Measurements of muscle morphology and composition with

ultrasound and MRI. Adam Shortland PhD

Consultant Clinical Scientist Guy’s & St Thomas’ NHS Foundation Trust

King’s Healthcare Partners Adam.shortland@gstt.nhs.uk

Outline

• Gross muscle morphology and muscle function. • The physics of ultrasound.

– B-mode, Doppler, Elastography.

• The physics of MRI. – Anatomical, Diffusion weighted, Dixon (fat imaging).

• Measurements of muscle morphology in typically developing individuals and individuals with CP (cross-sectional studies).

• Measurements of muscle composition in typically-developing individuals and individuals with CP.

• Dynamic measurements with ultrasound – insights into the passive and active characteristics of muscle and tendon.

Muscle design – series and parallel.

T

l

T

l T

l

l

l

T T

l

T

The sarcomere

FORCE

LENGTH

3.5 m

The sarcomere

FORCE

LENGTH

The sarcomere

FORCE

LENGTH

The sarcomere

FORCE

LENGTH

The sarcomere

FORCE

LENGTH

2.4 m

The sarcomere

FORCE

LENGTH

The sarcomere

FORCE

LENGTH

1.5 m

The sarcomere

FORCE

LENGTH

Gross morphology = sarcomere arrangement

Forc

e

Length

Forc

e

Velocity sarcomeres

sarcomeresserial

sarcomeresserial

sarcomeresparallel

NPower

NRange

Nv

NF

_

_

_

A B

Sarcomeres act at an angle

θ

Internal

Tendon

Physiological Cross-Sectional Area

In long muscles with short fibres, there is no anatomical plane that represents the number of sarcomeres in parallel! i.e. one that crosses perpendicular to the line of action to the fibres

.

fl

VPCSA

cos

Physiological Cross Sectional Area

Pre

dic

ted

Fo

rce

Actual Force

Powell et al (1984) JAP

A Tribute

PCSAs of muscles in the lower limb

0

10

20

30

40

50

60

70

SO

L

MG VL

RF

SM ST

TA

ED

L

EH

L

Muscle

PC

SA

(cm

2)

0

2

4

6

8

10

12

14

16

Fib

re l

en

gth

(cm

)

PCSA

Fibre Length

How do fibres works together to produce muscular forces?

Neurological coupling

Low Threshold

High Threshold

Mechanical Coupling

• ECM forms continuous mechanical support around muscle fibres.

•Much stiffer than the muscle fibres with which it is connected. •Distribution of tensile load across the muscle •Regulation of sarcomere length.

•ECM (peryimysium) is continuous with internal and external tendons.

Summary of gross architecture, morphology and structure

• The force-length and force-velocity properties of muscles are reflected in their muscle architecture.

• The regulation of muscle mechanical performance is dependent on motor unit size and speed.

• The transmission of force is dependent on the integrity of the extra-cellular matrix.

Why image muscle?

• We can measure gross muscle morphology and architecture.

• We can measure something of the mechanical properties of the muscles.

• We can measure operation of a muscle during a functional task.

How does (B-mode) ultrasound work?

Acoustic energy incident on the crystal cause an electrical voltage across it.

Piezo-electric crystals are electrically excited and produce a packet of high (2-13 MHz) frequency sound.

The wavepackets are partially reflected at surfaces within the tissue.

FAT Myo BONE

Reflections from deeper tissues take longer to reach the crystal

Ultrasound propagation in tissue

• Attenuation – Frequency dependent (A=A1M.f)

– Higher frequencies have lower penetration.

• Reflection – Strength of reflected wave depends on differences in

impedance between neighbouring tissues.

• Speed c – Air 300 m/s

– Muscle 1500m/s

– Bone 4000m/s

How does 2D ultrasound work?

Pulses from successive neighbouring crystals form an image.

There is an upper physical limit for the frequency of scans.

PRTNSFPRTNSRT

c

DPRT

.

1

2

D

Ultrasound Live!

