubrication mechanism.

In 1959, Charnley repeated Jones’ experiments with a somewhat different

apparatus. He also removed the tendons and ligaments from the joint, but used the

same principle. He found very low coefficients of friction (0.005 - 0.024) which

varied little with speed. This prompted Charnley to suggest that the mechanism of

joint lubrication was purely boundary lubrication (Charnley 1959). Probably the

largest obstacle preventing widespread acceptance of this theory was that boundary

lubrication typically yields coefficients of friction of about 0.1 in engineering

applications, and the values reported by Charnley were considered to be attainable

only in situations which lubricated via fluid-film mechanisms. Once the possibility

was raised that the lubrication mechanism may be either fluid-film or boundary in

nature, an increasing number and variety of experiments followed.

Barnett and Cobold (1962) removed the skin, tendons and ligaments from their test

joint in stages. This enabled them to show that the frictional force between the

cartilage surfaces was independent of the amplitude and hence of the speed of the

oscillations, a characteristic of boundary lubrication. (Barnett & Cobbold 1962)


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In 1967, (Faber, Williamson et al. 1967) used an apparatus other than a pendulum

to assess friction at the full physiological range of rubbing speeds within the living

joint. Using a spring-loaded vibrating device, they noted that the decay of

oscillations was neither purely linear nor purely exponential. This implicated the

presence of both a boundary mechanism and a fluid-film mechanism, the

contribution of each varying with the load applied to the joint. (Little, Freeman et

al. 1969) used the femoral head and acetabulum of human hip joints as the pivot on

a Stanton pendulum. The hip was oscillated at various loads, with either synovial

fluid or Ringer’s solution as the lubricant. Under all conditions, the decay of free

oscillation appeared to be independent of load and rate of movement. This led the

group to conclude that the dominant frictional forces were boundary in nature.

Alternate Testing Apparatus

Another friction testing apparatus frequently employed to assist in solving the

riddle of the lubrication mechanism acting within the joint is to slide small pieces

of cartilage over another surface, usually cartilage or an artificial material such as

glass. This system offers the means to separate purely surface friction effects from

“ploughing” effects (Mow & Mak 1987). A slight problem with this apparatus is

that, unlike the in vivo situation, the entire surface of the cartilage is under load.

It was while using this type of apparatus (cartilage on glass) that McCutchen

(McCutchen 1962) was able to demonstrate that as good a bearing as cartilage is

when lubricated by distilled water or saline, it is better with synovial fluid.

However, it was also demonstrated that over short periods of time, synovial fluid

showed little advantage over water or saline in the lubrication of this set-up.

However, as time progressed the synovial fluid was obviously superior. The

significant point here would seem to be not that synovial fluid was superior to

saline over extended periods of time, but the fact that there was any lubrication

with saline at all. This would strongly support an argument for a lubricant adsorbed

to the cartilage surface. As this lubricant was worn away without replacement, as

would be the situation when using saline and water as the fluid lubricant, the

coefficient of friction would rise. With synovial fluid as the lubricant, the adsorbed

layer could be continually replaced and µ should remain constant. McCutchen went


78

on to propose a model of lubrication that utilised boundary lubrication and could

combine with his theory of weeping lubrication.

Malcolm (Malcolm 1976) tested cartilage against cartilage in a continuously

rotating articulation and found that the interfacial coefficient of friction; (1)

increased with time under load, (2) increased with magnitude of load, (3) was

lower when using synovial fluid as a lubricant rather than saline and (4) was very

sensitive to small vertical oscillations imposed on the rotating cartilage. These

‘dynamic loads’ dramatically decreased the coefficient of friction between the

rotating surfaces. This effect was attributed to the expression of interstitial fluid

caused by the imposed oscillation. This frictional experiment demonstrated that

when the interstitial fluid was forcibly expressed into the gap by the oscillation, a

fresh fluid film was created and thus frictional resistance was reduced: i.e. the

lubrication mechanism changes from boundary to fluid-film. Other experiments

that explored a wide range of speeds utilising this type of apparatus (Faber,

Williamson et al. 1967; Linn 1967) produced observations that also indicated the

simultaneous presence of both boundary and fluid film lubrication.

The diversity of possible lubrication mechanisms has created considerable interest

and controversy over the last century. Evidence cited to support the various

hypotheses has often been indirect and conjectural; for example, the two theories,

weeping and boosted lubrication, are apparently in complete contradiction of each

other indicating that there still remains a basic lack of knowledge of the

biomechanics involved in the load bearing of the articular cartilage. Conversely,

theories derived from a purely engineering point of view often demonstrate a lack

of understanding of the nature of biological systems.

More recent biomechanical evidence, first described by (Mansour & Mow 1977),

(Lai, Kuei et al. 1978) and reviewed by (Mow & Mak 1987), would seem to

suggest the simultaneous existence of both fluid exudation and imbibition under a

moving load in a system of “self-lubrication’. Hence, both the weeping and boosted

lubrication models are probably only partially correct.


79

It would appear that the attempts to isolate a single mode of lubrication with

respect to the synovial joint may have been misguided and somewhat fruitless as

there is considerable evidence to support a mixed lubrication regime. The joints

appear to enjoy all of the common physical modes of lubrication plus some novel

ones which are, perhaps, unique to the synovial joint. Many of the studies

completed regarding the modes of lubrication acting in the joint demonstrate the

futility of trying to ascribe a single mode of lubrication to the synovial joint. Few

engineering bearings operate under a single mode of lubrication so it would seem

ludicrous to expect such a complex structure as the joint to be able to behave

differently to some of the comparatively simple bearings that are utilised in

industry.

Engineers have been tackling the issue of joint lubrication in a slightly different

manner (Mow, Holmes et al. 1984; Hou, Holmes et al. 1989; Schreppers, Sauren et

al. 1991; Jin, Dowson et al. 1993), developing mathematical laws regarding the

characteristics of both the articular cartilage and the synovial fluid before going on

to determine how applicable these laws would be in vivo. Using known anatomic,

biochemical, kinematic and loading characteristics for a specific joint, one could, in

theory, calculate which lubrication system is likely to be acting. To date, there is

still no clear understanding of the lubrication mechanisms except that it does

involve both boundary lubrication and fluid-film lubrication acting together, the

importance of each mechanism depending on the type of loading to which the joint

is subjected.

Although evidence supporting the role of fluid-film lubrication is strong, cartilage

is undoubtedly better lubricated by synovial fluid than by saline (McCutchen

1966). If the advantage is not provided by the behaviour of the liquid between the

surfaces, it must result from the behaviour of the liquid at the surfaces therefore it

must be boundary lubrication.

The common theories of joint lubrication will now be briefly reviewed.


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4.2.2 Fluid-Film Models

Under initial consideration it is easy to see how fluid-film lubrication theory was

first selected for the method of joint lubrication. Simply, it is the only method of

lubrication known in engineering that can achieve such low values of friction as

reported in the human joint. Several different models based on fluid-film

lubrication have been proposed and will be discussed briefly in the following

sections.

4.2.2.1 Hydrodynamic Lubrication

In 1932 MacConaill proposed that joint lubrication was hydrodynamic (Fig. 4.5)

(MacConaill 1932). He theorised that a wedge-shaped film would be formed

between the articulating joint surfaces by the synovial fluid, hence bearing the load

and preventing friction and wear of the joint surfaces. However, there was no

explanation for the low friction of joints starting from rest and he hadn’t taken into

account the incongruent nature of the opposing surfaces. Also, it seemed unlikely

since hydrodynamic lubrication requires low loads and high surface velocities

which are not found in the human synovial joint.

Figure 4.5: Hydrodynamic Lubrication; Diagram showing the

formation of the pressure generated due to a wedge of fluid that

separates the moving bearing surfaces. (Dinnar 1975)

It had long been recognised that cartilage was permeable, fluid soaked

(Benninghoff, 1925 cited by (McCutchen 1983)) and not rigid. Despite the

knowledge presented by Beninghoff, most engineers treated the cartilage as a

standard, non-deformable, non-porous and smooth material and it wasn’t until the

late 1950s that lubrication theories allowed for the incongruent surfaces and the

porous and elastic nature of the articular cartilage began to emerge.


81

Fluid-film lubrication may function in a number of different situations and in a

number of different modes: hydrodynamic (light loads at high speed),

elastohydrodynamic (moderate loads and speeds), and squeeze-film mechanisms

(impact loads) including boosted lubrication and weeping lubrication (a

modification of both hydrostatic and squeeze film mechanisms). The source of the

fluid film in the joint capsule depends upon the joint kinematics and the magnitude

of joint loading. Both synovial fluid and cartilage exudate are viable sources of the

fluid film and the various fluid-film models implicate both possible sources

(Dowson 1990).

Hydrodynamic lubrication, as already described, was one of the earliest modes of

lubrication implicated within the joint capsule. This mechanism requires

uninterrupted motion in the same direction to maintain the integrity of the wedge

(Figure 4.5.) and is especially efficient in high speed bearings. These requirements

indicate that pure hydrodynamic lubrication is unlikely to be solely applicable to

the synovial joint which requires frequent changes of direction or efficient

functioning at slow speeds, up to 0.1m/s (Dowson 1973; 1990) or at rest. Further

problems with this mechanism are highlighted when one examines the fluid film

thickness: minimum fluid thickness is in the order of 10-7

-10-3µm during the peak

loading period of a normal walking cycle (Mow & Mak 1987). When compared to

the average height of the healthy cartilage asperities (approximately 2-6µm)

(Dowson 1990) it is obvious that hydrodynamic lubrication alone would rapidly

result in considerable wear of the cartilage and is inadequate under the conditions

set within the synovial joint.

4.2.2.2 Weeping Lubrication

In 1959 McCutchen proposed that a synovial joint could 'be thought of as a bearing

with a thick film of lubricant, where 'weeping' through the porous wall supplies

enough liquid to maintain the (fluid) film'. (McCutchen 1959) He surmised that

application of a load to the cartilage must pressurise the liquid within it and, if the

cartilages were permeable enough, the liquid would flow out to the rubbing

surfaces, thus carrying the load (Figure 4.6.). Using this information he tried a


82

system using Rubazote (closed cell rubber foam which has a pocketed surface,

lubricated with soapy water) and obtained coefficients of friction of less than 0.003

when the load was first applied. This slowly rose as the lubricant leaked away. The

lubrication system with which he worked was a form of hydrostatic lubrication in

which the interstitial fluid of hydrated articular cartilage would flow out onto the

bearing surface when a load was applied to it. The cartilage would act as a self

pressurising sponge. When the pressure was released the fluid would flow back

into the cartilage, i.e. self-pressurised hydrostatic lubrication. Because the cartilage

would appear to be weeping under load, this mechanism was termed ‘weeping

lubrication’. In 1967, McCutchen coupled this basic description of weeping

lubrication with a unique form of boundary lubrication known as ‘osmotic

lubrication’ (4.2.3.1.).

Figure 4.6: Weeping or Hydrostatic Lubrication; a) as load is applied

fluid flows towards the rubbing surfaces at high pressure, carrying the

load with minimal friction. b) when the load is removed the cartilage

expands, drawing in synovial fluid. (Adapted from (McCutchen 1978))

Later, with Lewis, (Lewis & McCutchen 1959) McCutchen tested his weeping

lubrication theory using cartilage. They showed that cartilage does exude fluid as

load is applied and, under typical joint loads, exudes enough fluid to form an

effective lubricating surface layer. Later, in 1970, Radin et al concluded that the

'hydrostatic or "weeping" mechanism is a significant functioning process in joints'.

(Radin, Paul et al. 1970)


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4.2.2.3 Elastohydrodynamic Lubrication

A variation of the hydrodynamic and squeeze-film modes of fluid-film lubrication

occurs when bearing surfaces are elastic enough for the lubricant pressure

generated by motion under a given load to cause elastic deformation of one or both

of the opposing surfaces i.e. both the resistance due to the viscosity of the lubricant

(synovial fluid) and the elastic deformation of the bearing surface (articular

cartilage), playing a prominent role in the lubrication process (Mow & Mak 1987).

Dintenfass, in 1963, was probably the first in the biological field to highlight the

significance of the deformability of the articular cartilage in fluid-film mechanisms.

He postulated that the elastic deformation of the cartilage could

spread the load to a larger bearing area, thus reducing the velocity necessary to

maintain a fluid film between the bearing surfaces (Figure 4.7.). His theory

depended on 'the existence of a thixotropic and elastic fluid (synovial fluid)

between the articular surfaces, that the area of the load-carrying film depends on

the elasticity of the cartilage, and that the velocity gradient existing in the gap

between the articular surfaces depends also on the lateral deformation of these

surfaces' (Dintenfass 1963). Dintenfass found support through Medley, Dowson

and Wright (Medley, Dowson et al. 1984).

Figure 4.7: Elastohydrodynamic Lubrication; The top surface in this

diagram is deformable, providing a larger fluid film when load is

applied.(Adapted from (Dowson, Wright et al. 1969))

As with hydrodynamic lubrication, the thickness of the film developed from

elastohydrodynamic lubrication would not always be adequate to avoid wear and

tear of the cartilage asperities (Tanner 1966; Dowson 1966-67; Higginson 1978;

Dowson, Unsworth et al. 1981; Mow & Mak 1987). One model which was claimed


84

to overcome the problems of fluid thickness was a model derived from EHL called

microelastohydrodynamic lubrication (mEHL). Microelastohydrodynamic

lubrication refers to the elastic deformation of the asperities (Figure 4.8.) of the

articulating surfaces under load, decreasing the risk of surface contact and allowing

a thinner fluid film to be maintained. In 1970 Bennett and Higginson suggested that

microelastohydrodynamic lubrication is present in the human synovial joint

(Bennett & Higginson 1970). They were later supported by Dowson and Jin who

found that the microelastohydrodynamic action effectively smooths the rough

cartilage surfaces allowing a sufficiently thick fluid film to separate the surfaces of

the articulating bone ends (Dowson & Jin 1986).

Figure 4.8: Microelastohydrodynamic Lubrication; Diagram showing

the deformation of the asperities on the surface of the cartilage under

load decreasing the risk of contact and allowing maintenance of a thinner

fluid-film. (Adapted from (Dowson & Jin 1986))

4.2.3 Mixed Lubrication Models

In fact, problems with the theoretical predictions of film thickness in synovial

joints has been a major stumbling block for many of the proposed lubrication

theories and is probably the strongest argument for a mixed lubrication regime

within the joint.

It has been said that either hydrodynamic lubrication or boundary lubrication by

themselves are far too crude to represent the complex lubrication mechanism in

joints (Dintenfass 1963). This has led to several ‘mixed’ lubrication models, more

recently called Adaptive Multi-mode Lubrication (Murakami, Higaki et al. 1998)

which is a combination of many different lubrication regimes occurring (Fig. 4.9)

at the one time or individual regimes occurring throughout the loading cycle.


85

Figure 4.9. Mixed lubrication showing that one lubrication regime does not

answer the operating conditions in the joint but a combination of mechanisms.

Source: (Panjabi & White 2001)

As discussed in 4.2.1. Jones used a finger joint as the pivot of a pendulum to see

how the friction varies and whether or not it is proportional to the fixed load. The

results suggested mixed lubrication, with Jones concluding that human joints are

usually lubricated by fluid film lubrication but, when speed and/or eccentricity are

not enough to maintain a fluid film, a form of solid friction must occur, that is, the

surfaces come into contact. (Jones 1936) Jones' work on mixed lubrication has

received much support including Linn (Linn 1968), Dowson (Dowson 1973)) and,

Murakami et al (Murakami, Higaki et al. 1998).


86

Figure 4.10: Mixed Lubrication; When the fluid film fails, friction is

prevented by boundary lubrication. (Adapted from (Dowson, Wright et

al. 1969))

4.2.3.1 Osmotic Lubrication

In 1966 McCutchen suggested that mucin molecules might adsorb to the articular

surfaces at several particular points along the molecule leaving loops of mucin

chain still in solution. This would leave a higher charge density at the cartilage

surface compared to that in the bulk fluid, creating the effect of an osmotic

gradient. When a compressive load is applied to this layer of dissolved mucin

chains, it is resisted by a stress with the same origin as osmotic pressure; that is, the

tendency of solutes to distribute themselves evenly in a solvent (Davis, Lee et al.

1979). For this reason, McCutchen called this theory ‘osmotic lubrication’

(McCutchen 1966). It was McCutchen’s investigation into his osmotic theory that

led to the discovery that synovial fluid will only lubricate effectively after

sufficient soaking and that the friction will increase if resoaking is not allowed.

Both of these discoveries provide strong support for boundary lubrication.

4.2.3.2 Squeeze-Film Lubrication

Fein (1967) was the first to demonstrate the importance of such a mechanism in

synovial joint lubrication. He concluded that 'synovial joints are probably squeeze-

film lubricated with the squeeze film being replenished by hydrodynamic action

(entrainment of fluid when the joint is moved)'. The approaching surfaces generate


87

pressure (Figure 4.10.) in the lubricant as they squeeze it out of the area of

impending impact between them while the resulting pressure keeps the two

surfaces apart. The fluid must be squeezed out before the surfaces can come in

contact. This mechanism would fail if the maximal load were applied continuously.

However, if the load is only for short periods with the load being reduced while the

film remains reasonably thick, the film thickness can recover. In cartilage-on-

cartilage systems the film that forms in the transient area of impending contact has

been referred to as the “squeeze film”. Unfortunately, the work of Fein (1967)

ignored the permeability of the cartilage to water and small solutes. The effect of

cartilage permeability in a squeeze-film bearing would usually be to increase the

rate of leakage, thus reducing the time that such a bearing could support load

(Swanson 1979). However, in the articular joint, where synovial fluid fills the joint

cavity, the loss of water and small solutes would leave the hyaluronate and protein

between the bearing surfaces to potentially assume some role in lubrication. Such

an effect is covered in detail in the next section.

Hou et al and Hlavácek have both performed mathematical analyses of the squeeze

film theory, concluding that squeeze film lubrication is likely to occur but is most

probably supplemented by either boosted or boundary lubrication (Hou, Mow et al.

1992; Hlavacek 1995). Squeeze film lubrication occurs when a film of viscous

fluid is caught between a pair of normally approaching surfaces. The pressure due

to the applied normal force resists the tendency for the surfaces to approach each

other. (Archibald 1969)

Figure 4.11: Squeeze Film Lubrication; The arrows indicate the

movement of fluid away from the load-bearing region leaving an

enriched film of synovial fluid between the surfaces. (Adapted from

(Hou, Mow et al. 1992))


88

4.2.3.3 Boosted lubrication

Walker et al (1970) suggested that as load increases the low molecular weight

fraction of the synovial fluid is forced into the cartilage pores leaving trapped pools

of enriched synovial fluid in the rough surfaces of the cartilage. This theory was

called 'boosted' lubrication. This is a combination of both boundary and fluid

conditions, proposed independently by Maroudas (Maroudas 1967) and Walker

(Walker, Dowson et al. 1968). As the articulating surfaces approach each other, the

water and small solutes (<5µm diameter) in the synovial fluid are uniformly

squeezed out from between the region of contact and taken up into the cartilage

matrix. The closing gap, as load is applied, between the bearing surfaces increases

the resistance to sideways movement of the fluid from the gap tangent to a point

beyond the resistance of flow into the cartilaginous bearing material normal to the

articulating surface (Figure 4.11.). The effective pore size of healthy, non-

pathogenic cartilage (20A to 65A) (McCutchen 1962; Dowson, Wright et al. 1969)

does not allow passage of the macromolecular components of the synovial fluid,

including hyaluronic acid (HA) or the HA-protein complex (HAP), into the

cartilage matrix. The articular surface acts as an ultrafiltration membrane so that a

highly concentrated and viscous layer is left at the cartilage surface. Walker et al

postulated that this ‘gel’ layer was capable of carrying much greater loads for a

much longer time than normal synovial fluid with the diluted concentration of

HAP. It may be that the micro asperities at the articular surface provide “traps” for

the gel, providing enhancement for the formation of gel pockets at the joint surface

(Walker, Dowson et al. 1969; Walker, Sikorski et al. 1970). More recently, Tandon

et al have proposed a mathematical model that supports Walker's theory of boosted

lubrication (Tandon, Bong et al. 1994).


89

Figure 4.12: Boosted Lubrication; a) path of the fluid flow into the

cartilage surfaces while loaded. b) schematic diagram of the pools of

enriched synovial fluid formed on the surface of the cartilage. (Adapted

from (McCutchen 1978)

4.2.4 Boundary Lubrication Models

Charnley first suggested human joints acted under pure boundary lubrication in

1959 (Charnley 1959). Even before examining the problem experimentally there

were several theoretical criticisms which make the hydrodynamic theory unlikely.

Firstly, the articular cartilage, which is present as a layer about 3.25mm thick over

the sliding surfaces of the joint, is very resilient, being easily indented by the

pressure of the thumb-nail. An ankle joint of an adult male has a projected surface'

area of less than 13cm2, so that a man weighing 75kg carrying a 45kg load on his

shoulders will expose an ankle joint to pressures of about 10kg/cm2. There can be

little doubt that these resilient surfaces are intimately applied to each other over the

whole area even when not carrying loads. Secondly, there is the well-known fact

that hydrodynamic lubrication is not suited to conditions where the motion is

reciprocating, because no sooner has a fluid wedge been established for motion in

one direction than it is destroyed as motion starts in the other. Thirdly,

hydrodynamic lubrication is not easy to achieve with slow-moving surfaces under

heavy loads. In addition the in-viscous nature of synovial fluid and its shear

thinning behaviour would increase the difficulty of forming a fluid film. In further

support of boundary lubrication, Dowson showed that the fluid film thickness can

be maximised by increasing the femoral head diameter (Dowson, Fisher et al.

1991) but in considering the evolution from large femoral heads to smaller femoral


90

heads in prosthetic design this further reduces the chances of a suitably thick fluid

film ever forming (Hutchings 2003). Wang et al noted that the larger the femoral

head the worse the fluid-film lubrication condition (Wang, Essner et al. 1998).

Charnley came to this conclusion of pure boundary lubrication when he discovered

that there was little variation in friction with speed in pendulum experiments

similar to Jones’ (Unsworth 1991). Caygill et al came to the same conclusion in

1969 and suggested that hydrodynamic lubrication be discarded in favour of

alternative mechanisms (Caygill & West 1969). Boundary lubrication requires both

strong adsorption to the bearing surfaces and strong cohesion between the adsorbed

polymers. Boundary lubrication is said to occur when the surfaces of the bearing

solids are separated by a film of molecular proportion which are bonded in some

way to them. This type of action is more suited to slow reciprocating motion under

heavy loads.

Figure 4.13: Boundary Lubrication; The surface layer prevents the

articulating surfaces from coming into contact.(Adapted from (Wright &

Dowson 1976))

The essential requirement for boundary lubrication is the provision of a boundary

lubricant. Although the operating conditions of the joints’ indicate boundary

lubrication the existence of a boundary lubricant is necessary to validate the theory.

4.2.5 The Search for the Boundary Lubricant

It was obvious to everyone working in the field of joint lubrication that the

lubricant for fluid film lubrication had to be synovial fluid. However, the identity

of the boundary lubricant was not nearly so obvious. The search for an actual


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‘lubricating factor”, as required under boundary conditions, began well after the

start of the search for the lubrication mechanism itself. During the 1960s, research

groups were starting to analyse the synovial fluid in greater detail as it was

becoming more widely accepted that a boundary mechanism had a role in the

lubrication of the joint. The lubricant had to be contained within the synovial fluid

and also be located at the articulating surface. Initially there was little difference in

the fractions of synovial fluid that were identified but slowly it became easier to

characterise these fractions and to identify the role of each fraction. This led to the

discovery of fractions within fractions, i.e. sub-fractions. Gradually the identity of

the indigenous lubricant has emerged.

The role in lubrication of the macromolecular components of synovial fluid was

investigated because these constituents, collectively known as synovial mucin, are

one of the distinguishing features of synovial fluid when compared with blood

plasma (McCutchen 1962). Linn and Sokoloff analysed the fluid exuded from the

cartilage and found that it was essentially water and electrolytes (Linn & Sokoloff

1965). If the superior lubricating abilities of synovial fluid as compared to water

are supplied by the mucin, it is obvious that their supply is not from within the

cartilage. Thus, this work confirmed the general opinion that the source of the

lubricating factor is the synovial fluid.

Experiments to test synovial fluid lubrication have, as described, often used

systems involving cartilage rubbing on glass or cartilage rubbing on cartilage using

either saline or synovial fluid as the lubricant. Neither of these systems eliminates

the role of the interstitial fluid and the possibility of boundary lubrication from

substances adsorbed to the cartilage surface and so are not conclusive in identifying

the active lubricating mechanism. However, they are good systems in which to

compare the lubricity of different solutions and surfaces. Several experiments

(Ropes, Robertson et al. 1947; McCutchen 1966; Tanner 1966; Wilkins 1968) have

used alternative systems; for example, rubber rubbing on glass with either synovial

fluid or saline as the lubricant. The trial of McCutchen (1966), using rubber on

glass, demonstrated that synovial fluid was a superior lubricant, compared to 0.9%

saline, in the absence of the cartilage. Some of the other experiments which used


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articular cartilage for at least one of the rubbing surfaces did not show a clear

difference between synovial fluid and saline, at least not over a short period of time

(Little, Freeman et al. 1969; Radin, Swann et al. 1970). Unsworth and Dowson et al

wiped the cartilage surface dry before testing. Under a load of 800N or greater, the

‘dry’ cartilage performed equivalent to that lubricated with synovial fluid

(Unsworth, Dowson et al. 1975). Hence, the low coefficient of friction measured at

the joint surface would seem, to some extent, to depend on substances left on the

cartilage surface.

As just mentioned, McCutchen performed lubrication tests on the synovial fluid in

a system using surgical rubber against glass microscope slides. He found that

lubrication was poor until the rubber and glass had been in contact with the

synovial fluid for some minutes, indicating that a chemical reaction must occur

between the rubbing surfaces and the lubricant, as might be expected if a boundary

lubrication mechanism were acting. McCutchen further analysed the synovial fluid

using ultrafiltration of the synovial fluid with filters of varying porosity

(McCutchen 1966). He demonstrated that use of a 0.22µm filter retained the

lubricating ability in the residue, a larger porosity (0.65µm) allowed all of the

lubricating ability to be completely filtered. With a 0.45µm filter, the lubricating

ability was split between the filtrate and the residue. When using hyaluronidase

treated synovial fluid, a 0.1µm filter system divided the lubricating ability between

filtrate and residue. This suggested that the lubricating ability of the synovial fluid

was related to the hyaluronic acid, the enzymatic digestion breaking up the

lubricating molecules.

This implication of the hyaluronic acid, the component of synovial fluid that

imparts viscosity to the synovial fluid, in joint lubrication was supported in general

by most other studies preceding this work (e.g. (Ogston & Stanier 1953)), and

several more which followed McCutchen’s study (e.g. (Chikama 1985; Laurent,

Laurent et al. 1996; Marshall 2000; Mori, Naito et al. 2002)). But as discussed in

the overview (2.1.1.) HA does little more than effect the viscosity of SF in terms of

lubrication as it has been shown to fail to lubricate under any significant load.


93

4.2.5.1 Enzyme Studies

Research following on from this work of McCutchen also treated synovial fluid

with various enzymes to selectively destroy first the polysaccharide and then the

protein (Linn 1968; Linn & Radin 1968; Wilkins 1968), in order to determine

which part of the mucin component was essential for boundary lubrication.

Cleavage of the polysaccharide, using a 10 minute digestion protocol, with bovine

testicular hyaluronidase left a watery product which lubricated as well as whole

synovial fluid, something already noted by McCutchen, (1966). This was further

evidence that the viscosity or rheology of synovial fluid was not the vital

component in the joint lubrication system. However, extended digestion with the

hyaluronidase (43 hours at 38°C, pH 5.2) did affect the lubrication abilities under

boundary lubrication conditions in the study by Wilkins (1968), suggesting that, to

some degree, hyaluronic acid is required. However, these results must be

considered in light of the experimental conditions. The 10 minute digestion was

performed at 25°C and at neutral pH. The conditions for the extended digestion

were vastly different and could have had more widespread effects on the synovial

fluid than the short digestion. Linn and Radin found no deterioration in lubricating

ability following extended digestion (24 hours) under the same conditions (Linn &

Radin 1968).

Wilkins found that the separation of mucin from the synovial fluid by ultrafiltration

followed by treatment with proteolytic enzymes destroyed the lubricating ability

under conditions of boundary lubrication, even though the viscosity remained

completely intact (Wilkins 1968). The ultrafiltration was necessary as whole

synovial fluid contains protease inhibitors (Davis, Lee et al. 1979). Treatment with

papain also destroyed the lubricating ability of the synovial fluid. This strongly

indicated that the protein part of the synovial mucin was essential to its lubricating

ability, even though it accounts for only a small part of the total molecular weight

of the synovial mucin. Wilkins went on to suggest that the protein must act in a

relatively small domain, possibly serving as the anchor by which mucin ‘clings’ to

the surface or as a link to some “small, undiscovered anchoring group”. Hence, the

intact protein component of the synovial fluid is essential for boundary lubrication.

While the hyaluronic acid of the mucin complex also seems to be necessary, its


94

natural length can be considerably shortened before any detrimental effects on

boundary lubrication are obvious.

Jay (Jay & Cha 1999) was able to show that phospholipase digestion didn’t cause

the friction to increase by much whereas trypsin digestion caused the friction to

increase dramatically in contradiction to Hills’ (Hills & Monds 1998) studies which

showed the opposite. This has led to some debate (Hills & Jay 2002) and is still a

matter of current research.

4.2.5.2 Lubricating Glycoprotein

Radin et al pursued the implication that protein was essential for lubrication of the

cartilage (Radin, Swann et al. 1970). To test whether or not a protein fraction was

the active lubricant, the group had to separate the hyaluronate component of the

synovial fluid from the protein component without disrupting the physiochemical

properties of either component. This was achieved through density gradient

sedimentation equilibration. All of the hyaluronate banded in the middle of the

gradient, while the gross protein content was present in the top layer of the

gradient. The lubrication abilities of the different fractions were tested using a

modified Linn arthrotripsometer, which enabled the measurement of µ in

continually oscillating joints (Linn 1967; Radin, Paul et al. 1970). The hyaluronate

fraction showed no lubricating advantage over buffer, but the protein fraction had

lubricating abilities equivalent to that of whole synovial fluid. Further

characterisation of the protein fraction continued and a rigorous purification and

separation protocol was developed for the synovial fluid. The major glycoprotein

constituent was isolated from the gross protein component and shown to contain

boundary lubricating ability equivalent to that of whole synovial fluid (Swann &

Radin 1972; Swann, Sotman et al. 1977; Swann, Hendren et al. 1981). Because

plasma proteins were not known to lubricate, this one was considered to be

‘unique’ to the joint and was termed a lubricating glycoprotein (LGP) or “Lubricin”

(Swann, Slayter et al. 1981).

Following thorough efforts to characterise this new glycoprotein, it was established

that carbohydrate constituents represent approximately 44% (w/w) and amino acid


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constituents approximately 43% (w/w) of the molecule. However, 9.2% -13% of

the molecule remained unknown (Swann & Radin 1972; Swann, Sotman et al.

1977; Swann & Mintz 1979; Swann, Hendren et al. 1981; Swann, Slayter et al.

1981; Swann, Silver et al. 1985). Although the lubrication analyses of the LGP

fractions were performed under boundary conditions, the ability of the LGP to bind

to a surface had not been demonstrated until Swann et al carried out binding studies

using iodinated LGP to investigate the ability of the LGP to adsorb to cartilage.

This study indicated that 14% of the radioactive LGP was able to bind to the

cartilage.

The implication of Lubricin as a potential boundary lubricant for AC was discussed

by several authors (Swanson 1979; Swann, Bloch et al. 1984; Furey & Burkhardt

1997; Jay 2004), but no attempts were made to verify the presence of Lubricin on

the AC surface (Sarma, Powell et al. 2001).

At the time when the LGP molecule was being characterised, Davis and co-workers

were studying the detailed mechanisms involved in boundary lubrication for the

excised disks of bovine nasal cartilage (Davis, Lee et al. 1979). They used an

apparatus that was designed to discourage hydrodynamic effects and proposed the

existence of a thin, viscous structured hydration shell at the articular surface with

multiple layers of LGP held together by an alternating sequence of hydrophobic-

hydrophobic and hydrophilic-hydrophilic bonds. Davis et al proposed that one

portion of the LGP was adsorbed to the surface of the cartilage (the behaviour one

would expect of an amphipathic molecule at an interface). These mutual

electrostatic repulsive forces between the charged polysaccharide components

could enhance the boundary lubrication process. This model of the LGP molecules

being bound in layers to the articular surface has now reached a reasonable level of

acceptance in both the physical sciences and biology (DeHaven 1990; Jay 1990;

Mow, Ateshian et al. 1993).

4.2.5.3 Lipids

The presence of traces of fat in bovine synovial fluid was reported over a century

ago (Frerichs, 1846, cited by (Bole & Peltier 1962)). Stockwell (Stockwell 1965)


96

estimated the total fat content of articular cartilage to be about 1-2% of the wet

mass and McCutchen (McCutchen 1978) has commented on the “oily” nature of

the cartilage surface. Despite the accepted existence of lipid within the joint, there

has been little interest in it in terms of lubrication, despite the fact that fats are well

known to be slippery. The first study to investigate the role of lipid in joint

lubrication was that of Little et al (Little, Freeman et al. 1969). By using the hip

joint as a pivot of a Stanton pendulum, they showed that synovial fluid was a

lubricant but it was not the only lubricant in the joint. The team felt that there may

also be an intrinsic factor within the cartilage which would aid lubrication. Simple

tests were designed utilising synovial fluid and Ringer’s solution followed by a

study of the oscillation pattern of the joint. These showed linear decay of free

oscillation independent of the load or the rate of movement. This was a strong

indicator for the lubrication mechanism being boundary in type.

Little et al noted two factors during the experiments that indicated the presence of a

lubricant in, or adsorbed to, articular cartilage. (1) A very low µ could be obtained

using Ringer’s solution (rather than synovial fluid) on the cartilage and, (2) µ was

greatly increased following soaking of the cartilage surfaces with a fat solvent (2:1

chloroform/methanol). The extraction of fat left the cartilage unchanged both

histologically (as assessed using the following stains; haematoxylin, eosin,

toluidine blue and alcian blue) and in gross appearance. Further, the permeability

and compressive stiffness of the cartilage was not altered.

Little et al showed that fat could be readily demonstrated histologically in cartilage.

Staining cartilage with Sudan Black and Sudan 111 revealed fat at the superficial

layer of the articular cartilage. Preliminary work treating cartilage surfaces with

wheat germ lipase and also carbon tetrachloride produced increases in the

coefficient of friction similar to rinsing the cartilage surface with fat solvent.

Little’s team concluded that the lubrication was boundary in nature, even in the

presence of synovial fluid, and that the lipid present in articular cartilage enhanced

the lubrication mechanism by lowering the frictional characteristics of the two

surfaces. Unfortunately, despite the clear implications provided for a role of lipid as

the active boundary lubricating ingredient in the synovial fluid, this study into the


97

role of lipids stood virtually on its own until the 1980s. Hills reignited the interest

in the role of lipids, in particular for lubrication within the body in the early 1980s

as best described in his book ‘The Biology of Surfactant’ (Hills 1988). His work on

lipids carries on to this day.

More recently Benz et al confirmed some of Little’s findings in that µ indicated a

strong dependence on the lipids present on the cartilage surface and the removal of

which (with a 2:1 mixture of chloroform: methanol) caused an increase in µ (Benz,

Chen et al. 2005). Amongst other things, their results confirmed the predominant

role played by the surfaces rather than the fluids between them in joint lubrication.

Another recent study concluded that: “A layer of phospholipids is present on the

surface of articular cartilage. This layer can clearly be viewed in the SEM and

OM….The lipid layer acts as a boundary lubricant and is critically important to the

proper functioning of synovial joints” (Ballantine & Stachowiak 2002). They

suggested that proper functioning of synovial joints requires the presence of the

articular cartilage surface lipid layer and that removal or damage to this layer is a

key factor in the onset of OA.

4.2.5.4 Surface-active Phospholipid

One of the types of lipid present in the synovial fluid that could be readily acting as

a lubricant is phospholipid (3.4.5.) which constitutes at least one third of the lipids

present in the synovial fluid of the normal healthy joint (Rabinowitz, Gregg et al.

1984). Phospholipids are used in industry to enhance the boundary lubricating

abilities of oils primarily to reduce both the break-out force and, in consequence,

wear (Munro 1964; Larson & Larson 1969). Although few studies have been

performed on the lubricating abilities of surface-active agents in biology, those that

have been completed have shown promising results. Gvozdanovic et al (1975)

investigated the formation of lubricating monolayers at the cartilage surface during

their search for suitable synthetic synovial fluids (Gvozdanovic, Wright et al.

1975). They compared the effect of several surface-active substances with synovial

mucin using the cartilage on glass system to assess friction. An anionic surfactant

(sodium lauryl sulphate) behaved in a similar manner to the mucin at pH 7-10, but


98

a cationic surfactant (cetyl-3-methyl ammonium bromide) was not as effective and

required a pH of 6. In each case the initial coefficient of friction was low, typically

around 0.003-0.004, but it increased with the time of loading, the increase being

faster with the anionic surface-active chemical. It was concluded that electrostatic

forces alone could not account for the observations and that monolayers of

boundary lubricant formed from the surface-active materials were bound to the

cartilage more strongly than the synovial mucin. Gvozdanovic et al (1975) had

noted that cartilage surfaces needed prolonged washing before the lubricating

ability was eliminated. The same was found following the trials of surface-active

substances. When using the surface-active solutions, the value of mu decreased as

loads increased, far exceeding normal physiological loads.

In their studies, Gvozdanovic et al (1975) made no mention of the highly surface

active phospholipid which is already present in the synovial fluid; yet

phospholipids offer much potential for providing boundary lubrication in vivo. In

fact the unidentified 9.2—13% portion of LGP discussed in 4.2.5.2 has been

identified to be lipidic in nature (Schwarz & Hills 1998) and it seems more than

coincidental that this is approximately the same amount of Lubricin that was shown

to adsorb to the cartilage surface. Hence these lipids have been implicated as the

active boundary lubricant in synovial fluid and labelled Surface-Active

Phospholipid (SAPL). A review of boundary lubrication by SAPL will be

discussed in the following chapter that will show that the surface-active

phospholipids found in vivo have the capability of providing good boundary

lubrication at high load, as is necessary at times in the articular joint.

4.3 Artificial Joint Lubrication: A Review

Much of the discussion on the tribology of natural joints in the previous sections

applies equally here with the exception being that the replacement bearing does not

enjoy the unique properties bestowed by the original bearing material cartilage.

Therefore, the theories that relied upon the porous, complying nature of cartilage to

operate are not feasible in the artificial joint where the articular surfaces are

replaced with hard man-made materials.


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In comparison to the lubrication of the natural joint the artificial joint has received

little attention. Wang concluded in his review that one of the areas in artificial joint

tribology that is still the least understood is the mechanism of lubrication (Wang,

Essner et al. 1998). The majority of tribology studies on artificial joints are wear

related and will be discussed in (4.3.4.).

There has been relatively little work on the determination of the lubrication regime

for joint prostheses (Dumbleton 1981; Jalali-Vahid, Jagatia et al. 2001). This is

because it has been felt that lubrication is, so to speak, the dependent variable,

being specified by the design of the prosthesis, the nature of the fluid present, the

patient activity and the materials and surface finish of the sliding surfaces. It has

been felt that the lubrication regime is of the boundary type and that the best that

can be hoped for is the adsorption of surface active molecules on the sliding

surfaces, thus allowing the continued operation of the boundary lubrication

(Dumbleton 1981). In fact, it was that type of reasoning which made metal/plastic

prostheses so attractive, since it was thought that such devices were "self-

lubricating" and so the presence or absence of lubrication from the joint fluid was

of no importance. Replacement joints usually operate in the presence of a fluid

similar to healthy synovial fluid, but it is important to note that the original design

intent for those joints made of a metal-on-plastic combination of materials was so

they could perform adequately as dry bearings (Dowson, Wright et al. 1969). As

Unsworth mentioned in his review on the tribology of artificial joints, “Design for

lubrication using the body’s own lubricant has not, to date, been a feature of

artificial joints (Unsworth 1991). Recently there have been studies which indicate

that lubrication of the "mixed" type may be expected. Although the idea of fluid-

film lubrication in artificial joints has been explored, it faces more challenges than

fluid-film lubrication that has been shown in the natural joint due to the hard, non-

compliant materials used in total joint replacements.

In consideration of the artificial joint as a replacement bearing of the original, the

major and only difference is the bearing materials. The loading and operating

conditions remain the same and the same indigenous lubricant remains. The


100

bearing materials used in artificial joints have historically been selected for their

intrinsically low friction which typically means hard, metallic or ceramic materials

which are radically different to the original articular cartilage. The way that the

indigenous lubricant interacts with these surfaces is of interest as it is this

interaction that will determine the tribological performance and longevity of the

TJR.

Essentially the best that prosthesis designers with current technology can reasonably hope

for is boundary lubrication (Dumbleton 1981). Boundary lubrication may not be the

dominant mechanism in the natural joint but it is instrumental to the lubrication of

the joint under certain conditions as shown in the previous sections. Given this

knowledge TJRs will require the services of the identified boundary lubricant to

operate effectively in the boundary lubrication regime. Surfaces that can interact

favourably with the boundary lubricant are of utmost importance.

Many of the major problems encountered in prosthetic design are tribological in

nature. In the first place the rate of wear has to be sufficiently low to enable the

joint to operate satisfactorily as a bearing for the remaining life of the human

machine. Secondly, the friction force developed between the sliding surfaces

should be minimised, not only to provide freedom of movement for the patient, but

also to limit the severity of the problem of implant fixation.

Most replacement joints are either of the metal-on-metal or metal-on-plastic

varieties. If two metals are used it is customary to employ like materials to avoid

corrosion problems in the hostile environment of the body. Such a combination of

metals normally leads to high friction and is generally avoided in engineering

bearings. In the human joint many successful metal-on-metal bearings based upon

chrome-cobalt alloys have been designed and used. They have a relatively low

wear-rate but the friction forces and torques are high compared with metal-on-

plastic bearings. The friction coefficient for metal-on-metal prostheses has been

reported as high as 0.3 and as low as 0.04 for a Charnley type metal-on-plastic

prosthesis (Unsworth 1991). This µ value reported for a Charnley TJR is quite

remarkable and has not been seen to be as low by other researchers. Figure 4.14


101

indicates a range of values collated and their comparison to the natural joint.

Regardless of the actual values for the coefficient of friction, metal-on-plastic

prostheses offer the better frictional performance but unfortunately wear is still

known to occur with consequential effects.

Figure 4.14. Dependence of the efficiency on the friction coefficient in natural

and artificial joints. Source: (Gavrjushenko 1993)

More recent attempts to improve the lubrication of artificial joints have included

attempting to mimic the articular cartilage with elastomeric bearing surfaces and

even attempts to ‘regrow’ the original bearing surfaces with a biological equivalent

via tissue engineering (Shi 2004).

It is well established that boundary or at best mixed lubrication regimes exist in

artificial joints. However all models will be presented here.

4.3.1 Fluid Film Models

Several groups have investigated the possibility of hydrodynamic lubrication in

artificial joints (Scholes & Unsworth 2000; Jalali-Vahid, Jagatia et al. 2001; Jin,

Medley et al. 2002). The development of a fluid film is possible in artificial joints


102

under certain conditions; however, it has been concluded that the calculated film

thickness is not greater that the asperities and hence asperity contact will still exist

even though reduced by a fluid film in UHMWPE hip joint replacements (Jalali-

Vahid, Jagatia et al. 2000).

Other groups have promoted EHL through the use of elastomeric bearing surfaces

that mimic the mechanical properties of articular cartilage but have faced

difficulties with attaining the desired lubrication under all operating conditions (Jin,

Dowson et al. 1997; Oka, Kumar et al. 2000; Virdee, Wang et al. 2003; Scholes,

Unsworth et al. 2005).