3D ultrasound imaging

How Magnetic Resonance Imaging works

Picture to Proton

NORTH

SOUTH

NORTH

SOUTH

NORTH

SOUTH

NORTH

SOUTH

NORTH

SOUTH

Summary of Imaging Techniques

• Ultrasound

– Ultrasound waves are reflected at boundaries of differing acoustic impedance.

– Fat, blood, muscle, connective tissue present different acoustic impedances.

– Spatial resolution and imaging depth are affected by transmitted ultrasound frequency.

– Temporal resolution is affected by depth and the speed of ultrasound in tissue.

Summary of Imaging Techniques

• MRI – Hydrogen nuclei spin on their axis. – When magnetised they produce a lateral and

longitudinal oscillating magnetic moment. – Application of a radiofrequency pulse changes the net

longitudinal and lateral magnetisations. – Pulse sequences emphasise the relaxation of the

lateral or longitudinal components. – In different biological materials hydrogen nuclei have – Magnetic gradients allow the localisation according to

the frequency of precession.

Application I – measurement of fascicle length (ultrasound)

No

rmal

ise

d f

asci

cle

len

gth

Application II – measurement of muscle volume (3DUS/MRI)

3D ultrasound study – 6-22 years 26TD, 26CP

10 TD (darker), 10CP (lighter) 3DUS (solid), MRI (striped

Muscle growth and body growth

y = 1.802x - 11.36R² = 0.76

y = 1.377x - 13.74R² = 0.550

0

50

100

150

200

250

0 20 40 60 80 100 120

y = 1.610x - 16.17R² = 0.828

y = 0.738x + 1.147R² = 0.292

0

20

40

60

80

100

120

140

160

180

200

0 20 40 60 80 100 120

y = 6.758x - 119.1R² = 0.866

y = 3.081x - 4.244R² = 0.399

0

100

200

300

400

500

600

700

800

0 20 40 60 80 100 120

y = 2.462x - 25.38R² = 0.811

y = 1.474x - 10.93R² = 0.340

0

50

100

150

200

250

300

0 20 40 60 80 100 120

Application III – measurement of muscle composition

Application IV –dynamic performance of muscle

Fascicles maintain near-isometric length in single support

Tendon stretches during single support and recoils during push-off

Passive structures (tendon) perform most of the positive mechanical work which reduces the metabolic cost of muscle contractions

Ten

do

n

• The following subjects were recruited:

– Eight typically developing children (mean age, 10 ± 2 years)

– Eight independently ambulant children with spastic CP with an equinus gait pattern (mean age, 9 ± 2 years)

• TD children: normal heel-toe and voluntary toe walking

• Children with spastic CP: normal toe-walking gait

Muscle tendon interaction

• MTU length was modelled using knee and ankle joint kinematics (Eames et al, 1997)

• Ultrasound probe (with marker cluster) is placed over the distal aspect of the MG (MTJ)

• Tendon length estimated as distance between MTJ and the heel marker (insertion point of tendon in the calcaneus)

• Muscle belly length = MTU length – Tendon Length

50 100 150 200 250 300 350

50

100

150

200

250

Knee Ankle

Skin

Surface Belly MTJ

Methods

0 20 40 60 80

-5

-3

-1

1

3

% Gait Cycle

% C

ha

ng

e in

Le

ng

th

Muscle Belly Length Changes

AdultNormalWalking

TD ChildrenNormalWalking

CP Children

SWING

0 20 40 60 80

-5

-3

-1

1

3

% Gait Cycle

% C

hange in L

ength

Muscle Belly Length Changes

AdultNormalWalking

TD ChildrenNormalWalking

CP Children

SWING

0 20 40 60 80 100

-6

-4

-2

0

2

% Gait Cycle

% C

hange in L

ength

Muscle Belly Length Changes

STANCE SWING

Single Support

Results

0 20 40 60 80

-5

-3

-1

1

3

% Gait Cycle

% C

hange in L

ength

Muscle Belly Length Changes

AdultNormalWalking

TD ChildrenNormalWalking

CP Children

SWING

0 20 40 60 80

-5

-3

-1

1

3

% Gait Cycle

% C

ha

ng

e in

Le

ng

th

Muscle Belly Length Changes

AdultNormalWalking

TD ChildrenNormalWalking

CP Children

SWING

0 20 40 60 80

-5

-3

-1

1

3

% Gait Cycle

% C

hange in L

ength

Muscle Belly Length Changes

AdultNormalWalking

TD ChildrenNormalWalking

CP Children

SWING

0 20 40 60 80 100

-6

-4

-2

0

2

% Gait Cycle

% C

hange in L

ength

Muscle Belly Length Changes

STANCE SWING

Single Support

Results

Is toe walking the cause of eccentric muscle

contractions in children with spastic CP?