The search is continuing for biomaterials that can effectively mimic the properties

of cartilage and provide efficient lubrication under all operating conditions of the

joint. One such group (Williams, Powell et al. 1995) has attempted to improve the

poor tribological performance of these elastomeric bearing surfaces when a fluid-

film is not present by modifying the surface to adsorb DPPC. This is the

development of a model that covers more of the operating conditions of the joint.

Fluid-film lubrication via EHL when the velocities in the joint a sufficiently high

enough and boundary lubrication via surfactant at low joint velocities. This can be

regarded as a hybrid lubrication model combining the principles of both fluid film

lubrication and boundary lubrication which by nature will cover the middle ground

of mixed lubrication also.

4.3.2 Boundary Lubrication Models

It is well established that boundary lubrication or mixed lubrication is the best that

can be hoped for in the artificial joint (Unsworth 1975; 1978; Dumbleton 1981).

Boundary lubrication is more likely to occur in TJR because the bearing surface is

no longer cartilaginous but hard and therefore non-compliant and non-porous.

Because of this the lubrication regimes that relied upon the properties of cartilage

struggle to exist in the artificial joint; for example, interstitial pressurisation,

weeping, osmotic and boosted, essentially all the regimes that were fluid-film


103

related. As discussed in the previous section the calculated film thicknesses for

artificial joints is not great enough to cover the asperities on the bearing surfaces

and hence the last line of defence in lubrication falls to boundary lubrication.

Thankfully effective boundary lubrication is known to exist in the natural joint

(4.2.3.) and the artificial joint is also able to benefit from the body’s provision of a

boundary lubricant. In a study the first of kind, Purbach et al were able to

demonstrate the presence of surface active phospholipids on the surface of

retrieved hip implants (Purbach, Hills et al. 2002), thus proving that an indigenous

boundary lubricant is present even in arthritic joints and that the synovial cells

continue to produce lubricant.

An interesting study by Kobayashi et al directly observed the lubricating behaviour

of various joint surfaces indicating that, in fact, the cartilaginous surfaces did

benefit from a fluid-film between the surfaces whereas the artificial materials did

not (Kobayashi & Oka 2003). They predicted that boundary lubrication was all that

could be expected as direct contact of the bearing surfaces did occur. They

concluded that to improve the quality of artificial joints the characteristics of the

implant material surface and the synovial macromolecules must be considered i.e.

boundary lubrication.

Several groups have attempted to modify the surface of biomaterials to enhance

boundary lubrication (Williams, Powell et al. 1995; Williams III, Gilbert et al.

1997; Widmer 2002; Benz, Chen et al. 2005; Heuberger, Widmer et al. 2005;

Serro, Gispert et al. 2006). This was achieved by surface modification techniques

discussed in further detail in the next chapter with the goal of attracting the

lubricating molecules present in synovial fluid to the surface of the bearing

materials that would act as a protective film and hence reduce friction.

4.3.3 Mixed Lubrication Models

As discussed in the natural joint lubrication sections mixed lubrication occurs in

the joint when the operating conditions cause the mode of lubrication to change

from boundary to fluid-film. The same applies in artificial joints although as


104

explained above, the likelihood of a fluid-film being generated at all is low and

hence the best that the artificial joint can hope for is a mixed regime, whereby some

of the load is carried by a thin fluid-film and the remainder is handled by the

boundary lubrication mechanism (Unsworth 1995; Jalali-Vahid, Jagatia et al.

2001).

4.3.4 Tribological Studies for total joint replacements

Research is ongoing in the field of tribology of artificial joints with the goal of

improving the quality and durability of prostheses. The main focus is the

development of new biomaterials that have excellent tribological performance. The

research of the tribology for artificial joints is generally conducted in two areas: the

testing of suitable biomaterials for their frictional performance and the testing of

prostheses for their wear determination.

To study the tribology of biomaterials simple laboratory testing machines are

employed called tribometers (Figure 4.16.).

Figure 4.15. Geometric configurations of various tribometers. Source:

(Dumbleton 1981)

(a) pin-on-flat (c) annulus-on-flat

(b) pin-on-disc (d) disc-on-plate


105

To study the tribology of prosthetic joints in conditions similar to those prevailing

in the human body, joint simulators are necessary. The simulator study should

produce wear mechanisms, wear rates and wear debris similar to those seen

clinically. It is difficult to evaluate various simulators because of the lack of

consistent test parameters and the fact that even different tribocouples react

differently to the same lubricant (Brown & Clarke 2006).

The lubricant is a crucial parameter in the tribological studies for both the material

testing using tribometers and the simulator studies with prosthetic joints (Ahlroos

2001) and is one consideration in this thesis. Given that synovial fluid is the only

source of lubricant in the body and this is what natural and artificial joints must

operate with, it would follow that this is what should be used in tribo tests for

artificial joints. Unfortunately, as shown by Brown & Clarke in their excellent

review of the lubrication conditions for tribo testing, synovial fluid, even though

being the biological lubricant, it is present in far too small of quantities to be used

exclusively in tribo tests (Brown & Clarke 2006). Animal synovial fluid such as

bovine synovial fluid and equine synovial fluid have been used but are also

impractical due to not only the lack of quantity but the collection process which is

vulnerable to contamination. In addition, body fluids from other species may not

correlate to the human body and disease may also play a role (Coller 2002). Thus,

researchers have had to adopt alternative fluids for use as a lubricant in tribo tests.

So-called pseudo-synovial fluids (PSF) choices have included de-ionised water,

mineral oil, gelatin solutions, physiological saline, bovine serum, plasma, and

artificial lubricants (Brown & Clarke 2006). Bovine serum had emerged as the

lubricant of choice for wear simulator studies and the others have been deemed

inappropriate for use as tribo testing lubricants (Brown & Clarke 2006). Bovine

serum had been selected purely for the reason that it produces results most closely

matching clinical results with polyethylene bearings. Conversely the other

lubricants were deemed not appropriate because the wear results they produced did

not match clinical results. For example Ahlroos found that DPPC produced

negligible wear but yet concluded that DPPC was not important to the tribology of

prosthetic joints because the zero wear results did not match the much higher

clinical wear results! (Ahlroos 2001).


106

The key to selecting a suitable lubricant for tribo testing is to provide a lubricant as

close as possible to the biological lubricant. Several boundary lubricants have been

proposed and used in tribo testing as indicated in Table 4.1.

Table 4.1. Boundary lubricants within SF suitable for tribo tests. Source:

(Brown & Clarke 2006)

Brown & Clarke concluded that proteins may be essential in lubricating metals and

ceramic bearings but that they actively promote and increase the wear of polymeric

surfaces.

A standardised test lubricant has been proposed by several researchers including

Liao et al (Liao, Benya et al. 1998) which would certainly help to qualify test

results across the world.


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4.4 Summary

In applying the principles of lubrication engineering to the natural joint it becomes

apparent that not one but all lubrication mechanisms known to the engineer would

be needed to explain the excellent tribological performance of this biological

bearing. The extremely low friction achieved by the joint would suggest fluid-film

lubrication but the relatively slow joint velocities, high velocities and stop/start

motion do not support this but rather a boundary lubrication regime. Currently

there is no single comprehensive theory that covers all the friction and lubrication

characteristics existing within a joint cavity. The tribological efficiency of synovial

joints is most probably the result of a series of complicated dynamic interactions

occurring between the synovial fluid, macromolecular components, the articular

cartilage surface and matrix and the interstitial water. The unique lubricating

properties are not solely due to either the synovial fluid, or to the articular cartilage

but to some complex synergistic interaction of both.

It is clear that a combination of lubrication regimes exist when considering the

operating nature and loading of the joint within an ambulation cycle. The

lubrication for the periods of extended standing, heel strike and toe off can only be

explained in lubrication engineering by a boundary lubrication mechanism. The

swing through and weight transfer phase may be answered by a fluid-film

mechanism or a mixed lubrication regime. Plainly boundary lubrication has an

instrumental role to play in the lubrication of the natural bearing if only for those

times of high loads and very low velocities because the near frictionless

performance of the bearing continues through these times. This indicates the

presence of some ‘substance’ that keeps the bearing surfaces sliding over each

other so effortlessly. This substance or protective film/coating is referred to as the

boundary lubricant. For effective boundary lubrication to occur an effective

boundary lubricant must exist. One such boundary lubricant identified in the joint

is surface active phospholipids (SAPL).

Artificial joints do not enjoy the same excellent tribological performance of the

natural joint due to the replacement of at least one of the cartilage bearing surfaces


108

with a hard, metallic or ceramic surface. The lubrication of the replacement bearing

falls into the mixed regime at best and boundary lubrication becomes more crucial

in controlling wear and hence the long term performance of the artificial bearing.

Thankfully the lubricating ability of pathologic synovial fluid is not lost due to OA

and surface active phospholipids are available to potentially benefit the lubrication

of the total joint replacement.

Even though much research has focused on designing implants to encourage fluid

film lubrication, there is little doubt that the surfaces will make contact throughout

the walking cycle. It is at these times that boundary lubrication will occur and a

boundary lubricant will be necessary to facilitate this. Some groups have studied

compliant bearing surfaces in aid of elastohydrodynamic lubrication but still resort

to providing a surface that the boundary lubricant (SAPL) can adsorb to.

Chapter 5: Literature Review – Boundary Lubrication for Artificial Joints

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Chapter 5

Literature Review – Boundary

Lubrication for Artificial Joints

This chapter gives further consideration to boundary lubrication, boundary

lubricants and their relationships to surfaces like those in artificial joints. It will

discuss surface chemistry and tribochemistry with a focus on the role of

phospholipids for lubrication. The design of the chapter is to give an understanding

to the surface interaction of the lubricating fraction of synovial fluid.

Boundary lubrication is the antithesis of full-film lubrication in that it is the quality

of the substances comprising the sliding surfaces and the quality of the fluid used

as a lubricant which are the essential features; the shape of the surfaces and

viscosity of the fluid are unimportant. An example of the lack of correlation to

viscosity is the fact that a watery solution of oleic acid is a better lubricant for glass

sliding on glass than pure glycerine, though the latter is many times more viscous.

In this type of lubrication, the property of 'oiliness' is fundamental; however what is

most important is not the 'oiliness' of the lubricant itself but the property of oiliness

when applied to the sliding surface. Thus methylated spirit has no more suggestion

of oiliness than water when tested between the fingers, but for rubber it is a better

lubricant than water. This illustrates the important fact that in boundary lubrication

a lubricant has an affinity for the surface it lubricates so that when motion takes

place between two such lubricated surfaces it takes place between monomolecular

films of lubricant chemically adhered to the underlying surface. It is obvious that

monomolecular films which are bound to the sliding surfaces are less likely to

rupture under heavy loads than films of a lubricant which is inert towards the

substance of the surface, because the integrity of such a film depends only on the

intermolecular attraction in the fluid itself and the intermolecular attraction of a

fluid is obviously less than that of a solid. The molecules of a fluid which are

bound to the surface of a solid lose the physical properties of a liquid. In the case of

mineral oils, which have no chemical affinity for metals, the addition of small


110

quantities of fatty acids greatly enhances their lubricating properties; this is

explained by soaps being formed between the fatty acids and the metal with the

result that motion takes place between two layers of molecules all with their -

COOH groups attached to the metal surface and the fatty chain projecting like the

bristles of a brush (Charnley 1959).

Surface chemistry, boundary lubrication and tribochemistry are highly inter-related

and it is difficult to discuss any one without the others. Friction is the largest real

world example/use of surface chemistry. Boundary lubrication in artificial joints is

thought to be achieved by surface active lipids; lipids fall under the categories of

surfactants, colloids and monolayers which are themselves a subcategory of surface

chemistry.

Boundary lubrication by detailed definition is tribochemistry and tribochemistry is

the application of surface chemistry for tribological purposes. Boundary lubrication

may be the most complex of all the lubrication regimes as it involves these other

sciences that deal with the nanoscale interactions of surfaces and the lubricants,

with the purpose of determining the interactions that predominate and which forces

are at play. Boundary lubrication at this level may well be beyond the knowledge

of the engineering tribologist and maybe more fitting for a surface, tribo or even a

colloidal chemist. This chapter will cover the science but in consideration of the

engineer and his role to apply this science.

Considering that the mode of lubrication is most likely boundary in nature for

artificial joints and that an active lubricant of the joint has been identified, it is now

of utmost interest to investigate the interaction of this lubricant and the biomaterial

surfaces. As explained previously boundary lubrication is not about the bulk

properties of the lubricant but rather the ingredients of the lubricant and the

interaction of each constituent with the surfaces with which they come into contact.

In the previous chapters, lipids and, more specifically surface active phospholipids

(SAPL) have been identified as an active boundary lubricant in both the natural and


111

artificial joint; this chapter will discuss the interaction of SAPL and the bearing

surface.

5.1 Surface Chemistry

Surface chemistry can be broadly defined as the study of chemical reactions at

interfaces. It is the study of how certain substances interact with a surface. The

adhesion of gas or liquid molecules to the surface is known as adsorption. This can

be due to either chemisorption or by physisorption.

5.1.1 Surfaces and Surface Energy

Living material contains many boundaries. The boundaries are usually maintained

by membranes interfacing with each of the fluid compartments that they separate;

others are the natural interfaces that would exist between different phases even if

no membrane were to exist. Such phases include fat, aqueous fluids, various solids

and semi-solids, and the air or water of the external environment.

Each molecule at one of these interfaces possesses additional energy by virtue of its

location because it is surrounded by similar molecules on one side only. Thus, it

experiences an imbalance of intermolecular forces in contrast to the uniform field

of forces that would apply were it surrounded by a homogenous medium. For

liquids in air, this interfacial energy is manifest as surface tension, the property

that, for example, enables a steel needle to be ‘floated’ on still water or enables a

pond skater insect to ‘walk on water’. Although some surfaces may demonstrate

surface energy in more obvious ways than others, all surfaces possess energy, even

solids (Hills 1988).

Most substances can modify the surface energy of an interface to some degree but

some are much more effective than others and these are termed surfactants (surface

active agents). Surfactants tend to locate at air-liquid interfaces because this

reduces the surface energy, or boundary tension, of the interface (Adamson & Gast

1997). To be effective at an interface involving a solid, the surfactant needs to be


112

directly adsorbed (bound) to the solid surface. When surfactants are adsorbed to

solid surfaces they impart many highly desirable properties (Barnes & Gentle

2005) some of which have immediate physiological applications (Hills 1988).

Some of these attributes will be covered in greater detail later. When adsorbed to a

solid surface, surface-active agents completely change the nature of a surface, i.e.

hydrophilic surfaces will be rendered more hydrophobic.

5.1.2 Hydrophobic vs Hydrophilic

Since water is the predominant substance in all tissues and fluids in the body, the

affinities of various substances tend to be expressed relative to water. If they are

highly compatible with water they are termed hydrophilic from the Greek meaning

‘water loving’. When substances repel water, they are termed hydrophobic from the

Greek meaning ‘water hating’.

An important note is that the liquid can behave very differently when close to a

surface in comparison to the bulk and that the water or liquid structure near a single

surface is changed, often quite significantly, when another surface is near-by

(Benz, Chen et al. 2005).

Water comprises 50-80% of most living creatures. Hence, water is almost

invariably one of the phases present wherever interfaces occur in vivo and

consequently wherever surfactants are acting. The fact that water is incorporated

into a structure or that the material has an affinity for water is an important

indication that its surfaces are likely to be hydrophilic and will therefore tend to be

compatible with aqueous solutions or, if a solid, its surfaces should be readily

wetted by aqueous solutions. As a simple indication of compatibility, a droplet of

water will spontaneously spread over a very hydrophilic surface. By contrast, the

same droplet would not wet a hydrophobic surface but would bead up, as observed

when a raindrop falls on a cabbage leaf. In reality there is a spectrum of degrees of

wettability ranging from perfectly hydrophilic to very hydrophobic which can be

very conveniently quantified by this simple example as the contact angle (5.1.5.)


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imposed upon the droplet by the surface. Thus, the interfacial energy is very low

for compatible phases, but becomes higher as the surfaces become less compatible.

5.1.3 Surface Tension and its Measurement

The molecular forces which impart energy to an interface simply because it is an

interface have already been mentioned, along with an outline of the role of

surfactants in modifying the resultant interfacial energy. To quantify the effects of

surfactants, it is necessary to be able to measure the energy of an interface in the

absence of surfactant.

Definitions

The energy per unit area associated with an interface is usually denoted by E with

the two phases in contact denoted by suffixes for air or any gaseous phase (A),

liquid (L) or water or any aqueous phase (W), oil or lipid (0) and solid or

membrane (S).

Surface energy may be relatively easy to conceptualise with diagrams of molecular

forces but, in the real world, it is much easier to perceive surface tension as the

force retaining a pond skater insect on the surface of a pool of water. It has long

been recognised that surface tension (γ) is a manifestation of surface energy (E)

and can be equated under isothermal conditions (Adamson & Gast 1997). Both E

and γ have the same dimensions. E is usually expressed in erg cm-2

and γ in dyne

cm-1

which is actually the same because, by definition, 1 erg is the work needed to

move a force of 1 dyne by 1 cm (Barnes & Gentle 2005). Before any further

discussion of the methods of measuring surface tension, an explanation is

necessary of the relationship between the interfacial energies at points where three

phases meet.

5.1.4 The Young Equation

Many methods of measuring surface tension create a periphery at which the liquid

‘grips’ the solid. In cross section this is seen as the triple point where solid, liquid


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and air meet (Figure 5.1.) where θ is known as the contact angle, i.e. the angle

between solid:air and solid:liquid phases at that point. θ can have any value

between 0 and 180° depending on the nature of the phases (Phillips & Riddiford

1967). Resolving forces in the plane of the solid surface, which is not deformable,

there is a force of γSA pulling to the left. Pulling to the right is the solid:liquid

tension γSL plus the component of the liquid:air surface tension (γLA) resolved in

the plane in which the balancing forces have a net contribution of γLAcosθ. For

equilibrium, the forces pulling to the left will equal those pulling to the right when:

Equation 5.1. γSA = γSL + γLAcosθ

This is generally known as the Young equation and states that the competition

between the cohesive forces of a liquid to itself and the adhesive forces between the

liquid and solid surface result in a contact angle which, at equilibrium, is constant

and specific to the particular system (Gellman & Spencer 2005). The importance of

the Young equation is that it enables solid surface energies to be determined using

the contact angle technique (Israelachvili 1992; Shpenkov 1995; Adamson & Gast

1997; Barnes & Gentle 2005; Gellman & Spencer 2005; Stachowiak & Batchelor

2005).

Figure 5.1. The triple point in cross section. Depicting the balance of forces at

the edge of a droplet where the liquid, solid and air all meet to subtend a

contact angle (θ).


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5.1.5 The Contact Angle

Equation 5.1 can be rearranged to express the difference between the dry and the

wet surface tension of the solid (γSA - γSL) as γLAcosθ. Since γLA is the liquid-air

interface tension, i.e. the readily measured surface tension of the liquid, the term

γLAcosθ is easily determined if θ is known. The contact angle can be measured

directly via a goniometer; this enables (γSA - γSL) to be determined and, hence, the

energy difference (ESA - ESL). This difference is also known as the work of

adhesion (Adamson & Gast 1997; Barnes & Gentle 2005) since it represents the

work done in breaking an adhesive bond affected by the liquid. The difference is

also an important parameter for the following reason.

A solid surface which is incompatible with water is termed hydrophobic. Thus it

has a high interfacial energy when in contact with water (ESL) while it is

compatible with air, so that the interface now has a lower surface energy (ESA).

This means that the difference (ESA - ESL) decreases substantially as the surface

becomes more hydrophobic. If the liquid is water and its surface tension remains

constant, the Young equation predicts that cosθ will decrease and even go negative

if ESL>ESA. Since the angle increases as the cosine decreases, this explains the

larger contact angles observed on more hydrophobic surfaces. The contact angle is

a good measure of the everyday experience whereby water tends to ‘bead up’ on

waxed surfaces and, in the light of the Young equation, represents a good index of

surface hydrophobicity (Hills 1988).

5.1.6 Surfactants

The interfacial energy can be greatly modified by substances with amphipathic

properties. Molecules with combinations of moieties (ends) which have an affinity

for the phase in which they are dissolved and moieties which tend to be repelled by

the medium are termed amphipathic. Amphiphilic by definition is a molecule

having a polar, water-soluble group attached to a nonpolar, water-insoluble

hydrocarbon chain. These ‘ends’ are covalently bound to each other, one being

hydrophobic and the other hydrophilic. When located at an interface the molecule

will locate with its ‘ends’ orientated to minimise interfacial energy. Certain


116

chemical groups can be selected as likely for the moiety with an affinity for the

medium and another set for the “antipathic” moiety (Barnes & Gentle 2005). These

are bound by a strong covalent bond, i.e. it can only be broken by strong chemical

agents.

5.1.7 Electrical Charge

The hydrophilic moieties fall into four categories, with respect to electrical charge.

They may carry no net charge (nonionic), a negative charge (anionic) or a positive

charge (cationic). In the fourth case, the moieties carry both charges; the

phosphoric acid end of the phospholipid molecule can still ionise giving a negative

charge which is comparable in magnitude to the positive charge of the amine or

quaternary ammonium ion, to produce a charge dipole and a molecule classified as

a ‘zwitterion’. Zwitterionic is best explained by a zwitterion which is a dipolar ion

that is capable of carrying both a positive and negative charge simultaneously

(Barnes & Gentle 2005).

5.1.8 Adsorption

To change the surface tension of a solid the surfactant molecule attaches to the

surface by any of a variety of chemical and physical bonds known as adsorption.

Adsorption is a common process, especially the weak physical (Van der Waal’s)

type (physisorption). The much stronger type, chemical adsorption (alias

chemisorption), can be effected when one of the chemical groups (moieties) in the

molecule forms a reversible bond with the surface which is chemical in nature. The

widespread occurrence of adsorption is generally not obvious to an observer as like

tends to attract like; so, in the case of adsorption of the usual homopathic molecule,

it presents a surface not unlike the one it is covering. If, however, the molecule is

highly amphipathic, especially in its affinities for water, adsorption can be readily

recognised (Hills 1988).

The attachment of a surfactant molecule by electrostatic attraction between the

polar moiety and a fixed charge on the surface orientates the molecule with its non

polar group facing outward. This presents a new surface with a total change in

‘personality’ from the one covered. In the case of hydrophobic solids the


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hydrocarbon moieties will be attracted and adsorbed to the surface to leave the

polar ends outwards rendering the surface hydrophilic. Such agents are then acting

as wetting agents. On the other hand, hydrophilic surfaces will attract the polar

ends which then adsorb to the surface. This orientates the hydrocarbon end

outwards rendering the surface hydrophobic. Thus, droplets of water which would

have spread spontaneously on the hydrophilic surface now “bead up” to display a

contact angle which, as previously discussed, provides a convenient index of the

change in surface energy upon the surface.

Often adsorption of synthetic surfactants in vitro does not stop at the monolayer

state but proceeds to multilayers (Dowson, Priest et al. 1998; Barnes & Gentle

2005). When these layers are well defined and widely spaced, they can be effective

boundary lubricants. This process is known as lamellated solid lubrication

(Stachowiak & Batchelor 2005).

5.2 Tribochemistry

Tribochemistry is basically a sister science to both boundary lubrication and

surface chemistry. It takes the principles of surface chemistry and applies them to

the field of friction, lubrication and wear. Thus, in combining tribology and

chemistry, it is the area where these two sciences overlap that becomes

tribochemistry.

‘Tribochemistry generally refers to the chemistry that occurs between the lubricant

(and/or the environment) and the rubbing surfaces under boundary lubrication

conditions. This includes specific reactions that occur only under rubbing

conditions and reactions that would occur independently under the temperatures

and pressures in the contact. The reactions that take place only during rubbing

usually involve direct chemical interactions with the surface. The reactions that

would occur independently can be defined as contact chemistry (oxidation, thermal

degradation, catalysis, polymerisation). The two sets of reactions are intimately

intertwined and one affects the other.


118

There are two possible sources of tribochemistry: the mechanically induced

chemistry (fresh nascent surface, electron emission) and the thermally induced

chemistry at the asperity tips due to flash temperatures. Specific attribution of a

reaction to these two possible sources has not been delineated. Speculations abound

in the literature but experimental difficulties prevent a clear definition of this

important issue.

The definition of ‘‘tribochemistry’’ is not very precise, even though most

researchers declare that their motivation for studying tribochemistry is to

understand the boundary lubrication mechanism. Under the banner of

tribochemistry, researchers have studied the nature of ‘‘friction polymers’’, surface

oxidation reactions and environmental reactions with water.’(Hsu, Zhang et al.

2002)

Surface tribochemistry refers to the physical adsorption or chemisorption of the

boundary lubricant and its relationship to wear (Pawlak 2003). Much of this has

already been covered in the surface chemistry sections and further discussion will

follow in subsequent sections.

Tribochemistry is a new area of research. It is useful to the engineer considering

the finer details of boundary lubrication such as the mechanism of lubrication for

the synovial joint, in particular the artificial replacement.

5.3 Surfactants for Boundary Lubrication

Surfactants, both anionic and cationic, are frequently used in many aspects of

industry. Probably the largest source of surfactant use in industry is as detergents

(Shaw 1992; Barnes & Gentle 2005). Common soap is the anionic surfactant best

known as a detergent for washing ourselves and clothing. Soap is essentially the

sodium salt of the fatty acid, most commonly stearic (C18) but also palmitic (C16)

and some unsaturated fatty acids (Hills 1988). Unfortunately the detergency of the

salts of these fatty acids, which are derived from fat, suffers due to the insolubility

of their calcium salts. The great economic incentive to find acids whose calcium


119

salts were soluble created a surge in surfactant technology which led to the

development of synthetic surfactants, many of which were found to have other

highly desirable properties, creating an enormous industry which touches almost

every other industry.

Another large user of surfactants is the food industry which uses Lecithin

(phospholipids) in substances requiring a natural emulsifier, release agent and/or

lubricant. For example, lecithin is the emulsifier that keeps cocoa and cocoa butter

from separating in chocolate.

Although it was the need for good detergents and emulsifiers which prompted the

development and production of synthetic surfactants early in the last century, it was

soon found that these new products needed little modifying for applications in

other areas. These included lubrication, protection from wear, inhibition of

corrosion, water repellency, modification of permeability, defence against

biological invasion, release (anti-stick) action and viscosity modification (Larson &

Larson 1969; Biresaw 1989).

Several of these applications, especially lubrication, anti-wear and release are

beneficial within the biological system. Indeed, there is now considerable interest

in the roles of surfactant in biology.

5.3.1 Lubrication via Surfactants

Surfactants are used in industry under conditions where boundary lubrication is

required (Chung, Homolam et al. 1991; Pawlak 2003; Liang 2004). The primary

requirements for an effective boundary lubricant are the following:

(1) Strong binding to the surface as found with chemisorption.

(2) Adsorption in an adequate quantity to form a continuous monolayer.

(3) Strong cohesion of the adsorbed film to prevent penetration by asperities

on the counterface -a primary consideration in reducing wear (Briscoe,

1980- cited by (Hills 1988)).


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(4) Mechanisms should be provided for replenishing the monolayer or wear

and friction will increase with time.

Fatty acids have been used as lubricants in the form of soaps since ancient times.

Lead soap is used in gear oils (Munro 1964), the intermeshing of gears representing

a classical application of boundary lubrication in mechanical engineering. Fatty

acids are of interest as they represent the hydrocarbon moieties as found in

phospholipids (Figure 5.2.). Studies in vitro of their lubricating properties have

demonstrated that lubrication improves as chain length increases. The best fatty

acids for maintaining good lubrication were found to be palmitic (C16) and stearic

(C18) (Dowson, Priest et al. 1998; Barnes & Gentle 2005). Studies of fatty-acid

monolayers adsorbed to metal surfaces may seem far removed from any situation in

vivo, but they do provide information about packed hydrocarbon moieties which

constitute the exposed surface in many situations.

Having outlined the basic principles of boundary lubrication (see also 4.1.2), it is

now appropriate to discuss surfactants in vivo which have also displayed boundary

lubrication ex vivo.

5.3.2 Biological Surfactants

It is worthwhile briefly tracing through the history of how research in surface-

active agents and biology came to meet, prior to pursuing the current scientific

interest surrounding surfactants, especially phospholipids. Apart from free-fatty

acids and phospholipids acting as emulsifying agents at oil-water interfaces, the

major interest in surfactants in biology has centred around the lung and surface

activity is only mentioned in most physiological texts with respect to the lung.

A role for surface-active substances in the lung was derived largely by inference.

The earliest implication of surface activity in the lung can be traced to von

Neergaard (1929, cited by (Hills 1988)) who found that the pressure required to

inflate an excised lung with an aqueous fluid was about one-quarter to one-third of

the pressure required to achieve the same volume change using air. He compared

the lungs to soap bubbles, and interpreted his results as though the liquid used for


121

inflation had filled the bubbles, thus eliminating the air-liquid interface and the

associated collapsing pressure. Von Neergaard’s classical study was seldom

referenced for a number of years following its publication in 1929 and it was some

time before surface activity of the alveolar wall again attracted attention.

Pattle (Pattle 1950) had been interested in the control of foaming in the lungs

following chemical injury using certain agents categorised as ‘anti-foams’. Pattle

(Pattle 1955; 1956) found that these agents did not break the foam expressed from

rabbit lungs and was most impressed by the stability of this foam which persisted

for days. It was argued that this extreme stability was only possible if the surface

activity was “near zero”, since small bubbles with a normal surface tension shrink

rapidly. Pattle’s observations led him to propose the existence of a powerful

surfactant. This growing interest in the possible presence of a surfactant in the

lungs attracted the interest of (Clements 1957) and (Brown, Johnson et al. 1959)

who, using the standard ‘tools’ employed by surface chemists, decided to

investigate the surface-activity of lung extracts. They found that the surface tension

of water could be greatly reduced by lung secretions and washings, thereby

confirming the presence of a highly potent surfactant by standard physiochemical

methods. Following extraction of the surfactant from the lungs, (Pattle & Thomas

1961) and (Klaus, Clements et al. 1961) found it to be a lipoprotein rich in

phospholipid. Brown (Brown 1964) later determined the surface-active ingredient

to be dipalmitoyl lecithin, today more commonly termed dipalmitoyl

phosphatidylcholine (DPPC).

Following on from the detection of surfactant in the lungs the role of phospholipids

was studied for their role in other locations in the body. Hills dominated much of

the research in the 80s and 90s with other groups becoming involved over that

time. Surfactants were considered for their role ranging from the boundary

lubrication of the pleurae (Hills, Butler et al. 1982) to gaseous and solute exchange

in the intestinal membrane (DeSchryver-Kecskemeti, Eliakim et al. 1989). Apart

from the work done on surfactant in the lungs the remainder of the work in the

literature is dominated by the role that surfactant plays in the lubrication of surfaces

in the body (eg. (Butler, Lichtenberger et al. 1983; Hills 1984; Hills & Butler 1984;


122

Hills & Butler 1986; Hills & Cotton 1986; Hills 1989; Girod, Zahm et al. 1992;

Williams III, Powell et al. 1993; Bernhard, Postle et al. 1995; Higaki, Murakami et

al. 1998; Ethell, Hodgson et al. 1999; Chen & Hills 2000)).

5.3.3 Types of Lipids

In order to be an effective surfactant, a molecule needs a substantial hydrocarbon

moiety which is readily provided in vivo by fatty acid chains. These are found in

four basic forms of complex lipids: acyiglycerols, phosphoglycerides,

sphingolipids and the waxes (Tro 2003; Muller 2004). These differ in the backbone

structure to which the fatty acids are covalently bound. Neither the acyiglycerols

nor the waxes are amphipathic, leaving just two lipid families of high surface

activity: the sphingolipids containing sphingosine as their backbone and the

phosphoglycerides, loosely referred to as phospholipids or phosphatides (Figure

5.2.).


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Figure 5.2. General structure of phosphoglycerides, emphasizing their

amphipathic nature (Schwarz 1994). Various groups for X are given in Figure

5.3.

Phosphoglycerides

When one of the hydroxyl groups of glycerol is esterified by phosphoric acid,

phosphatidic acid is produced which provides the backbone for the

phosphoglycerides (PG). Two fatty-acid chains are normally attached to the

glycerol by esterifying the two remaining hydroxyl groups. One of the two

hydroxyl groups on the phosphatidic acid backbone can be replaced by

esterification of an alcohol (X-OH) to the phosphoric acid. X-OH can be any of six


124

or so alcohols: ethanolamine, choline (containing a quaternary ammonium ion),

inositol, serine, glycerol and diglycerol; see Figure 5.3.

Figure 5.3. Various polar head groups for the general phosphoglyceride

depicted in Figure 5.2. Source: (http://en.wikipedia.org/wiki/Membrane_lipids

2005)

Phosphatidylcholine

Phosphatidylcholines (PC) are the dominant species of PG in biology and is present

in most mammalian cell membranes. PCs are also the major constituents of


125

pulmonary surfactant, in particular DPPC (Brown 1964). PCs can either be

saturated or unsaturated. The term saturated and unsaturated phosphatidylcholine

refers to the presence or lack of a double bond in the fatty acid chains. When both

the fatty acid chains are saturated, it is called saturated phosphatidylcholine (SPC).

When one of both of the fatty acid chains are unsaturated, it is called unsaturated

phosphatidylcholine (USPC) (Chen, Hills et al. 2005). DPPC contains two

saturated fatty acid chains and is a SPC. USPCs are distinguished by a kink in at

least one of the fatty acid chains at the point of the additional bond (Figure 5.3.

Oleate). SPCs do not exhibit this kink and appear like Figure 5.2.

The highly surface-active surfactant dipalmitoylphosphatidylcholine (DPPC) found

in synovial fluid contains a highly positively charged quaternary ammonium (QA)

ion at its terminal group that is ideal for binding these small molecules to the

negatively charged surfaces.

Much research has been aimed at determining the types of lipids present in the

human body and more recently in particular the types of lipids present in the

synovial joint (Prete, Gurakar-Osborne et al. 1995; Ballantine & Stachowiak 2002).

Rabinowiz et al were the first to report on the lipid profiles of the tissues of the

knee joint. However they were not able to completely identify all lipid types or

their subgroups (Rabinowitz, Gregg et al. 1979). Similarly Sarma et al identified

some classes of lipids present in articular cartilage but not all (Sarma, Powell et al.

2001).

The term SAPL is used loosely. Although the title suggests surface active

phospholipids, its actual components are phosphatidylcholines which are two

subcategories below phospholipids; see Figure 5.3. It is suggested that SAPL be

retitled with SAPC (surface active phosphatidyl choline) for a more accurate

representation. However, SAPL will be used throughout this thesis even though it

refers to a group of PCs that make up part of phospholipids. SAPL is made up of a

number of PCs and it is has been assumed that DPPC is the dominant component as

it is in the lungs (Brown 1964). The actual detail of all the components of SAPL is

largely unknown.


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5.3.4 Phospholipid Analysis

Very little phospholipid occurs as individual molecules in solution because their

solubility is so low. They are more likely to form micelles, vesicles, liposomes,

adsorbed layers, lamellar bodies or tubular myelin (Hills 1988). Phospholipid is a

major component of most biological membranes. Various phospholipids can form

associations with numerous substances including protein, bile salts and

polysaccharide, all of which can change the quantity determined by assay

depending upon the ability of the method used to break the chemical or physical

associations and to extract the phospholipid from the membranous material present.

The quantification (certainly estimations) of phospholipid can be achieved through

several methods, two of which are viz solvent extraction and chromatographic

separation of phospholipids. High performance liquid chromatography (HPLC) has

been found to be effective for the identification of lipids (Chen, Hills et al. 2005).

5.3.5 Adsorption in Biology

In the section on adsorption (5.1.8.) there seemed little doubt that adsorption could

occur very readily, at least in industrial situations. Adsorption is a very common

process and there is also substantial evidence for its occurrence at interfaces in the

body. Most surfaces are negatively charged, be they metal or a mucosal surface

with carboxyl or sulphonyl groups incorporated into its structure (Dorinson &

Ludema 1985; Hills 1988). There is a vast range of cationic surfactants which are

effectively adsorbed to negatively charged surfaces (Sharma; Adamson & Gast

1997; Barnes & Gentle 2005) and many of these possess the highly positively

charged quaternary ammonium ion which is very common in the form of the

choline group.

Surfactant monolayers adsorbed to solids can be encouraged to increase the

tightness of packing following the addition of cations. The interspersion of these

positive ions between the negative phosphate ions at the distal end of the polar

moieties would have the effect of pulling those groups together, Figure 5.4., which


127

imparts greater cohesion - a highly desirable feature for effective boundary

lubrication (Hills 1988). This role of cations (Shah & Schulman 1965; Watkins

1968) was demonstrated at the liquid-air interface by the reduction in the surface

area per molecule at the same pressure. Later the same forces have been used to

explain the packing of monolayers adsorbed to solids (Hills 1984; 1984; Hills &

Butler 1984).

Figure 5.4. A molecular model for the adsorption of phospholipid zwitterions

to a negatively charged surface in which cations in the plane of the phosphate

ions pull those ions together, thus enhancing close packing of both polar and

non polar moieties and imparting coherency. (Hills 1988)

One of the desirable properties imparted by adsorption of surfactants in industry,

which also plays a large role in biology, is lubrication.

5.3.6 Biological Surfactants and Lubrication

There are many pairs of surfaces in the body which need to move either by sliding

over each other or by separating to allow air, fluid or water to pass between them.

This movement needs to be achieved with minimal friction and wear and, when

appropriate, be facilitated by good lubrication. Hence, it is very interesting to find

many of the same surface-active phospholipids in many organs and in the fluids

adjacent to surfaces which, if they were to stick or rub, could severely compromise


128

physiological function (Rapport, Lim et al. 1975; Hills 1984; Hills & Butler 1985;

Hills & Butler 1986; Hills & Cotton 1986; Hills 1988). This opens up an interesting

new field for surfactant whose molecules are very similar to many of their synthetic

counterparts already used as lubricants and release agents with great success in

industry (Dorinson & Ludema 1985).

Of particular interest is the reduction of friction and wear in the synovial joint

where wear is known to have serious implications to the longevity of both the

natural and artificial joint (3.5 & 3.6.1.).

5.4 Boundary Lubrication via SAPL

Having outlined the theoretical aspects of surfactant adsorption to membrane

surfaces, it is now appropriate to consider the highly desirable properties which an

adsorbed layer might impart.

The theory of how phospholipids can facilitate sliding basically follows that of

boundary lubrication (a phenomenon experienced after touching a wet bar of soap

and squeezing the water from between ones fingers: the slipperiness remains).The

surface active phospholipids offer much potential for providing boundary

lubrication in vivo for several reasons:

(1) SAPLs are found in vivo adjacent to the moving surfaces of the body in

forms in which they are available in a surface-active form (5.3.6.) and they

have also been shown to display multilayer adsorption to biological

surfaces (Ueda, Kawamura et al. 1985; Hills 1990; Hills 1990; 1990).

(2) Most SAPLS possess polar moieties which readily bind to the negative

sites on most biological surfaces (especially mucosal and epithelial

surfaces) and artificial surfaces to affect strong adsorption (5.3.5.).

Cations interspersed in the plane of the phosphate ions will neutralize

these ions, effectively rendering the phospholipids cationic with

characteristically strong adsorption (Figure 5.4.).


129

(3) The fatty acids in the hydrophobic moieties are mostly of ideal chain

length for lubrication, namely C16 and C18 (5.3.1.).

(4) When adsorbed these long hydrocarbon chains are orientated and packed

in much the same way as free fatty acids (5.3.1.) and the lubrication is as

good, but the monolayer is more tightly bound and, therefore, more

durable.

(5) Durability is improved by the insolubility of these layers (Hills 1988).

(6) Phospholipids contain a phosphate group at the middle of the molecule

which is ionized at physiological pH for most locations. These ions

provide an ideal point for pulling neighbouring molecules together if small

cations are placed between them, thus imparting strong cohesion (Figure

5.4) in addition to adhesion (Hills & Butler 1984).

Experimental evidence is also in strong support of phospholipids being able to

lubricate in vivo by Hills and others (Moro-oka, Miura et al. 2000). When tested

using a simple apparatus to measure the effectiveness of surfactant, the reductions

in the coefficient of friction for a glass-on-glass system were DPPC (70%),

dipalmitoyl phosphatidylethanolamine (72%) and sphingomyelin (70%) according

to Hills et al (Hills, Butler et al. 1982). The coefficient of kinetic friction for DPPC

was found to be 0.02 under dry conditions, representing a 99% reduction in friction

(Hills & Butler 1986). Similar values were achieved using DPPC at 37°C in the

method of (Radin & Paul 1971) in which lubrication under high stress (up to 13

kg/cm2 compared with a typical loading in the human knee joint of 3 kg/ cm

2) was

tested.

Surface-active phospholipid (SAPL) has been found to act as an effective boundary

lubricant in the lungs (pleural surfaces) (Hills, Butler et al. 1982), pericardium

(Hills & Butler 1986), gastrointestinal tract (Hills 1996), and tendons (Uchiyama,

Amadio et al. 1997).

Morphological studies have provided visible evidence of oligolamellar

phospholipid at the articular cartilage surface (Hills 1989; Hills 1990; Guerra,

Frizziero et al. 1996; Hills 2000) the alveolar surface (Ueda, Kawamura et al. 1985)


130

and the mesothelial surface of the visceral pleura (Ueda, Kawamura et al. 1986).

These lamellar structures bear a striking similarity to the structure of graphite and

MoS2, recognised ‘solid’ lubricants used widely as boundary lubricants in industry

(Larson & Larson 1969). Hills suggested that this layer upon layer of SAPL may be

protecting the underlying surface by acting as sacrificial layers (Hills 1989)

Many studies by Hills and others (eg. (Little, Freeman et al. 1969; Gavrjushenko

1993; Higaki, Murakami et al. 1997; Hills & Thomas 1998; Hills 2000; 2002; Hills

& Jay 2002; Hills & Crawford 2003; Ozturk, Stoffel et al. 2004)) has led to the

identification of SAPL as a remarkable load-bearing lubricant in the normal joint

i.e. a vital active ingredient in the lubrication of joints. SAPL is also a very

efficient release (anti-stick) agent, which, as a thin lining, enables the articular joint

surfaces to violate the first principle of lubrication engineering by allowing

surfaces of the same material to slide over each other without binding.

Of particular interest to the lubrication of artificial joints was a study by Purbach et

al who were the first to report on the presence of SAPL on artificial joints

(Purbach, Hills et al. 2002). They rinsed the bearing surface of a number of

removed total hip replacement prostheses obtained at revision. Analysis of these

rinsings showed that sufficient SAPL was present to form oligolamellar layers on

the bearing surfaces. Purbach et al. suggested that, if indeed formed, this layered

structure of phospholipid would act similar to a lamellated-solid lubricant,

protecting the surface from wear and ensuring low coefficients of friction.

The body of studies exploring the lubricating potential of surface-active

phospholipids is steadily increasing, continually adding support to the theory that

surface-active phospholipids may be providing boundary lubrication in vivo.

5.4.1 SAPL and Wear in artificial joints

SAPL lubrication has attracted much attention from the groups studying wear in

prosthetic joints (Ahlroos 2001; Bell, Tipper et al. 2001; Calonius 2002). All

groups have shown remarkably low wear rates of UHMWPE when DPPC was used


131

as a lubricant. Bell et al showed that at higher DPPC concentrations (5% w/v) the

wear was reduced by some 25-50 times as compared to the control bovine serum

lubricant and by at least threefold at relatively low concentrations (0.05% w/v).

Ahlroos reported that in several tests using DPPC as a lubricant, the lubricant

completely prevented polyethylene transfer, practically no wear debris was

generated and that the surfaces looked unchanged under microscopy.

Even Hills proved the anti-wear efficacy of SAPL by subjecting it to a traditional

engineering wear test called a standard four-ball test, a test normally reserved for

qualifying extreme pressure (EP) lubricants. Despite using speeds and loads that

were "extreme" by engineering criteria, i.e., several orders of magnitude in excess

of physiological logical loadings, the indices of wear (mean scar diameters) were

comparable to those of the best industrial lubricants. Hills concluded with ‘This

lubricant imparts not only phenomenal anti-wear properties, but also the

remarkable reduction in friction reported previously’(Hills 1995).