0 10 20 30 40 50 60 70 80 90 100-7

-6

-5

-4

-3

-2

-1

0

1

2

3

% Gait Cycle

% C

ha

ng

e in

Le

ng

th

TD Children Muscle Belly Length Changes

TD Child Heel-Toe

TD Child Toe Walking

STANCE SWING

0 20 40 60 80 100-7

-6

-5

-4

-3

-2

-1

0

1

2

3

% Gait Cycle

% C

hange in

Length

TD Children Muscle Belly Length Changes

STANCE SWING

Single

Support

Heel-toe and toe walking

Summary

• Muscle weakness is a feature of spastic CP and other upper motor neurone conditions.

• A part of that weakness is due to structural changes in the muscles

• Muscles and tendons have a beautiful interaction in walking but in children with CP this interaction is altered an muscle bellies may be exposed to eccentric lengthening.

Pros & Cons of Imaging

• Pros

– Non-invasive; quantitative; repeatable, representative; unambiguous, technically achievable in the clinical environment.

• Cons

– Limited resolution, limited functional information, ambiguous(!).

Muscle Imaging Futures

• Routine implementation

• Portable 3D systems

• Elastography

Key references 1. Lieber RL, Fridén J. Functional and clinical significance of skeletal muscle architecture. Muscle & nerve.

2000;23:1647–1666.

2. Ward SR, Eng CM, Smallwood LH, Lieber RL. Are current measurements of lower extremity muscle architecture accurate? Clinical Orthopaedics and Related Research. 2009;467:1074–1082.

3. Fry NR, Gough M, Shortland a P. Three-dimensional realisation of muscle morphology and architecture using ultrasound. Gait & posture. 2004;20(2):177–82. Available at: http://www.ncbi.nlm.nih.gov/pubmed/15336288. Accessed September 9, 2010.

4. Shortland AP, Harris C a, Gough M, Robinson RO. Architecture of the medial gastrocnemius in children with spastic diplegia. Developmental medicine and child neurology. 2002;44(3):158–63. Available at: http://www.ncbi.nlm.nih.gov/pubmed/12005316.

5. Mohagheghi a a, Khan T, Meadows TH, Giannikas K, Baltzopoulos V, Maganaris CN. In vivo gastrocnemius muscle fascicle length in children with and without diplegic cerebral palsy. Developmental medicine and child neurology. 2008;50(1):44–50. Available at: http://www.ncbi.nlm.nih.gov/pubmed/18173630.

6. Barber L, Hastings-Ison T, Baker R, Barrett R, Lichtwark G. Medial gastrocnemius muscle volume and fascicle length in children aged 2 to 5 years with cerebral palsy. Developmental medicine and child neurology. 2011;53(6):543–8. Available at: http://www.ncbi.nlm.nih.gov/pubmed/21506995. Accessed March 20, 2012.

7. Noble JJ, Fry NR, Lewis AP, Keevil SF, Gough M, Shortland AP. Lower limb muscle volumes in bilateral spastic cerebral palsy. Brain & development. 2014;36:294–300.

8. Barber L, Barrett R, Lichtwark G. Passive muscle mechanical properties of the medial gastrocnemius in young adults with spastic cerebral palsy. Journal of Biomechanics. 2011;44:2496–2500.

9. Noble JJ, Charles-Edwards GD, Keevil SF, Lewis AP, Gough M, Shortland AP. Intramuscular fat in ambulant young adults with bilateral spastic cerebral palsy. BMC musculoskeletal disorders. 2014;15:236.