5.5 Summary

Surface and tribo chemistry are necessary to understand the boundary lubrication

that is sure to occur in the synovial joint. Joint surfactant, or surface active

phospholipids, has been implicated as the indigenous boundary lubricant for the

body. It is speculated that SAPL will function effectively in the artificial bearing.

However the constitution of SAPL is still largely unknown.

Chapter 6: Scientific Paper I

133

Chapter 6

Scientific Paper I - The Role of SAPL as a

Boundary Lubricant in Prosthetic Joints

Lorne R. Gale, BEng(Hons), Rebecca Coller, BEng(Hons), Doug J. Hargreaves,

DPhil, Brian A. Hillsa, DPhil, D.Sc., Sc.D and Ross W. Crawford, DPhil, MBBS.

School of Mechanical, Manufacturing and Medical Engineering, Queensland

University of Technology, Brisbane, Australia and the aMater Medical Research

Institute, South Brisbane, Australia

Published in: Tribology International, (2007). 40(4): p. 601-606.

Authors Contributions:

Lorne R Gale: All experimental work, data analysis and manuscript composition.

Rebecca Coller: Advisory role (ex-student)

Brian A Hills: Guidance and assistance with contact angle measurements and

adsorption tests. Supervisory role.

Doug J Hargreaves & Ross W Crawford: Supervisory role

Corresponding author:

Lorne R Gale

School of Mechanical, Manufacturing and Medical Engineering,

Queensland University of Technology,

2 George St,

Brisbane, Australia

Tel.: +617 3864 2423

Fax: +617 3864 1469

Email: [email protected]

Keywords: Boundary lubrication; SAPL; DPPC; Prosthetic joint; Synovial joint;

Biotribology

Chapter 6: Scientific Paper I

134

halla

This article is not available here. Please consult the hardcopy thesis available from QUT Library

Chapter 7: Scientific Paper II

141

Chapter 7

Scientific Paper II – Boundary lubrication

of Pyrolytic Carbon with Surface Active

Phospholipids: Tribological Assessment

for Artificial Joints

Lorne R. Gale1, Brian A. Hills

2, Doug Hargreaves

1, Ross Crawford

1,

Jerry Klawitter3

1Medical Engineering, Queensland University of Technology, Brisbane, Australia

2Mater Medical Research Institute, Brisbane, Australia

3Ascension Orthopedics, Austin, Texas USA

Revised and resubmitted: Acta Orthopaedica (2007)


Lorne R Gale: All experimental work, data analysis and manuscript composition.

Brian A Hills: Guidance and assistance with adsorption tests. Supervisory role.

Doug J Hargreaves & Ross W Crawford: Supervisory role.

Jerry Klawitter: Provided PyC specimens


Lorne R Gale

Medical Engineering,


2 George St,

Brisbane, Australia

Tel.: +617 3864 2423

Fax: +617 3864 1469


Keywords: Boundary lubrication; SAPL; DPPC; Prosthetic joint; PyC; Pyrolytic

Carbon; Biotribology

Chapter 7: Scientific Paper II

142

halla


Chapter 8: Scientific Paper III

149

Chapter 8

Scientific Paper III – Boundary

lubrication of joints: Characterisation of

Surface-Active Phospholipids found on

retrieved implants

Lorne R. Galea, BEng(Hons), Yi Chen

a, DPhil, Brian A. Hills

b, DPhil, D.Sc., Sc.D

and Ross W. Crawforda,c

, DPhil, MBBS.

aSchool of Mechanical, Manufacturing and Medical Engineering, Queensland

University of Technology, Brisbane, Australia

bMater Medical Research Institute, South Brisbane, Australia

cThe Prince Charles Hospital, Rode Rd, Chermside, Australia

Published in: Acta Orthopaedica, (2007). 78(3): p. 309-314.


Lorne R Gale: Experimental work, data analysis and manuscript composition.

Yi Chen: HPLC analysis

Brian A Hills: Guidance and assistance with surface rinsings. Supervisory role.

Ross W Crawford: Supervisory role


Lorne R Gale



2 George St,

Brisbane, Australia

Tel.: +617 3864 2423

Fax: +617 3864 1469


Keywords: Boundary lubrication; SAPL; DPPC; Prosthetic joint; Biotribology;

PC; USPC; SPC; phosphatidylcholine

Chapter 8: Scientific Paper III

150

halla


Chapter 9: Scientific Paper IV

157

Chapter 9

Scientific Paper IV - Tribological Testing

of Saturated and Unsaturated Surface

Active Phospholipids: Implications for

artificial joints

Lorne R. Galea, BEng(Hons), Yi Chen

a, DPhil, Prasad Gudimetla

a, DPhil, Doug

Hargreavesa, DPhil and Ross W. Crawford

a,b, DPhil, MBBS.

aSchool of Engineering Systems, Queensland University of Technology, Brisbane.

bThe Prince Charles Hospital, Rode Rd, Chermside, Australia

Submitted to: Proceedings of the Institution of Mechanical Engineers: Part H;

Journal of Engineering in Medicine


Lorne R Gale: Experimental work, data analysis and manuscript composition.

Prasad Gudimetla: Supervisory role and manuscript composition

Yi Chen: Chemistry role, mixed solutions.

Doug Hargreaves & Ross W Crawford: Supervisory role


Lorne R Gale



2 George St,

Brisbane, Australia

Tel.: +617 3864 2423

Fax: +617 3864 1469


Keywords: Boundary lubrication; SAPL; DPPC; Prosthetic joint; Biotribology;

PC; USPC; SPC; phosphatidylcholine

Chapter 9: Scientific Paper IV

158

halla


Chapter 10: General Discussion

165

Chapter 10

General Discussion

The work presented for examination in this thesis started with a pilot study

(Chapter 6) to investigate the tribological interactions of Pyrolytic carbon, a novel

load-bearing biomaterial, and SAPL the implicated indigenous boundary lubricant

by performing adsorption tests, contact angle measurements and tribo tests.

Common prosthetic materials, stainless steel and UHMWPE were also included for

part of the testing. It was found that a synthetic SAPL in the form of DPPC

promoted much surface activity in all materials and dramatically reduced the

friction between each tribo pair when tested under boundary lubrication conditions.

The prerequisite for boundary lubrication is that the surfactant be strongly adsorbed

to the surface, and ideally, this adsorbed lining be highly cohesive such that an

asperity from the counterface is less likely to penetrate the lubricating lining. The

results from the contact angle measurements indicated high surface activity

bestowed by the application of SAPL to the PyC surfaces. The PyC surface was

transformed from a hydrophobic surface (large contact angle) to a hydrophilic

surface (zero contact angle). In fact, the PyC surface became spontaneously

wettable indicating that DPPC was acting as an excellent wetting agent and that a

DPPC coating/film was obviously present. This adsorbed coating would be of

limited benefit as a boundary lubricant unless it was shown to be tenaciously

adsorbed. The results obtained from the adsorption tests indicated that DPPC is

indeed strongly adsorbed to the PyC surface. More than 80% of the originally

applied DPPC remained after 18 hrs of vigorous shaking in a saline bath meaning

that DPPC is strongly retained by the PyC surface. From a surface chemistry

standpoint these tests intimate that DPPC was attaching strongly to the PyC surface

and providing high surface activity, what remained to be seen for the purpose of

this surfactant being an effective boundary lubricant when in the presence of PyC

was whether this coating/film could in fact reduce the friction between the PyC

surface and another.


166

Pyrolytic carbon has been used successfully for prostheses in the heart and in hand

surgery and is known to be long lasting/wear resistant material in these

applications. It also has potential as a novel load-bearing surface for prosthetic

hips and knees, especially if it can be demonstrated to produce minimal wear under

load. One way to achieve this is to effect excellent boundary lubrication which has

become the accepted mode of lubrication in the artificial joint. Effective boundary

lubrication reduces friction and, hence, abrasive wear. In addition, SAPL, as an

excellent release agent when adsorbed to a surface, will inhibit adhesive wear.

The later stage to the first study (Chapter 6) began by tribo testing the

UHMWPE/SS tribo-couple. The tribo tests were performed at two temperatures,

body temperature and room temperature, to determine if temperature had an effect

upon the frictional performance of the tribo-couple when lubricated with DPPC and

saline and when in a non-lubricated state using physiological saline only. The

results did not show a marked difference in frictional force between the two

conditions and it was deemed that for the purpose of the tribo testing, the data

collected was relevant to the physiological state even though the tests were

conducted at a temperature lower than the body’s. The remainder of the tribo tests

were all performed at room temperature for ease of experimentation.

The pin-on-flat tribometer chosen for the tribo tests was suited for measurements

within the boundary lubrication regime, that is, relatively high loads and slow

speeds. Testing of the SS/PE tribo-couple with DPPC validated the results obtained

in a previous study (Coller, Hargreaves et al. 2004) whereby the friction was

reduced by more than 50% when lubricated with DPPC and saline as compared to a

non-lubricated (physiological saline) state. This alone was a remarkable result

supporting the role of SAPL reducing the friction between a prosthetic material

couple. More outstanding was the results obtained from the tribometer for the

UHMWPE/PyC combination. The friction between the tribo-pair was reduced by

more than 75% with DPPC as the lubricant as compared to the control lubricant

saline.


167

The excellent results obtained from the tribo tests in the first study (Chapter 6)

provided sound evidence that DPPC was certainly aiding the lubrication of the

tribo-couples in what can only be described as boundary lubrication conditions. At

this early stage of the thesis DPPC was assumed to differ little from the native

SAPL whereby DPPC was considered to be the dominant portion of SAPL as it is

in the lung. In addition Purbach et al has identified the presence of SAPL on

retrieved hip prostheses (Purbach, Hills et al. 2002). Therefore if a SAPL

equivalent can act as an effective boundary lubricant in vitro with prosthetic

bearing materials there is little reason to think that the same would not occur in

vivo. The pilot study for Pyrolytic carbon returned encouraging results and it was

suggested that further testing be done to assess the suitability of PyC as a candidate

material for load bearing prosthetic joints.

The second study (Chapter 7) was a follow on study which investigated the

tribological interactions of various forms of PyC (coupled with PyC and

UHMWPE) and SAPL by performing adsorption and tribo tests. The various forms

were largely denoted by their surface roughness. The results from the adsorption

tests showed similar results to the previous study, that is, PyC showed an affinity

for DPPC, however in contrast to previous results the smoothest PyC surface

showed less retention than the similar surface in the previous study. Although the

surface roughness was the same in both cases (0.03µm) the specimens were quite

different, the original was a circular disc whereas the specimen in this study was an

actual half crescent shape ‘leaflet’ prosthetic heart valve. The difference in results

may be explained by two reasons; 1) the PyC heart prosthesis was physically much

smaller than the original circular disc and therefore the tenacity tests became more

difficult to perform and 2) the number of tests was greatly reduced in the 2nd

study

from n=18 to n=4 hence reducing the accuracy of the results. The greater retention

by the rougher surfaces may also be explained by the larger surface area available

for the molecules to attach to as opposed to the lipids layering upon each other and

being more likely to detach from one another as on a smoother surface.

The results from the tribo tests showed an excellent tribological performance for all

cases where UHMWPE slid against PyC under the boundary lubricating influence


168

of DPPC. The trend in the results indicated that the smoother the PyC surface the

greater the friction reduction achieved by the lubricant. This follows for two

reasons; 1) in engineering generally smoother, harder surfaces are intrinsically

lower friction couples; and, 2) smoother surfaces have less surface area for the

lipids to attach to, therefore encouraging multiple layers which is conducive to

better lubrication (lamellated solid lubrication). Some results from the tribo tests

were inconclusive. In regards to all cases where PyC rubbed against PyC, SAPL

had little to no effect in reducing the friction between the tribo-pairs. This is best

explained in lubrication engineering by analysing the surface roughness of the

specimens and considering the hardness of the material as PyC is a hard material.

In all instances where PyC was coupled with PyC at least one of the surfaces were

relatively rough and hence only the highest asperities make contact under load.

Since little or no deformation can occur due to the high hardness the lubricant can

only protect the small areas of contact which are naturally under higher load. This

demands more than the lubricant can provide. More than likely, the lubricant, in

this case the surface active lipids, are quickly rubbed off from the peaks and

deposited into the valleys where they are of no effect and wear between the

contacting asperities will be likely to occur.

These overall results from the PyC studies indicate that regardless of the tenacity of

the lubricant (DPPC) to the surface which in most cases is quite high and shows

high surface activity, it is the smoothest PyC surfaces that show the greatest

reduction in friction. Although the additional manufacturing process of polishing

PyC is labour intensive and hence expensive, it is strongly suggested that as a

candidate material for future prosthetic joints that polishing be done so that

indigenous SAPL can ideally reduce friction and wear the greatest amount in a PyC

bearing.

Pyrolytic carbon has received large merit as a biomaterial in the body for many

years where it has been used primarily for heart valves. Wear resistance of the

pyrolytic carbon is excellent. The strength, stability and durability of Pyrolytic

carbon are responsible for the extension of mechanical valve lifetimes from less

than 20 years to more than the recipient’s expected lifetime (More, Haubold et al.


169

2000). This property alone makes PyC attractive for use in the body where wear is

known to be an issue. It is interesting to note that some PyC heart valves have

PyC/PyC hinge joints that allow the valve leaflets to open and close about 40

million times a year and have shown very little wear after 10 – 20 years of service.

Contact pressures at the PyC/PyC hinge joint are high due to the “water hammer”

effect at valve closure. Other studies by Ascension Orthopedics (unpublished) have

performed wear tests with PyC and noted remarkable anti-wear properties, superior

to other common prosthetic materials, even when bovine serum was used as the

lubricant. The tribological performance of PyC is excellent and its mechanical

properties are within acceptable ranges suitable for a load bearing joint making

PyC a highly recommended candidate material for future hip, knee and shoulder

prostheses.

It is worthwhile at this point to discuss a possible explanation of the lubricating

mechanism of SAPL and artificial surfaces. Firstly, there is an interesting

difference between what was found with PyC, SS and UHWMPE and how it

differs from traditional studies of adsorbed surfactants. Normally, surface chemists

select the polar 'head' of a surfactant molecule or chemically modify the surface

itself to obtain binding by adsorption. This orientates the non-polar group

outwards such that the surface is typically transformed from hydrophilic to

hydrophobic (Figure 5.4.). However, in the case of these artificial materials we are

finding the exact reverse. We start with a hydrophobic surface and then render it

very hydrophilic/wettable. This implies that the SAPL molecules are attaching

themselves to the surface by means of their hydrophobic/hydrocarbon moieties,

thus orientating the polar ends outwards to provide a highly wettable surface.

Surprisingly, this bonding is quite tenacious. This would also explain subsequent

blood protein adsorption that occurs in PyC heart valves in vivo according to the

literature. Regardless of how these lipids attach themselves to the artificial surface,

it is undeniable that they reduce friction extremely well. A lubrication model that

may explain this behaviour has been developed by considering the work done by

two groups in the literature (Davis, Lee et al. 1979; Benz, Chen et al. 2005). Since

SAPL renders the artificial surface spontaneously wettable there is considerable

attraction for water (the major constituent of synovial fluid) to be present at the


170

surface. Basically these groups show that water in confined spaces takes on

properties markedly different to that of the bulk and may act as a repulsive

lubricant; that is, water and the presence of surface active molecules keep the two

surfaces apart by a repulsive force. This suggests that SAPL may work in

conjunction with water to lubricate the bearing surfaces of artificial joints.

The third paper presented in this thesis (Chapter 8) was the first study to date that

has completely characterised the constituents of the SAPL adsorbed to the surface

of load-bearing artificial joints. These retrieval studies were also the first to identify

the presence of SAPL on the surface of knee implants. Previously SAPL had only

been shown on the surface of retrieved hip implants (Purbach, Hills et al. 2002) so

this finding adds further support to the role of SAPL as a boundary lubricant in vivo

for artificial joints. The results from the HPLC analysis of the adsorbed SAPL

identified eight different species of phosphatidylcholines with the majority being

made up by four of the PCs. Basically 90% of SAPL was equally made up of three

unsaturated PCs (USPC) and the remaining 10% was DPPC a saturated PC (SPC).

This finding closely matches the profile that was detected on other biological

surfaces outside of the lung including articular cartilage (Chen & Hills 2004) and

reinforces the fact that all non-lung locations are dominated by USPC. This is an

interesting finding as all previous studies for friction and wear have used DPPC

which was thought to be the dominant species within SAPL given that that was the

case in the lung. The reason for the difference in SAPL profiles between lung and

non-lung tissues has been proposed to be due to differences in the ability of

saturated and unsaturated PCs to reduce surface tension (Bernhard, Postle et al.

2001). Furthermore, DPPC has a gel-liquid crystal transition temperature of 41.5°C

which makes it effectively a rigid molecule at body temperature and thus better

able to reduce surface tension. However, unsaturated PCs have phase transition

temperatures far below body temperature, which enables them to adsorb more

easily.

This third study (Chapter 8) also showed that SAPL, in particular the specific PCs

mentioned above, were detected on all prosthetic surfaces analysed. That is the

same profile that was noted on the various materials of CoCr, Ti, SS and


171

UHMWPE. The materials were divided into two groups for analysis: metallic and

polymeric. The statistical analysis did not show a significant difference between the

two groups indicating that the profile of SAPL was the same for both types of

materials. This interesting finding must be considered under the context of the

study which was to identify the profile of the constituents (their relative

concentrations) rather than the amounts of SAPL present. It is known that SAPL

has an affinity for particular surfaces (as shown by the PyC surface) and therefore

this finding does not mean that SAPL attaches equally to all prosthetic materials

but that a similar profile of SAPL is present on all surfaces. SAPL may well prefer

a metallic surface as could be expected but only a study on the amounts of SAPL

present on the respective surfaces would reveal that. It is difficult to analyse the

amounts of SAPL present on a prosthetic surface given the large range of prosthetic

types and sizes and make a meaningful comparison.

There has been a need for a lubricant suitable for the laboratory testing of

prostheses and their materials for quite some time. As stated by a prominent group

that studies the wear of prosthetic joints “Unfortunately, wear studies are hampered

by the lack of a reliable, stable lubricant that accurately replicates joint fluid.”

(Ahlroos & Saikko 1997). Often the results obtained from in vitro tests do not

match the results obtained in clinical studies for prosthetic joints. One major factor

identified in the literature that may play a role in the disparaging results is the

lubricant used for the tribo tests. Several lubricants are used but none that mimic

the lubricating portion of synovial fluid. It is agreed that in vitro testing should be

performed with a lubricant as close as possible to what the body provides and given

the impracticality of using synovial fluid an equivalent pseudo-synovial fluid (PSF)

is required. The literature and these studies give strong support for SAPL being the

lubricating factor in the joint. The data obtained in this study emphasizes that

POPC, SLPC, PLPC and DPPC are the major constituents of the SAPLs adsorbed

to joint surfaces and not just DPPC as previously assumed. It is clear that a

combination rather than a single SAPL constitutes the boundary lubricant of

diarthrodial joints. Thus, in formulating a lubricant whose composition closely

resembles the proportion of unsaturated and saturated PCs found in the joint, a

suitable ‘artificial joint fluid’ was tendered for future friction and wear studies.


172

Cost and availability of large quantities of the individual PC species for wear

studies should not pose a problem as they are readily available for harvesting from

various sources such as egg yolk, bananas and their peels. This PSF may have

implications beyond the laboratory in providing a joint supplement similar to HA

viscosupplementation but for total joint replacement patients and even possibly be

useful in the development of pharmaceutical products for OA sufferers. In addition

a suitable PSF may reduce the variability in results noted between in vivo and in

vitro studies.

HA injections (viscosupplementation) have been shown to have some positive

effects even though HA is no longer considered to be the lubricant in the joint. This

causes one to wonder if HA affects more than the viscosity in the joint and the

literature seems to agree. HA may be acting as a carrier for the lubricant or in

synergy with SAPL. The same has been suggested for Lubricin and hence both

should be considered in the development of a PSF that may have implications

towards a pharmaceutical product.

Previous work (Chen, Hills et al. 2005) seemed to suggest that USPC species may

lubricate better than SPC species. DPPC is a saturated PC that has been shown to

reduce friction between two artificial surfaces quite remarkably and the suggestion

that a combination of USPCs and DPPC (the true SAPL profile) may reduce the

friction further was of keen interest. The fourth study (Chapter 9) in this thesis

investigated this suggestion and unfortunately did not find the same results as

previously reported. The PSF did not lubricate as well as DPPC by itself when used

as lubricants for a UHMWPE/SS tribo-pair. DPPCs tribological performance was

superior and reduced friction by more than 50% over the control lubricant whereas

the PSF reduced friction by up to 40% over the control. This may be explained by

the packing order of the USPC species versus the SPC species when adsorbed to

the surface. USPC only differ in structure by an extra bond in the fatty acid chains

which causes the fatty acid chain to kink part way along its length. This causes the

USPC molecules to pack less densely when compared to the straight chains of the

SPC species which can pack tighter and provide a more cohesive surface layer and,


173

hence, a better boundary against friction. Regardless, the PSF still lubricated well

and can still be regarded as an active boundary lubricant for the joint.

An additional study (unpublished) in this thesis, a first of its kind, verified the

action of SAPL on a prosthesis directly by measuring the friction of an explanted

ball from an artificial hip. Specimens were taken directly from the operating room

and tested on a tribometer to determine the frictional performance of the surface

adsorbed substances. The metallic balls were slid against a stainless steel surface

and showed that the friction was 50% less prior to cleaning the prosthetic surface

with a strong organic solvent. This is the same result that the first study showed

when UHMWPE was slid against SS when lubricated with DPPC. This finding is

excellent confirmation of the role of SAPL in the boundary lubrication of artificial

joints.

10.1 Conclusions

It is still largely unknown how and with what the human joint is lubricated. Surface

Active Phospholipid (SAPL) has been implicated as the boundary lubricant in the

human synovial joint, where such conditions exist that boundary lubrication is

crucial to the integrity of the natural bearing. More so, a previous study has shown

the presence of SAPL on retrieved hip implants suggesting that SAPL may play an

integral role in the boundary lubrication of the artificial joint.

This thesis has verified the action of a synthetic SAPL (DPPC) on common

prosthetic materials in vitro. SAPL does effectively lubricate prosthetic materials in

vitro under boundary lubrication conditions.

In addition, the action of SAPL with a novel load-bearing biomaterial, Pyrolytic

carbon, under boundary lubricated conditions returned an excellent tribological

performance. The interaction between SAPL and PyC is very favourable

suggesting that PyC receive further consideration for future prosthetic designs.


174

This thesis contained a study which was the first to identify the presence of SAPL

on retrieved knee implants and the first to characterise the constituents of the

adsorbed SAPL. This evidence that indigenous SAPL adsorbs to artificial surfaces

in vivo adds to the strong support that artificial joints are lubricated by SAPL. The

composition of SAPL found on retrieved implants is made up of four main species

of PC: namely PLPC, POPC, SLPC and DPPC. USPC species are dominant. Future

tribo tests (friction and wear trials) should adopt a lubricant similar to this detected

composition of the indigenous lubricant. The discovery of the constituents of SAPL

is invaluable for not only future tribo testing but also for artificial joint developers

and for the development of effective cures for several disease processes in the

natural joint where lubrication may play a role. Treatments for OA that inject a so-

called lubricant (viscosupplementation) into the joint should adopt a lubricant that

mimics the lubricating portion of SF that has been detected on TJRs.

The effectiveness of adsorbed SAPL to an artificial joint as a boundary lubricant

was proven when an explanted prosthesis was shown to have considerably less

friction when tested on a tribometer in its ex vivo state prior to being cleaned with a

strong organic solvent. Therefore artificial joints are boundary lubricated in vivo

and the indigenous boundary lubricant has been identified as SAPL. This adds to

the strong support that the same occurs in the natural joint and has implications to a

model for the pathogenesis for osteoarthritis.

Regardless of the material, future prosthetic designs need to take into consideration

the surface active nature of the indigenous boundary lubricant and provide surfaces

that are conducive to SAPL attachment in order to reduce friction and, ultimately,

wear. One such surface ideal for this application is the PyC surface.

10.2 Future Work

• Determine actual amounts of SAPL attached to retrieved implants and

hence determine what surfaces are preferred in vivo. This would also

indicate the concentration or amount of SAPL to be applied to surfaces for

in vitro testing.


175

• Visualisation is key to understanding the mechanism whereby SAPL

lubricates a surface for both the natural joint and the artificial joint. AFM

and SFA may be useful for this.

• Modify the surface of PyC (and the other prosthetic materials for that

matter) to enhance SAPL attachment.

• Continue Pyrolytic Carbon along the development path as a very real

candidate for future load bearing prostheses by performing wear

simulations.

• Search for the presence of HA and Lubricin on retrieved implants to either

prove or disprove their role in the lubrication of artificial joints.

• Further studies into the tribology of the natural and artificial joint will be

invaluable to the quality of life for millions of individuals if OA can be

cured.


176

177

References

1. Adamson, A.W. and Gast, A.P. (1997) Physical Chemistry of Surfaces. 6th

ed, New York / Chichester / Weinheim / Brisbane / Singapore / Toronto:

John Wiley & Sons Inc. 784.

2. Ahlroos, T. (2001) Effect of Lubricant on the Wear of Prosthetic Joint

Materials, in Laboratory of Machine Design, Helsinki University of

Technology: Helsinki. 26.

3. Ahlroos, T. and Saikko, V. (1997). "Wear of prosthetic joint materials in

various lubricants." Wear 211(1): 113-119.

4. American Academy of Orthopaedic Surgeons (2002) FAQ's about

Osteoarthritis. Your Orthopaedic Connection,

5. Archibald, F.R. (1969) Squeeze films, in Handbook of Lubrication, J.J.

O'Connor, Boyd, J., Avallone, E.A., Editor, McGraw-Hill: New York. p. 7-

1 - 7-8.

6. Australian Orthopaedic Association (2002) National Joint Replacement

Registry. 82.

7. Axén, N., Hogmark, S., and Jacobson, S. (2001) Friction and Wear

Measurement Techniques, in Modern Tribology Handbook, B. Bhushan,

Editor, CRC Press: New York. p. 493-510.

8. Bader, D. and Lee, D. (2000) Structure - properties of soft tissues: articular

cartilage, in Structural Biological Materials: Design and Structure-

Property Relationships, M. Elices, Editor, Elsevier Science Ltd.: Oxford. p.

75-103.

9. Baier, R.E., Gott, V.L., and Feruse, A. (1970). "Surface chemical

evaluation of thromboresistant materials before and after venous

implanttion." Trans Am Soc Artif Intern Organs 16: 50-7.

10. Balazs, E.A. (1968). "Viscoelastic properties of hyaluronic acid and

biological lubrication." Univ Mich Med Cent J: 255-9.

11. Ballantine, G.C. and Stachowiak, G.W. (2002). "The effects of lipid

depletion on osteoarthritic wear." Wear 253(3-4): 385-393.

12. Barnes, G.T. and Gentle, I.R. (2005) Interfacial Science - An Introduction.

1st ed, New Tork: Oxford. 247.

13. Barnett, C.H. and Cobbold, A.F. (1962). "Lubrication within living joints."

Journal of Bone and Joint Surgery 44B: 662.

178

14. Batchelor, A.W. and Stachowiak, G.W. (1996). "Arthritis and the

interacting mechanisms of synovial joint lubrication. Part II - Joint

lubrication and its relation to arthritis." J. Orthop. Rheumatol. 9: 11-21.

15. Bell, J., Tipper, J.L., et al. (2001). "The influence of phospholipid

concentration in protein-containing lubricants on the wear of ultra-high

molecular weight polyethylene in artificial hip joints." Proceedings of the

Institution of Mechanical Engineers, Part H: Journal of Engineering in

Medicine 215(2): 259-263.

16. Bennett, A. and Higginson, G.R. (1970). "Hydrodynamic lubrication of soft

solids." Journal of Mechanical Engineering Science 12(3): 218-222.

17. Benz, M., Chen, N., et al. (2005). "Static forces, structure and flow

properties of complex fluids in highly confined geometries." Ann Biomed

Eng 33(1): 39-51.

18. Bernhard, W., Postle, A., et al. (1995). "Composition of phospholipid

classes and phosphatidylcholine molecular species of gastric mucosa and

mucus." Biochim Biophys Acta 1255: 99-104.

19. Bernhard, W., Postle, A., et al. (2001). "Pulmonary and gastric surfactants.

A comparison of the effect of surface requirements on function and

phospholipid composition." Comp Biochem Physiol A Mol Integr Physiol

(129): 173-182.

20. Bhushan, B. (2001) Modern Tribology Handbook. Vol. 1, New York: CRC

Press.

21. Biresaw, G., ed. (1989) Tribology and the Liquid-Crystalline State.

American Chemical Society. Vol. 441: Miami Beach, Florida, Maple Press,

York. 133.

22. Black, J. and Hastings, G., eds. (1998) Handbook of Biomaterial

Properties. Melbourne, Chapman and Hall.

23. Blanchard, C.R. (1995) Biomaterials: Body Parts of the Future. [cited;

Available from: http://www.swri.edu/3pubs/ttoday/fall95/implant.htm.

24. Bokros, J.C. (1969) Deposition, structure, and properties of pyrolytic

carbon, in Chemistry and Physics of Carbon. p. 1-118.

25. Bole, G.G., Jr. and Peltier, D.F. (1962). "Synovial fluid lipids in normal

individuals and patients with rheumatoid arthritis." Arthritis Rheumat. 5:

589-601.

26. Bowsher, J.G. and Shelton, J.C. (2001). "A hip simulator study of the

influence of patient activity level on the wear of crosslinked polyethylene

under smooth and roughened femoral conditions." Wear 250(1-12): 167-

179.

179

27. Brandt, K.D., Smith, G.N., Jr., and Simon, L.S. (2000). "Intraarticular

injection of hyaluronan as treatment for knee osteoarthritis: what is the

evidence?" Arthritis Rheum 43(6): 1192-203.

28. Broom, N.D. (1988) The collagen framework of articular cartilage: its

profound influence on normal and abnormal load-bearing function, in

Collagen, M.E. Nimni, Editor, CRC Press: Boca Raton. p. 244-264.

29. Brown, E.S. (1964). "Isolation and Assay of Dipalmityl Lecithin in Lung

Extracts." Am J Physiol 207: 402-6.

30. Brown, E.S., Johnson, R.P., and Clements, J.A. (1959). "Pulmonary surface

tension." J Appl Physiol 14: 717-20.

31. Brown, S.S. and Clarke, I.C. (2006). "A Review of Lubrication Conditions

for Wear Simulation in Artificial Hip Replacements." Tribology

Transactions 49(1): 72.

32. Buckwalter, J.A. (1983). "Articular cartilage." Instr Course Lect 32: 349-

70.

33. Buckwalter, J.A. and Lane, N.E. (1997). "Athletics and osteoarthritis." Am

J Sports Med 25(6): 873-81.

34. Butler, B.D., Lichtenberger, L.M., and Hills, B.A. (1983). "Distribution of

surfactants in the canine gastrointestinal tract and their ability to

lubricate." Am J Physiol 244(6): G645-51.

35. Calonius, O. (2002) Tribology of Prosthetic Joints - Validation of Wear

Simulation Methods, in Department of Mechanical Engineering, Helsinki

University of Technology: Espoo.

36. Caplan, A.I., Elyaderani, M., et al. (1997). "Principles of cartilage repair

and regeneration." Clinical Orthopaedics and Related Research 342: 254-

269.

37. Caygill, J.C. and West, G.H. (1969). "The rheological behaviour of

synovial fluid and its possible relation to joint lubrication." Medical and

Biological Engineering 7: 507-516.

38. Charnley, J. (1959). "The lubrication of animal joints." Institution of

Mechanical Engineers: Symposium on Biomechanics 17: 12-22.

39. Charnley, J. (1966). "An artificial bearing in the hip joint: implications in

biological lubrication." Fed Proc 25(3): 1079-81.

40. Charnley, J. (1982) Long Term Results of Low-Friction Arthroplasty. in The

Hip: Proceedings of the Tenth Open Scientific Meeting of the Hip Society.

1982. St Louis: C. V. Mosby.

41. Chen, Y. and Hills, B. (2004) Unsaturated phosphatidylcholines and uses

thereof: International Patent Application - Australia. PCT/AU2004/001290.

180

42. Chen, Y. and Hills, B.A. (2000). "Surgical Adhesions: Evidence for

Adsorption of Surfactant to Peritoneal Mesothelium." ANZ Journal of

Surgery 70(6): 443-447.

43. Chen, Y., Hills, B.A., and Hills, Y.C. (2005). "Unsaturated

phosphatidylcholine and its application in surgical adhesion." ANZ Journal

of Surgery 75(12): 1111-1114.

44. Chikama, H. (1985). "The role of protein and hyaluronic acid in the

synovial fluid in animal joint lubrication." Nippon Seikeigeka Gakkai

Zasshi 59(5): 559-72.

45. Chung, A.C., Shanahan, J.R., and Brown, E.M., Jr. (1962). "Synovial fluid

lipids in rheumatoid and osteoarthritis." Arthritis Rheum 5: 176-83.

46. Chung, Y., Homolam, A.M., and Bryan Street, G., eds. (1991) Surface

Science Investigations in Tribology. York, PA, Maple Press. 253.

47. Clements, J.A. (1957). "Surface tension of lung extracts." Proc Soc Exp

Biol Med 95(1): 170-2.

48. Coller, R. (2002) Friction Testing Using Surfactant as the Boundary

Lubricant, Queensland University of Technology. 85.

49. Coller, R., Hargreaves, D.J., et al. (2004). "Is SAPL the Boundary Lubricant

in Prosthetic Joints: Friction Testing and Surface Rinsing." Australian

Journal of Mechanical Engineering 1: 63-71.

50. Comper, W.D. and Laurent, T.C. (1978). "Physiological function of

connective tissue polysaccharides." Physiol Rev 58(1): 255-315.

51. Cook, S.D., Thomas, K.A., and Kester, M.A. (1989). "Wear characteristics

of the canine acetabulum agianst different femoral prostheses." The Journal

of Bone and Joint Surgery 71-B(2): 188-197.

52. Cooke, A.F., Dowson, D., and Wright, V. (1978). "The rheology of synovial

fluid and some potential synthetic lubricants for degenerate synovial

joints." Engineering in Medicine 7: 66-72.

53. Craig, L.E. and LaBerge, M. (1994) Effect of DPPC concentration on the

boundary lubrication of rigid bearings: An arthroplasty model. in

Proceedings of the 15th Annual Conference of the Canadian Biomaterials

Society. 1994. Quebec City, Quebec.

54. Currey, J., Unsworth, A., and Hall, D.A. (1981) Properties of bone,

cartilage & synovial fluid., in Introduction to Joints and Joint Replacement,

D. Dowson and V. Wright, Editors, Mechanical Engineering Publications

Ltd: London. p. 103-119.

55. Davis, W.H., Jr., Lee, S.L., and Sokoloff, L. (1978). "Boundary lubricating

ability of synovial fluid in degenerative joint disease." Arthritis Rheum

21(7): 754-6.

181

56. Davis, W.H., Lee, S.L., and Sokoloff, L. (1979). "A Proposed Model of

Boundary Lubrication by Synovial Fluid: Structuring of Boundary Water."

Journal of Biomechanical Engineering 101: 185-192.

57. de Medicis, R., Reboux, J.F., and Lussier, A. (1976). "[Synovial fluid.

Review of international literature from 1972 to 1975 (author's transl)]."

Pathol Biol (Paris) 24(9): 641-56.

58. DeHaven, K.E. (1990). "Decision-making factors in the treatment of

meniscus lesions." Clin Orthop Relat Res (252): 49-54.

59. DeSchryver-Kecskemeti, K., Eliakim, R., et al. (1989). "Intestinal

surfactant-like material. A novel secretory product of the rat enterocyte." J

Clin Invest 84(4): 1355-61.

60. Dinnar, U. (1975). "Lubrication theory in synovial joints." CRC Critical

Reviews in Bioengineering 2(2): 159-177.

61. Dintenfass, L. (1963). "Lubrication in synovial joints." Nature 197: 496-

497.

62. Dintenfass, L. (1963). "Lubrication in synovial joints: a theoretical analysis

- a rheological approach to the problems of joint movement and joint

lubrication." Journal of Bone and Joint Surgery 45A: 1241-1256.

63. Donnelly, W.J., et al. (1997). "Radiological and survival comparison of

four methods of fixation of a proximal femoral stem." Journal of Bone and

Joint Surgery 79-Br(3): 351-360.

64. Dorinson, A. and Ludema, K.C. (1985) Lubricant additive action. I - Basic

catergories and mechanisms., in Mechanics and Chemistry in Lubrication,

A. Dorinson and K.C. Ludema, Editors, Elsevier: Amsterdam. p. 198-254.

65. Dorinson, A. and Ludema, K.C. (1985) Lubricant additive action. II -

Chemical reactivity and additive functionality., in Mechanics and

Chemistry in Lubrication, A. Dorinson and K.C. Ludema, Editors, Elsevier:

Amsterdam. p. 255-307.

66. Dowson, D. (1966-67). "Modes of lubrication in human joints - Paper 12."

Proceedings of the Institution of Mechanical Engineers 191(3-J): 45.

67. Dowson, D. (1973). "Lubrication and wear of joints." Physiotherapy 59(4):

104-106.

68. Dowson, D. (1990) Biotribology of natural and replacement synovial joints,

in Biomechanics of Diarthroidal Joints, V.C. Mow, A. Ratcliffe, and S.L.Y.

Wood, Editors, Springer-Verlag: New York. p. 305-345.

69. Dowson, D., Fisher, J., et al. (1991). "Design considerations for cushion

form bearings in artificial hip joints." Proc Inst Mech Eng [H] 205(2): 59-

68.

182

70. Dowson, D. and Jin, Z. (1986). "Micro-elastohydrodynamic lubrication of

synovial joints." Proceedings of the Institution of Mechanical Engineers.

Part H - Journal of Engineering in Medicine 15(2): 63-65.

71. Dowson, D., Longfield, M.D., et al. (1968). "An investigation of the friction

and lubrication in human joints." Proceedings of the Institution of

Mechanical Engineers 182(London): 68-76.

72. Dowson, D., Priest, M., et al., eds. (1998) Lubrication at the frontier : the

role of the interface and surface layers in the thin film and boundary

regime. Tribology and Interface Engineering Series, No. 36, ed. D.

Dowson, Elsevier. 893.

73. Dowson, D., Unsworth, A., et al. (1981) Lubrication of Joints, in An

Introduction to the Biomechanics of Joints and Joint Replacement, D.

Dowson and V. Wright, Editors, Mechanical Engineering Publication Ltd.:

London. p. 120-145.

74. Dowson, D. and Wright, V. (1973) Bio-Tribology, in The Rheology of

Lubricants, T.C. Davenport, Editor, Barking : Applied Science Publishers

on behalf of the Institute of Petroleum: Longman London. p. 81-88.

75. Dowson, D., Wright, V., and Longfield, M.D. (1969). "Human joint

lubrication." Biomedical Engineering 4: 160-165.

76. Dumbleton, J.H. (1981) Tribology of Natural and Artificial Joints,

Amsterdam: Elsevier Scientific Publishing.

77. Erdemir, A. (2001) Solid lubricants and self-lubricating solids, in Modern

Tribology Handbook, B. Bhushan, Editor, CRC Press: New York. p. 787-

825.

78. Ethell, M.T., Hodgson, D.R., and Hills, B.A. (1999). "The synovial

response to exogenous phospholipid (synovial surfactant) injected into the

equine radiocarpal joint compared with that to prilocaine, hyaluronan and

propylene glycol." New Zealand Veterinary Journal 47(4): 128-132.

79. Eyre, D.R., Wu, J.J., and Apone, S. (1987). "A growing family of collagens

in articular cartilage: identification of 5 genetically distinct types." J

Rheumatol 14 Spec No: 25-7.

80. Faber, J.J., Williamson, G.R., and Feldman, N.T. (1967). "Lubrication of

joints." J Appl Physiol 22(4): 793-799.

81. Felson, D.T. (1990). "Osteoarthritis." Rheum Dis Clin North Am 16(3):

499-512.

82. Felson, D.T. (1998) Epidemology of osteoarthritis, in Osteoarthritis, K.D.

Brandt, M. Doherty, and L.S. Lomander, Editors, Oxford University Press:

New York. p. 13-22.

183

83. Felson, D.T. and Radin, E.L. (1994). "What causes knee osteoarthrosis: are

different compartments susceptible to different risk factors?" J Rheumatol

21(2): 181-3.

84. Ferguson, J. and Nuki, G. (1973) The Rheology of a Synthetic Joint

Lubricant, in The Rheology of Lubricants, T.C. Davenport, Editor, Barking

: Applied Science Publishers on behalf of the Institute of Petroleum:

Longman London. p. 89-95.

85. Fisher, J. (2000) Materials for Improved Wear Resistance of Total Artificial

Joints, M.o. Understanding, Editor, University of Leeds: Leeds.

86. Fisher, J. and Dowson, D. (1991). "Tribology of total artificial joints."

Proceedings of the Institution of Mechanical Engineers. Part H - Journal of

Engineering in Medicine 205(2): 73-79.

87. Flores, R.H. and Hochberg, M. (1998) Definition and classification of

osteoarthritis, in Osteoarthritis, K.D. Brandt, M. Doherty, and L.S.

Lomander, Editors, Oxford University Press: New York. p. 1-12.

88. Fox, R.I., Lotz, M., and Carson, D.A. (1989) Structure and function of

synviocytes, in Arthritis and Allied Conditions, a Textbook of

Rheumatology, D.J. McCarty, Editor, Lea & Febiger: Philadelphia. p. 273-

288.

89. Fraser, J.R. and Laurent, T.C. (1989). "Turnover and metabolism of

hyaluronan." Ciba Found Symp 143: 41-53; discussion 53-9, 281-5.

90. Freeman, M.A.R. and Meachim, G. (1974) Ageing, degeneration and

remodelling of articular cartilage, in Adult Articular Cartilage, M.A.R.

Freeman, Editor, Grune and Stratton, Inc.: New York. p. 287-329.

91. Freeman, M.A.R., Swanson, S.A.V., and Manley, P.T. (1975). "Stress-

lowering function of articular cartilage." Medical and Biological

Engineering: 245-251.

92. Fukuda, Y., Takai, S., et al. (2000). "Impact load transmission of the knee

joint - influence of leg alignment and the role of meniscus and articular

cartilage." Clinical Biomechanics 15: 516-521.

93. Furey, M.J. (2000) Joint Lubrication, in The Biomedical Engineering

Handbook, Second Edition, J.D. Bronzino, Editor, CRC Press: Boca Raton.

p. 1-27.

94. Furey, M.J. and Burkhardt, B.M. (1997). "Biotribology: Friction, wear and

lubrication of natural synovial joints." Lubric Sci 9(3): 273-281.

95. Furey, M.J. and Burkhardt, B.M. (1997) Biotribology: Friction, Wear, and

Lubrication of Natural Synovial Joints, in Lubrication Science. p. 255-271.

184

96. Gale, L.R., Chen, Y., et al. (2006). "Boundary lubrication of joints:

Characterisation of Surface-Active Phospholipids found on retrieved

implants." Acta Orthopaedica In Press.

97. Gale, L.R., Coller, R., et al. (2007). "The role of SAPL as a boundary

lubricant in prosthetic joints." Tribology International 40(4): 601-606.

98. Gavrjushenko, N.S. (1993). "Recommendations with respect to the

improvement of lubricating qualities of synovial fluid in artificial joints."

Proc Inst Mech Eng [H] 207(2): 111-4.

99. Gellman, A.J. and Spencer, N.D. (2005) Surface chemistry in tribology, in

Wear : materials, mechanisms and practice, G.W. Stachowiak, Editor,

Wiley: Chichester. p. 458.

100. Ghadially, F.N. (1978) Fine structure of joints, in The Joints and Synovial

Fluid, L. Sokoloff, Editor, Academic Press: New York. p. 105-176.

101. Ghadially, F.N. (1983) Fine structure of synovial joints. A Text and Atlas

of the Ultrastructure of Normal and Abnormal Synovial Joints, England:

Butterworth & Co Ltd.

102. Ghadially, F.N., Lalonde, J.M., and Wedge, J.H. (1983). "Ultrastructure of

normal and torn menisci of the human knee joint." J Anat 136(Pt 4): 773-

91.

103. Girod, S., Zahm, J.M., et al. (1992). "Role of the physiochemical properties

of mucus in the protection of the respiratory epithelium." Eur Respir J 5(4):

477-87.

104. Glenister, T.W. (1976). "An embryological view of cartilage." J Anatomy

122: 323-330.

105. Glynn, L.E. (1977). "Primary lesion in osteoarthrosis." Lancet 1(8011):

574-5.

106. Gray, H. (1918) Anatomy of the Human Body, Philadelphia: Lea &

Febiger.

107. Greenwald, R.A., Moy, W.W., and Seibold, J. (1978). "Functional

properties of cartilage proteoglycans." Semin Arthritis Rheum 8(1): 53-67.

108. Guerra, D., Frizziero, L., et al. (1996). "Ultrastructural identification of a

membrane-like structure on the surface of normal articular cartilage." J

Submicrosc Cytol Pathol 28(3): 385-93.

109. Gvozdanovic, D., Wright, V., and Dowson, D. (1975). "Formation of

lubricating monolayers on the cartilage surface." Ann Rheum Dis

34(Suppl. 2): 100-101.

185

110. Hale, J.E., Rudert, M.J., and Brown, T.D. (1993). "Indentation assessment

of biphasic mechanical property deficits in size-dependant osteochondral

defect repair." J Biomechanics 26: 1319-1325.

111. Hall, R.M., Unsworth, A., et al. (1997). "The friction of explanted hip

prostheses." British J Rheumatology 36(1): 20-26.

112. Hamerman, D., Rosenberg, L.C., and Schubert, M. (1970). "Diarthrodial

joints revisited." J Bone Joint Surg Am 52(4): 725-74.

113. Hanson, S.R. (1998) Blood-Material Interactions, in Handbook of

Biomaterial Properties, J. Black and G.R. Hastings, Editors, Chapman and

Hall: London. p. 545-555.

114. Henderson, B. and Pettipher, E.R. (1985). "The synovial lining cell: biology

and pathobiology." Semin Arthritis Rheum 15(1): 1-32.

115. Henderson, B., Revell, P.A., and Edwards, J.C. (1988). "Synovial lining cell

hyperplasia in rheumatoid arthritis: dogma and fact." Ann Rheum Dis

47(4): 348-9.

116. Heuberger, M.P., Widmer, M.R., et al. (2005). "Protein-mediated boundary

lubrication in arthroplasty." Biomaterials 26(10): 1165-73.

117. Higaki, H., Murakami, T., and Nakanishi, Y. (1997). "Lubricating Ability of

Langmuir-Blodgett films as boundary lubricating films on articular

surfaces." JSME Int J 40(4): 776-781.

118. Higaki, H., Murakami, T., et al. (1998). "The Lubricating Ability of

Biomembrane Models with Dipalmitoyl Phosphatidylcholine and gamma-

Globulin." Proceedings of the Institution of Mechanical Engineers, Part H:

Journal of Engineering in Medicine 212(5): 337-346.

119. Higginson, G.R. (1978). "Elastohydrodynamic lubrication in human joints."


120. Hills, B.A. (1984). "Analysis of eustachian surfactant and its function as a

release agent." Arch Otolaryngol 110(1): 3-9.

121. Hills, B.A. (1984). "Hydrophobic lining of the eustachian tube imparted by

surfactant." Arch Otolaryngol 110(12): 779-82.

122. Hills, B.A. (1984). "Surfactant as a release agent opposing the adhesion of

tumor cells in determining malignancy." Med Hypotheses 14(1): 99-110.

123. Hills, B.A. (1988) The Biology of Surfactant. Vol. 321, Cambridge:

Cambridge University Press.

124. Hills, B.A. (1989). "Oligolamellar lubrication of joints by surface active

phospholipid." J Rheumatol 16(1): 82-91.

186

125. Hills, B.A. (1990). "Multiple roles for surface-active phospholipid in

hypertension." Medical Hypotheses 33(4): 275-281.

126. Hills, B.A. (1990). "Oligolamellar Nature of the Articular Surface." Journal

of Rheumatology 17(3): 349-356.

127. Hills, B.A. (1990). "Surface-active phospholipid in muscle lymph and its

lubricating and adhesive properties." Lymphology 23(1): 39-47.

128. Hills, B.A. (1995). "Remarkable anti-wear properties of joint surfactant."

Ann Biomed Eng 23(2): 112-5.

129. Hills, B.A. (1996). "Lubrication of visceral movement and gastric motility

by peritoneal surfactant." Journal of Gastroenterology and Hepatology 11:

797-803.

130. Hills, B.A. (2000). "Boundary lubrication in vivo." Proceedings of the

Institution of Mechanical Engineers. Part H - Journal of Engineering in

Medicine 214(1): 83-94.

131. Hills, B.A. (2000). "Role of surfactant in peritoneal dialysis." Peritoneal

Dialysis International: Journal Of The International Society For Peritoneal

Dialysis 20(5): 503-515.

132. Hills, B.A. (2002). "Surface-active phospholipid: a Pandora's box of

clinical applications. Part II. Barrier and lubricating properties." Intern

Med J 32(5-6): 242-251.

133. Hills, B.A. and Butler, B.D. (1984). "Identification of surfactants in

synovial fluid and their ability to act as boundary lubricants." Ann. Rheum.

Dis. (48): 51-57.

134. Hills, B.A. and Butler, B.D. (1984). "Surfactants identified in synovial fluid

and their ability to act as boundary lubricants." Ann Rheum Dis 43(4):

641-8.

135. Hills, B.A. and Butler, B.D. (1985). "Phospholipids identified on the

pericardium and their ability to impart boundary lubrication." Ann Biomed

Eng 13(6): 573-86.

136. Hills, B.A. and Butler, B.D. (1986). "Surfactants identified on the

pericardium and their ability to impart boundary lubrication." Annals of

Biomedical Engineering 13: 573-586.

137. Hills, B.A., Butler, B.D., and Barrow, R.E. (1982). "Boundary lubrication

imparted by pleural surfactants and their identification." Journal of Applied

Physiology 53(2): 463-9.

138. Hills, B.A. and Cotton, D.B. (1986). "Release and lubricating properties of

amniotic surfactants and the very hydrophobic surfaces of the amnion,

chorion, and their interface." Obstet Gynecol 68(4): 550-4.

187

139. Hills, B.A. and Crawford, R.W. (2003). "Normal and prosthetic synovial

joints are lubricated by surface-active phospholipid: a hypothesis." The

Journal of Arthroplasty 18(4): 499-505.

140. Hills, B.A. and Jay, G.D. (2002). "Identity of the Joint Lubricant." J

Rheumatol 29(1): 200-1.

141. Hills, B.A. and Monds, M. (1998). "Enzymatic identification of the load-

bearing boundary lubricant in the joint." Rheumatology 37(2): 137-142.

142. Hills, B.A. and Thomas, K. (1998). "Joint Stiffness and 'articular gelling':

inhibition of the fusion of articular surfaces by surfactant." British Journal

of Rheumatology 37: 532-538.

143. Hlavacek, M. (1995). "The role of synovial fluid filtration by cartilage in

lubrication of synovial joints--IV. Squeeze-film lubrication: the central film

thickness for normal and inflammatory synovial fluids for axial symmetry

under high loading conditions." Journal of Biomechanics 28(10): 1199-

1205.

144. Hou, J.S., Holmes, M.H., et al. (1989). "Boundary conditions at the

cartilage-synovial fluid interface for joint lubrication and theoretical

verifications." J Biomech Eng 111(1): 78-87.

145. Hou, J.S., Mow, V.C., et al. (1992). "An analysis of the squeeze-film

lubrication mechanism for articular cartilage." Journal of Biomechanics

25: 247-259.

146. How, M.J., Long, V.J., and Stanworth, D.R. (1969). "The association of

hyaluronic acid with protein in human synovial fluid." Biochim Biophys

Acta 194(1): 81-90.

147. Hsu, S.M. and Gates, R.S. (2001) Boundary lubrication and boundary

lubricating films, in Modern Tribology Handbook, B. Bhushan, Editor,

CRC Press: New York. p. 455-492.

148. Hsu, S.M., Zhang, J., and Yin, Z. (2002). "The Nature and Origin of

Tribochemistry." Tribology Letters 13(2): 131-139.

149. http://en.wikipedia.org/wiki/Membrane_lipids. (2005) [cited.

150. http://www.utahhipandknee.com/history.htm. (2004) [cited.

151. Huber, M., Trattnig, S., and Lintner, F. (2000). "Anatomy, biochemistry,

and physiology of articular cartilage." Invest Radiol 35(10): 573-80.

152. Hutchings, I.M., ed. (2003) Friction, Lubrication, and Wear of Artificial

Joints. London, Professional Engineering Publishing. 133.

153. Ingham, E. and Fisher, J. (2000). "Biological reactions to wear debris in

total joint replacement." Proceedings of the Institution of Mechanical

Engineers. Part H - Journal of Engineering in Medicine 214(1): 21-37.

188

154. Israelachvili, J.N. (1992) Intermolecular and surface forces. 2nd ed, London

; New York: Academic Press. 450p.

155. Jalali-Vahid, D., Jagatia, M., et al. (2000) Elastohydrodynamic lubrication

analysis of UHMWPE hip joint replacements. in Thinning films and

tribological interfaces. 2000. Leeds: Elsevier.

156. Jalali-Vahid, D., Jagatia, M., et al. (2001). "Prediction of lubricating film

thickness in UHMWPE hip joint replacements." J Biomech 34(2): 261-6.

157. Jay, G.D. (1990) Joint lubrication: A physicochemical study of a purified

lubricating factor from bovine synovial fluid, State University of New York

at Stony Brook: United States -- New York.

158. Jay, G.D. (2004). "Lubricin and surfacing of articular joints." Current

Opinion in Orthopedics 15(5): 355-359.

159. Jay, G.D. and Cha, C.J. (1999). "The effect of phospholipase digestion upon

the boundary lubricating ability of synovial fluid." J Rheumatol 26(11):

2454-7.

160. Jay, G.D., Elsaid, K.A., et al. (2004). "Lubricating ability of aspirated

synovial fluid from emergency department patients with knee joint

synovitis." J Rheumatology 31(3): 557-64.

161. Jayson, M.I. and Dixon, A.S. (1970). "Intra-articular pressure in

rheumatoid arthritis of the knee. 3. Pressure changes during joint use." Ann

Rheum Dis 29(4): 401-8.

162. Jazrawi, L.M., Kummer, F.J., and DiCesare, P.E. (1998). "Alternative

bearing surfaces for total joint arthroplasty." Journal of the American

Academy of Orthopaedic Surgeons 6(4): 198-203.

163. Jin, Z., Dowson, D., and Fisher, J. (1993) Fluid film lubrication in natural

hip joints. in Thin Films in Tribology: Tribology Series 25. 1993.

University of Leeds, U.K.: Elsevier.

164. Jin, Z.M., Dowson, D., and Fisher, J. (1997). "Analysis of Fluid Film

Lubrication in Artificial Hip Joint Replacements with Surfaces of High

Elastic Modulus." Proceedings of the Institution of Mechanical Engineers,

Part H: Journal of Engineering in Medicine 211(3): 247-256.

165. Jin, Z.M., Medley, J.B., and Dowson, D. (2002) Fluid film lubrication in

artificial hip joints. in Tribological Reserach and Design for Engineering

Systems: Tribology Series, 41. 2002. Leeds, UK: Elsevier.

166. Jones, E.S. (1934). "Joint lubrication." Lancet: 1426-1427.

167. Jones, E.S. (1936). "Joint lubrication." Lancet: 1043-1044.

168. Jones, H.P. and Walker, P.S. (1968). "Casting techiques applied to study of

human joints." Scientific Technology 14: 57-68.

189

169. Kawano, T., Miura, H., et al. (2003). "Mechanical effects of the

intraarticular administration of high molecular weight hyaluronic acid plus

phospholipid on synovial joint lubrication and prevention of articular

cartilage degeneration in experimental osteoarthritis." Arthritis Rheum

48(7): 1923-9.

170. Klaus, M.H., Clements, J.A., and Havel, R.J. (1961). "Composition of

surface-active material isolated from beef lung." Proc Natl Acad Sci U S A

47: 1858-9.

171. Knight, A.D. and Levick, J.R. (1983). "The density and distribution of

capillaries around a synovial cavity." Q J Exp Physiol 68(4): 629-44.

172. Kobayashi, A., et al (1997). "Early radiological observations may predict

the long term survival of femoral hip prostheses." Journal of Bone and Joint

Surgery 79-B(4): 583-589.

173. Kobayashi, M. and Oka, M. (2003). "The lubricative function of artificial

joint material surfaces by confocal laser scanning microscopy. Comparison

with natural synovial joint surface." Biomed Mater Eng 13(4): 429-37.

174. Kuettner, K.E., Aydelotte, M.B., and Thonar, E.J. (1991). "Articular

cartilage matrix and structure: a minireview." J Rheumatol Suppl 27: 46-8.

175. LaGrange, L.D., Gott, V.L., et al. (1969) Compatibility of carbon and

blood. in Artificial Heart Program Conference Proceedings. 1969.

Washington, DC.: US Government Printing Office.

176. Lai, W.M., Kuei, S.C., and Mow, V.C. (1978). "Rheological Equations for

Synovial Fluids." Journal of Biomechanical Engineering 100: 169-186.

177. Lane, N.E. and Buckwalter, J.A. (1993). "Exercise: a cause of

osteoarthritis?" Rheum Dis Clin North Am 19(3): 617-33.

178. Larsen, R.G. and Perry, G.L. (1950) Chemical Aspects of Wear and

Friction, in Mechanical Wear, American Society of Metals, J.T. Burwell,

Editor. p. 73-94.

179. Larson, C.M. and Larson, R. (1969) Lubricant additives, in Standard

Handbook of Lubrication, J. O'Connor.J, Boyd, J., Avallone, E.A., Editor,

McGraw-Hill: New York. p. 14-1 - 14-24.

180. Laurent, T.C., Laurent, U.B., and Fraser, J.R. (1996). "The structure and

function of hyaluronan: An overview." Immunol Cell Biol 74(2): A1-7.

181. Levick, J. (1987) Synovial fluid and trans-synovial flow in stationary and

moving normal joints, in Joint Loading, H.J. Helminen, et al., Editors,

Wright: Bristol.

182. Levick, J. (1989). "Synovial Fluid Exchange - A Case of Flow Through

Fibrous Mats." News Physiol Sci 4(5): 198-202.

190

183. Levick, J.R. (1995). "Microvascular architecture and exchange in synovial

joints." Microcirculation 2(3): 217-33.

184. Lewis, P.R. and McCutchen, C.W. (1959). "Experimental evidence for

weeping lubrication in mammalian joints." Nature 184: 1285.

185. Liang, H. (2004) Mechanical Tribology: Materials, Characterization and

Applications, ed. G.E. Totten, Seattle, WA USA: Marcel Dekker Inc. 496.

186. Liao, Y.-S., Benya, P.D., and McKellop, H.A. (1998). "Effect of protein

lubrication on the wear properties of materials for prosthetic joints."

Journal of Biomedical Materials Research 48(4): 465 - 473.

187. Ling, F.F., Klaus, E.E., and Fein, R.S., eds. (1969) Boundary Lubrication:

An Appraisal of World Literature. ASME Research Committe on

Lubrication: New York, United Engineering Center. 576.

188. Linn, F.C. (1967). "Lubrication of Animal Joints. I. The arthrotripsometer."

The Journal of Bone and Joint Surgery 49(A): 1079-1098.

189. Linn, F.C. (1968). "Lubrication of animal joints II: The mechanism."

Journal of Biomechanics 1: 93-205.

190. Linn, F.C. and Radin, E.L. (1968). "Lubrication of animal joints: III. The

effect of certain chemical alterations of the cartilage and the lubricant."

Arthritis & Rheumatism 11: 674.

191. Linn, F.C. and Sokoloff, L. (1965). "Movement and Composition of

Interstitial Fluid of Cartilage." Arthritis Rheum 8: 481-94.

192. Little, T.D., Freeman, M.A.R., and Swanson, S.A. (1969) Experiments on

friction in the human hip joint, in Lubrication and Wear in Joints,, V.

Wright, Editor, Lippincott Publisher,: Philadelphia. p. 110–114.

193. Lohmander, S. (1988). "Proteoglycans of joint cartilage. Structure,

function, turnover and role as markers of joint disease." Baillieres Clin

Rheumatol 2(1): 37-62.

194. Lu, Y., Levick, J.R., and Wang, W. (2005). "The mechanism of synovial

fluid retention in pressurized joint cavities." Microcirculation 12(7): 581-

95.

195. Ludema, K.C. (2001) Friction, in Modern Tribology Handbook, B.

Bhushan, Editor, CRC Press: New York. p. 205-233.

196. MacConaill, M.A. (1932). "The function of intra-articular fibrocartilages,

with special reference to the knee and inferior radio-ulnar joints." Journal

of Anatomy 66: 210-227.

197. Malcolm, L.L. (1976) An experimental investigation of the frictional and

deformational responses of articular cartilage interfaces to static and

dynamic loading., University of California: San Diego.

191

198. Mankin, H.J. and Brandt, K.D. (1984) Biochemistry and metabolism of

cartilage in osteoarthritis., in Osteoarthritis: Diagnosis and Management,

R.W. Moskowitz, et al., Editors, WB Sauders Co.: USA. p. 43-79.

199. Mankin, H.J. and Lippiello, L. (1969). "The turnover of adult rabbit

articular cartilage." J Bone Joint Surg Am 51(8): 1591-600.

200. Mansour, J.M. and Mow, V.C. (1977). "On the Natural Lubrication of

Synovial Joints: Normal and degenerate." Journal of Lubrication

Technology: 163-171.

201. Marcinko, D.E. and Dollard, M.D. (1986). "Physical and mechanical

properties of joints (the pathomechanics of articular cartilage

degeneration)." J Foot Surg 25(1): 3-13.

202. Maroudas, A. (1967). "Hyaluronic Acid Films." Proceedings of the

Institution of Mechanical Engineers 3J(181): 122-124.

203. Maroudas, A. (1976). "Transport of solutes through cartilage: permeability

to large molecules." J Anat 122(Pt 2): 335-47.

204. Maroudas, A. and Bullough, P. (1968). "Permeability of articular

cartilage." Nature 219(5160): 1260-1.

205. Maroudas, A. and Venn, M. (1977). "Chemical composition and swelling of

normal and osteoarthrotic femoral head cartilage. II. Swelling." Ann

Rheum Dis 36(5): 399-406.

206. Maroudas, A.I. (1976). "Balance between swelling pressure and collagen

tension in normal and degenerate cartilage." Nature 260(5554): 808-9.

207. Marshall, K.W. (2000). "Intra-articular hyaluronan therapy." Curr Opin

Rheumatol 12(5): 468-74.

208. McCutchen, C.W. (1959). "Mechanism of animal joints. Sponge-hydrostatic

and weeping bearings." Nature 184: 1284-1285.

209. McCutchen, C.W. (1962). "The frictional properties of animal joints."

Wear 5: 1-17.

210. McCutchen, C.W. (1966). "Boundary lubrication by synovial fluid:

demonstration and possible osmotic explanation." Fed. Am. Soc. Exp. Biol.

25: 1061-1068.

211. McCutchen, C.W. (1967). "Physiological lubrication." Proceedings of the

Institution of Mechanical Engineers 181(Part 3J): 55-62.

212. McCutchen, C.W. (1978) Lubrication of joints, in The Joints and Synovial

Fluid, L. Sokoloff, Editor, Academic Press, Inc: New York. p. 437-483.

213. McCutchen, C.W. (1982). "Cartilage is poroelastic, not viscoelastic

(including an exact theorem about strain energy and viscous loss, and an

192

order of magnitude relation for equilibration time)." J Biomechanics 15(4):

325-327.

214. McCutchen, C.W. (1983) Lubrication of and by articular cartilage, in

Cartilage, B.K. Hall, Editor, Academic Press Inc.: New York. p. 340.

215. McIlwraith, C.W. and Vachon, A. (1988). "Review of pathogenesis and

treatment of degenerative joint disease." Equine Vet J Suppl (6): 3-11.

216. McKibbin, B. and Maroudas, A. (1979) Nutrition and Metabolism, in Adult

Articular Cartilage, M.A.R. Freeman, Editor, Pitman Medical Publishing

Co.: London. p. 461-486.

217. Meachim, G. and Brooke, G. (1984). "The synovial response to intra-

articular acrylic cement particles in guinea pigs." Biomaterials 5(2): 69-

74.

218. Meachim, G. and Stockwell, R.A. (1974) The matrix, in Adult Articular

Cartilage, M.A.R. Freeman, Editor, Grune and Stratton, Inc.: New York. p.

1-50.

219. Medley, J.B., Dowson, D., and Wright, V. (1984). "Transient

elastohydrodynamic lubrication models for the human ankle joint."

Engineering in Medicine 13: 137-151.

220. Momberger, T.S., Levick, J.R., and Mason, R.M. (2005). "Hyaluronan

secretion by synoviocytes is mechanosensitive." Matrix Biol 24(8): 510-9.

221. More, R.B., Haubold, A.D., and Bokros, J.C. (2000) Pyrolytic Carbon for

Long-Term Medical Implants, Medical Carbon Research Institute: Austin,

Texas.

222. Mori, S., Naito, M., and Moriyama, S. (2002). "Highly viscous sodium

hyaluronate and joint lubrication." Int Orthop 26(2): 116-21.

223. Moro-oka, T., Miura, H., et al. (2000). "Mixture of hyaluronic acid and

phospholipid prevents adhesion formation on the injured flexor tendon in

rabbits." J Orthop Res 18(5): 835-40.

224. Mow, V.C., Ateshian, G.A., and Spilker, R.L. (1993). "Biomechanics of

diarthrodial joints: a review of twenty years of progress." J Biomech Eng

115(4B): 460-7.

225. Mow, V.C., Fithian, D.C., and Kelly, M.A. (1988) Fundamentals of

articular cartilage and meniscus biomechanics, in Articular Cartilage and

Knee Joint Function: Basic Science and Arthroscopy, J.W. Ewing, Editor,

Raven Press: New York. p. 1-18.

226. Mow, V.C. and Hayes, W.C. (1997) Basic Orthopaedic Biomechanics. 2nd

ed, Philadelphia: Lippincott-Raven.

193

227. Mow, V.C., Holmes, M.H., and Lai, W.M. (1984). "Fluid Transport and

Mechanical Properties of Articular Cartilage: A Review." Journal of

Biomechanics 17(5): 377-394.

228. Mow, V.C., Kuei, S.C., et al. (1980). "Biphasic Creep and Stress

Relaxation of Articular Cartilage in Compression: Theory and

Experiments." Journal of Biomechanical Engineering 102: 73-84.

229. Mow, V.C. and Mak, A.F. (1987) Lubrication of Diarthrodial Joints, in

Handbook of Bioengineering, McGraw-Hill. p. 5.1-5.34.

230. Muir, I.H.M. (1980) The chemistry of the ground substance of joint

cartilage, in The Joints and Synovial Fluid, L. Sokoloff, Editor, Academic

Press, Inc.: New York. p. 27-94.

231. Muller, F.J., Pita, J.C., et al. (1989). "Centrifugal characterization of

proteoglycans from various depth layers and weight-bearing areas of

normal and abnormal human articular cartilage." J Orthop Res 7(3): 326-

34.

232. Muller, M. (2004) Chemistry and the Building Blocks of Life. [cited.

233. Munro, L.A. (1964) Chemistry in Engineering, Englewood Cliffs, NJ.:

Prentice-Hall Inc. 159-190.

234. Murakami, T., Higaki, H., et al. (1998). "Adaptive multimode lubrication in

natural synovial joints and artificial joints." Proceedings of the Institution

of Mechanical Engineers. Part H - Journal of Engineering in Medicine 212:

23-35.

235. Myers, S.L. and Christine, T.A. (1983). "Hyaluronate synthesis by synovial

villi in organ culture." Arthritis Rheum 26(6): 764-70.

236. Nakano, T., Momozono, S., and Aizawa, S. (2000). "Tribological analysis

of bacterial flagellar motor." Japanese journal of tribology 45(1): 97-103.

237. Neame, P.J. and Barry, F.P. (1994). "The link proteins." Exs 70: 53-72.

238. Neame, R.L., Muir, K., et al. (2004). "Genetic risk of knee osteoarthritis: a

sibling study." Ann Rheum Dis 63(9): 1022-7.

239. Nitzan, D.W. (2001). "The process of lubrication impairment and its

involvement in temporomandibular joint disc displacement: a theoretical

concept." J Oral Maxillofac Surg 59(1): 36-45.

240. Nitzan, D.W., Mahler, Y., and Simkin, A. (1992). "Intra-articular pressure

measurements in patients with suddenly developing, severely limited mouth

opening." J Oral Maxillofac Surg 50(10): 1038-42; discussion 1043.

241. Nixon, A.J. (1991). "Articular cartilage surface structure and function."

Equine Vet Education 3: 72-75.

194

242. Nixon, J.S., Bottomley, K.M., et al. (1991). "Potent collagenase inhibitors

prevent interleukin-1-induced cartilage degradation in vitro." Int J Tissue

React 13(5): 237-41.

243. O'Hara, B.P., Urban, J.P., and Maroudas, A. (1990). "Influence of cyclic

loading on the nutrition of articular cartilage." Ann Rheum Dis 49(7):

536-9.

244. Ogston, A.G. and Stanier, J.E. (1953). "Some effects of hyaluronidase on

the hyaluronic acid of ox synovial fluid, and their bearing on the

investigation of pathological fluids." J Physiol 119(2-3): 253-8.

245. Oka, M., Kumar, P., et al. (2000). "Development of Artificial Articular

Cartilage." Proceedings of the Institution of Mechanical Engineers, Part H:

Journal of Engineering in Medicine 214(1): 59-68.

246. Ozturk, H.E., Stoffel, K.K., et al. (2004). "The Effect of Surface-Active

Phospholipids on the Lubrication of Osteoarthritic Sheep Knee Joints:

Friction." Tribology Letters 16(4): 283-289.

247. Panjabi, P.M. and White, A.A. (2001) Joint Friction, Wear and

Lubrication, in Biomechanics in the Musculoskeletal System, R. Zorab,

Editor, Churchill Livingstone: Philadelphia. p. 151-166.

248. Panush, R.S. (1990). "Does exercise cause arthritis? Long-term

consequences of exercise on the musculoskeletal system." Rheum Dis Clin

North Am 16(4): 827-36.

249. Pattle, R.E. (1950). "The control of foaming. I. The mode of action of

chemical anti-foams." J. Soc. Chem. Ind. 69: 363-368.

250. Pattle, R.E. (1955). "Properties, function and origin of the alveolar lining

layer." Nature 175(4469): 1125-6.

251. Pattle, R.E. (1956). "A test of silicone antifoam treatment of lung oedema in

rabbits." J Pathol Bacteriol 72(1): 203-9.

252. Pattle, R.E. and Thomas, L.C. (1961). "Lipoprotein composition of the film

lining the lung." Nature 189: 844.

253. Pawlak, Z. (2003) Tribochemistry of Lubricationg Oils. Tribology and

Interface Engineering Series, No. 45, ed. B.J. Briscoe: Elsevier. 368.

254. Phillips, M.C. and Riddiford, A.C. (1967) Contact angles and the free

surface energies of solids, in Wetting, Staples Printers Ltd. p. 31-56.

255. Pickard, J.E., Fisher, J., et al. (1998). "Investigation into the effects of

proteins and lipids on the frictional properties of articular cartilage."

Biomaterials 19(19): 1807-1812.

195

256. Prete, P.E., Gurakar-Osborne, A., and Kashyap, M.L. (1993). "Synovial

fluid lipoproteins: review of current concepts and new directions." Semin

Arthritis Rheum 23(2): 79-89.

257. Prete, P.E., Gurakar-Osborne, A., and Kashyap, M.L. (1995). "Synovial

fluid lipids and apolipoproteins: a contemporary perspective." Biorheology

32(1): 1-16.

258. Purbach, B., Hills, B.A., and Wroblewski, B.M. (2002). "Surface-active

phospholipid in total hip arthroplasty." Clinical Orthopaedics and Related

Research 396: 115-118.

259. Rabinowitz, J.L., Gregg, J.R., and Nixon, J.E. (1984). "Lipid composition of

the tissues of human knee joints. II. Synovial fluid in trauma." Clinical

Orthopaedics and Related Research 190: 292-298.

260. Rabinowitz, J.L., Gregg, J.R., et al. (1979). "Lipid Composition of the

Tissues of Human Knee Joints. I. Observations in normal joints (articular

cartilage, meniscus, ligaments, synovial fluid, synovium, intra-articular fat

pad and bone marrow)." Lipids of Normal Knee Joints 143: 260-265.

261. Radin, E., Swann, D., and Weisser, P. (1970). "Separation of a

hyaluronate-free lubricating fraction from synovial fluid." Nature

228(269): 377-8.

262. Radin, E.L. and Paul, I.L. (1971). "Response of joints to impact loading."

Arthritis & Rheumatism 14: 356-362.

263. Radin, E.L., Paul, I.L., and Pollock, D. (1970). "Animal joint behaviour

under excessive loading." Nature 226: 554-555.

264. Radin, E.L., Paul, I.L., et al. (1971). "Lubrication of synovial membrane."

Ann Rheum Dis 30(3): 322-5.

265. Rapport, P.N., Lim, D.J., and Weiss, H.S. (1975). "Surface-active agent in

Eustachian Tube Function." Arch Otolaryngol 101(5): 305-11.

266. Reilly, D.T. and Burstein, A.H. (1974). "Review article. The mechanical

properties of cortical bone." J Bone Joint Surg Am 56(5): 1001-22.

267. Reilly, D.T., Burstein, A.H., and Frankel, V.H. (1974). "The elastic

modulus for bone." J Biomech 7(3): 271-5.

268. Ropes, M.W., Muller, A.F., and Bauer, W. (1960). "The entrance of glucose

and other sugars into joints." Arthritis Rheum 3: 496-514.

269. Ropes, M.W., Robertson, W.B., et al. (1947). "Synovial fluid mucin,." Acta

Med. Scand. 196(Suppl.): 700–714.

270. Ropes, M.W., Rossmeisl, E., and Bauer, W. (1939). "The Relationship

between the Erythrocyte Sedimentation Rate and the Plasma Proteins." J

Clin Invest 18(6): 791-8.

196

271. Rorvik, A.M. and Grondahl, A.M. (1995). "Markers of osteoarthritis: a

review of the literature." Vet Surg 24(3): 255-62.

272. Saikko, V. and Ahlroos, T. (1997). "Phospholipids as boundary lubricants

in wear tests of prosthetic joint materials." Wear 207(1-2): 86-91.

273. Sandy, J.D., Brown, H.L., and Lowther, D.A. (1978). "Degradation of

proteoglycan in articular cartilage." Biochim Biophys Acta 543(4): 536-

44.

274. Sarma, A.V., Powell, G.L., and LaBerge, M. (2001). "Phospholipid

composition of articular cartilage boundary lubricant." Journal of

Orthopaedic Research 19(4): 671-676.

275. Sayles, R.S., Thomas, T.R., et al. (1979). "Measurement of the surface

microgeometry of articular cartilage." J Biomech 12(4): 257-67.

276. Scholes, S.C. and Unsworth, A. (2000). "Comparison of Friction and

Lubrication of Different Hip Prostheses." Proceedings of the Institution of

Mechanical Engineers, Part H: Journal of Engineering in Medicine 214(1):

49-57.

277. Scholes, S.C., Unsworth, A., et al. (2005). "Design aspects of compliant,

soft layer bearings for an experimental hip prosthesis." Proc Inst Mech Eng

[H] 219(2): 79-87.

278. Schreppers, G.J., Sauren, A.A., and Huson, A. (1991). "A model of force

transmission in the tibio-femoral contact incorporating fluid and mixtures."

Proc Inst Mech Eng [H] 205(4): 233-41.

279. Schurz, J. and Ribitsch, V. (1987). "Rheology of Synovial Fluid."

Biorheology 24(4): 385-399.

280. Schwarz, I.M. (1994) The isolation of the lubricating factor in the synovial

joint : implications for the development of an artificial synovial fluid,

University of New England: Armidale.

281. Schwarz, I.M. and Hills, B.A. (1998). "Surface-active phospholipid as the

lubricating component of lubricin." Br J Rheumatol 37(1): 21-6.

282. Scmalzried, T.P. and Callaghan, J.J. (1999). "Wear in total hip and knee

replacements." Journal of Bone and Joint Surgery 81-A(1): 136-155.

283. Scott, D.L. and Walton, K.W. (1984). "The significance of fibronectin in

rheumatoid arthritis." Semin Arthritis Rheum 13(3): 244-54.

284. Serro, A.P., Gispert, M.P., et al. (2006). "Adsorption of albumin on

prosthetic materials: Implication for tribological behavior." J Biomed

Mater Res A 78(3): 581-9.

197

285. Shah, C.O. and Schulman, J.H. (1965). "Binding of metal ions to

monolayers of lecithins, plasmalogen, cardiolipin and dicetyl phosphate." J

Lipid Res 6: 341-349.

286. Sharma, R., ed. Surfactant Adsorption and Solubilization. York, PA, Maple

Press. 401.

287. Shaw, D.J. (1992) Chapter 4, Liquid-gas and liquid-liquid interfaces, in

Introducton to Surface and Colloid Chemistry, Butterworth Hienemann:

Oxford. p. 64-114.

288. Shi, B. (2004) Tribological comparison of materials, University of Alaska

Fairbanks: United States -- Alaska.

289. Shpenkov, G.P. (1995) Friction surface phenomena. Tribology and

Interface Engineering Series, No. 29: Elsevier. 358.

290. Simkin, P.A. (1991). "Physiology of normal and abnormal synovium."

Semin Arthritis Rheum 21: 179-183.

291. Simkin, P.A. (1993) Synovial physiology, in Arthritis and Allied

Conditions, a Textbook of Rheumatology, D.J. McCarty and W.J. Koopman,

Editors, Lea & Febiger: Philadelphia. p. 199-212.

292. Simmons, C.A., Shaker, M.A., and Pilliar, R.A. (2001). "Differences in

osseointegration rate due to implant surface geometry can be explained by

local tissue strains." Journal of Orthopaedic Research 19: 187-194.

293. Skotheim, J.M. and Mahadevan, L. (2004). "Soft lubrication." Phys Rev

Lett 92(24): 245509.

294. Small, D.M., Cohen, A.S., and Schmid, K. (1964). "Lipoproteins of

Synovial Fluid as Studied by Analytical Ultracentrifugation." J Clin Invest

43: 2070-9.

295. Smith, C., Habermann, E., and Hamerman, D. (1979). "A technique for

investigating the antigenicity of cultured rheumatoid synovial cells." J

Rheumatol 6(2): 147-55.

296. Stachowiak, G. and Batchelor, A.W. (2005) Engineering Tribology. 3rd ed.

Tribology and Interface Engineering Series, No. 24: Elsevier.

297. Stachowiak, G.W., ed. (2005) Wear - Materials, Mechanisms and Practice.

Chichester, John Wiley & Sons Ltd. 458.

298. Stachowiak, G.W. and Podsiadlo, P. (1997). "Analysis of wear particle

boundaries found in sheep knee joints during in vitro wear tests without

muscle compensation." Journal of Biomechanics 30(4): 415-419.

299. Stockwell, R.A. (1965). "Lipid in the matrix of ageing articular cartilage."

Nature 207(995): 427-8.

198

300. Sumner, D.R., et al. (1998). "Functional adaption and ingrowth of bone

vary as a function of hip implant stiffness." Journal of Biomechanics 31:

909-917.

301. Swann, A.D. (1978) Macromolecules of synovial fluid, in The Joints and

Synovial Fluid, L. Sokoloff, Editor, Academic Press Inc.: New York. p.

407-435.

302. Swann, A.D., Silver, H.F., et al. (1985). "The molecular structure and the

lubricating activity of lubricin isolated from bovine and human synovial

fluids." Journal of Biochemistry 225: 195-201.

303. Swann, A.D., Sotman, S.L., et al. (1977). "The isolation and partial

characterization of the major glycoprotein (LGP-I) from the articular

lubricating fraction from bovine synovial fluid." Biochem J 161(3): 473–

485.

304. Swann, D. and Mintz, G. (1979). "The isolation and properties of a second

glycoprotein (LGP-II) from the articular lubricating fraction from bovine

synovial fluid." Biochem J 179(3): 465-71.

305. Swann, D.A., Bloch, K.J., et al. (1984). "The lubricating activity of human

synovial fluids." Arthritis Rheum 27(5): 552-6.

306. Swann, D.A., Hendren, R.B., et al. (1981). "The lubricating activity of

synovial fluid glycoproteins." Arthritis Rheum 24(1): 22-30.

307. Swann, D.A. and Radin, E.L. (1972). "The Molecular Basis of Articular

Lubrication. I. Purification and properties of a lubricating fraction from

bovine synovial fluid." J. Biol. Chem. 247(24): 8069-8073.

308. Swann, D.A., Radin, E.L., et al. (1974). "Role of hyaluronic acid in joint

lubrication." Ann Rheum Dis 33(4): 318-26.

309. Swann, D.A., Slayter, H.S., and Silver, F.H. (1981). "The molecular

structure of lubricating glycoprotein-I, the boundary lubricant for articular

cartilage." J. Biol. Chem. 256(11): 5921-5925.

310. Swanson, S.A.V. (1979) Friction, Wear and Lubrication, in Adult Articulat

Cartilage, M.A.R. Freeman, Editor, Pitman Medical: UK. p. 415-460.

311. Szeri, A.Z. (2001) Hydrodynamic and elastohydrodynamic lubrication, in

Modern Tribology Handbook, B. Bhushan, Editor, CRC Press: New York.

p. 383-453.

312. Tandon, P.N., Bong, N.H., and Kushwaha, K. (1994). "A new model for

synovial joint lubrication." International Journal of Bio-Medical Computing

35(2): 125-140.

313. Tanner, R.I. (1966). "An alternative mechanism for the lubrication of

synovial joints." Physics in Medicine and Biology 11: 119.

199

314. Tew, W.P. (1980). "Synovial fluid particle analysis in equine joint disease."

Mod Vet Pract 61(12): 993-7.

315. Tro, N.J. (2003) Chapter 19 Biochemistry, in Introductory Chemistry,

Prentice-Hall Inc.

316. Tsukamoto, Y., Yamamoto, M., et al. (1983). "Boundary lubricating

property of synovial fluid on artificial material and lubrication of artificial

joints." Nippon Seikeigeka Gakkai Zasshi 57(1): 91-9.

317. Uchiyama, S., Amadio, P.C., et al. (1997). "Boundary lubrication between

the tendon and the pulley in the finger." Journal of Bone and Joint Surgery

79A: 213-220.

318. Ueda, S., Kawamura, K., et al. (1985). "Ultrastructural studies on surfaces

lining layer of the lungs. Part IV. Resected human lung." J Jpn Med Soc

Biol Interface 16: 36-60.

319. Ueda, S., Kawamura, K., et al. (1986). "Morphological studies on surface

lining layer of the lungs. Part VI. Surfactant-like substance in other organs

(plueral cavity, vascular lumen and gastric lumen) than lungs." J Jpn Med

Soc Biol Interface 17: 132-156.

320. Unsworth, A. (1975). "Endoprosthetic design." Physiotherapy 61(10): 296-

301.

321. Unsworth, A. (1978). "The effects of lubrication in hip joint prostheses."

Physics in Medicine and Biology 23(2): 253-268.

322. Unsworth, A. (1991). "Tribology of human and artificial joints."

Proceedings of the Institution of Mechanical Engineers. Part H - Journal of


323. Unsworth, A. (1995). "Recent developments in the tribology of artificial

joints." Tribology International 28(7): 485-495.

324. Unsworth, A., Dowson, D., and Wright, V. (1975). "Some new evidence on

human joint lubrication." Ann Rheum Dis 34: 277-285.

325. Virdee, S.S., Wang, F.C., et al. (2003). "Elastohydrodynamic lubrication

analysis of a functionally graded layered bearing surface, with particular

reference to 'cushion form bearings' for artificial knee joints." Proceedings

of the Institution of Mechanical Engineers, Part H: Journal of Engineering

in Medicine 217(3): 191-198.

326. Walker, E.R., Boyd, R.D., et al. (1991). "Morphologic and morphometric

changes in synovial membrane associated with mechanically induced

osteoarthrosis." Arthritis Rheum 34(5): 515-24.

327. Walker, P.S., Dowson, A.D., et al. (1968). ""Boosted Lubrication" in

Synovial Joints by Fluid Entrapment and Enrichment." Ann Rheum Dis 27:

512-520.

200

328. Walker, P.S., Dowson, D., et al. (1969). "Lubrication of human joints." Ann

Rheum Dis 28(2): 194.

329. Walker, P.S., Sikorski, J., et al. (1970). "Features of the synovial fluid film

in human joint lubrication." Nature 225: 956-957.

330. Wang, A., Essner, A., et al. (1998). "Lubrication and wear of ultra-high

molecular weight polyethylene in total joint replacements." Tribology

International 31(1-3): 17-33.

331. Watkins, J.C. (1968). "The surface properties of pure phospholipids in

relation to those of lung extracts." Biochim Biophys Acta 152(2): 293-306.

332. Weinberger, A. and Simkin, P.A. (1989). "Plasma proteins in synovial

fluids of normal human joints." Semin Arthritis Rheum 19(1): 66-76.

333. Widmer, M.R. (2002) Modified molecular friction in artificial hip joints,

Eidgenoessische Technische Hochschule Zuerich (Switzerland):

Switzerland.

334. Wildner, M. and Sangha, O. (2000) Epidemiological and economic aspects

of osteoarthritis, in Osteoarthritis: Fundamentals and Strategies for Joint-

Preserving Treatment, J. Grifka and D.J. Ogilvie-Harris, Editors, Springer-

Verlag: Berlin. p. 1-8.

335. Wilkins, J.F. (1968). "Proteolytic destruction of synovial boundary

lubrication." Nature 219: 1050-1051.

336. Williams III, P.F., Gilbert, J.A., et al. (1997). "Evaluation of the Frictional

Properties of an Elastomer with Enhanced Lipid-Adsorbing Ability."

Proceedings of the Institution of Mechanical Engineers, Part H: Journal of


337. Williams III, P.F., Powell, G.L., and LaBerge, M. (1993). "Sliding friction

analysis of phosphatidylcholine as a boundary lubricant for articular

cartilage." Proc Inst Mech Eng [H] 207(1): 59-66.

338. Williams, J. (2005) Engineering Tribology: Cambridge University Press.

488.

339. Williams, P.F. (1998) General Concepts of Biocompatibility, in Handbook

of Biomaterial Properties, J. Black and G.R. Hastings, Editors, Chapman

and Hall: London. p. 481-489.

340. Williams, P.F., 3rd, Powell, G.L., et al. (1995). "Fabrication and

characterization of dipalmitoylphosphatidylcholine-attracting elastomeric

material for joint replacements." Biomaterials 16(15): 1169-74.

341. Wise, C.M., White, R.E., and Agudelo, C.A. (1987). "Synovial fluid lipid

abnormalities in various disease states: review and classification." Semin

Arthritis Rheum 16(3): 222-30.

201

342. Wobig, M., Dickhut, A., et al. (1998). "Viscosupplementation with hylan G-

F 20: a 26-week controlled trial of efficacy and safety in the osteoarthritic

knee." Clin Ther 20(3): 410-23.

343. Wright, V. and Dowson, D. (1976). "Lubrication and cartilage." Journal of

Anatomy 121: 107-118.

344. Wyn-Jones, G. (1986). "In search of the causes and pathogenesis of

lameness." Equine Vet J 18(3): 163-4.

345. Yehia, S.R. and Duncan, H. (1975). "Synovial fluid analysis." Clin Orthop

Relat Res (107): 11-24.

346. Yielding, K.L., Tomkins, G.M., and Bunim, J.J. (1957). "Synthesis of

hyaluronic acid by human synovial tissue slices." Science 125(3261): 1300.