Exercise in SCI_Sports Med 2004_Review

Sports Med 2004; 34 (11): 727-751REVIEW ARTICLE 0112-1642/04/0011-0727/$31.00/0 2004 Adis Data Information BV. All rights reserved.

Exercise Recommendations forIndividuals with Spinal Cord InjuryPatrick L. Jacobs1,2 and Mark S. Nash1,3

1 Department of Neurological Surgery, University of Miami School of Medicine, Miami,Florida, USA

2 Center of Excellence for Restoration of Function in Chronic SCI, Miami VA Medical Center,Miami, Florida, USA

3 Department of Orthopedics & Rehabilitation, University of Miami School of Medicine, Miami,Florida, USA

ContentsAbstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7281. Neurological Classification of Persons with Spinal Cord Injury (SCI) . . . . . . . . . . . . . . . . . . . . . . . . . . . . 729

1.1 Upper and Lower Motor Neuron Lesions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7301.2 Defining Spinal Cord Lesions: Plegias . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7311.3 Neurological, Sensory and Motor Levels . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7311.4 Complete and Incomplete Spinal Cord Lesions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7311.5 SCI Syndromes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 732

1.5.1 Anterior Cord Syndrome . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7321.5.2 Central Cord Syndrome . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7321.5.3 Brown-Sequard Syndrome . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7331.5.4 Conus Medullaris and Cauda Equina Syndrome. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 733

2. Medical and Health Consequences of SCI . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7332.1 Physical Deconditioning . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7332.2 Musculoskeletal Decline . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7342.3 Cardiovascular Disease, Dyslipidaemia and Comorbidities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7342.4 Cardiac Structure and Function . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7352.5 Vascular Structure and Function . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7352.6 Autonomic Dysregulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 736

3. Volitional Upper Extremity Exercise in Persons with SCI . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7363.1 Acute Physiological Responses to Exercise Stress . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7363.2 Cardiorespiratory Testing . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7373.3 Endurance Training . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7383.4 Resistance Training for Persons with SCI . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 739

4. Electrically Stimulated Exercise in Persons with SCI . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7404.1 Basis of Electrically Stimulated Movement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7404.2 Leg Cycling Exercise . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7404.3 Bipedal Ambulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 741

5. Risks of Exercise When Performed by Persons with SCI . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7425.1 Autonomic Dysreflexia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7425.2 Musculoskeletal Injury . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7435.3 Hypotension . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7435.4 Thermal Dysregulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 743

6. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 743

728 Jacobs & Nash

Persons with spinal cord injury (SCI) exhibit deficits in volitional motorAbstractcontrol and sensation that limit not only the performance of daily tasks but also theoverall activity level of these persons. This population has been characterised asextremely sedentary with an increased incidence of secondary complicationsincluding diabetes mellitus, hypertension and atherogenic lipid profiles. As thedaily lifestyle of the average person with SCI is without adequate stress forconditioning purposes, structured exercise activities must be added to the regularschedule if the individual is to reduce the likelihood of secondary complicationsand/or to enhance their physical capacity. The acute exercise responses and thecapacity for exercise conditioning are directly related to the level and complete-ness of the spinal lesion. Appropriate exercise testing and training of persons withSCI should be based on the individuals exercise capacity as determined byaccurate assessment of the spinal lesion. The standard means of classification ofSCI is by application of the International Standards for Classification of SpinalCord Injury, written by the Neurological Standards Committee of the AmericanSpinal Injury Association. Individuals with complete spinal injuries at or abovethe fourth thoracic level generally exhibit dramatically diminished cardiac accel-eration with maximal heart rates less than 130 beats/min. The work capacity ofthese persons will be limited by reductions in cardiac output and circulation to theexercising musculature.

Persons with complete spinal lesions below the T10 level will generally displayinjuries to the lower motor neurons within the lower extremities and, therefore,will not retain the capacity for neuromuscular activation by means of electricalstimulation. Persons with paraplegia also exhibit reduced exercise capacity andincreased heart rate responses (compared with the non-disabled), which have beenassociated with circulatory limitations within the paralysed tissues. The recom-mendations for endurance and strength training in persons with SCI do not varydramatically from the advice offered to the general population. Systems offunctional electrical stimulation activate muscular contractions within theparalysed muscles of some persons with SCI. Coordinated patterns of stimulationallows purposeful exercise movements including recumbent cycling, rowing andupright ambulation. Exercise activity in persons with SCI is not without risks,with increased risks related to systemic dysfunction following the spinal injury.These individuals may exhibit an autonomic dysreflexia, significantly reducedbone density below the spinal lesion, joint contractures and/or thermal dysregula-tion. Persons with SCI can benefit greatly by participation in exercise activities,but those benefits can be enhanced and the relative risks may be reduced withaccurate classification of the spinal injury.

The human spinal cord is a complex association or disease of spinal tracts results in varying typesand degrees of dysfunction depending upon the spe-of upper and lower motor neurons that functions as acific neural structures affected.bidirectional conduit between the brain and its mo-

tor, sensory and autonomic targets. It also serves as a The interruption of spinal cord functions by trau-site for reflex integration between body sensors and ma affects 10 000 Americans annually, with an esti-their motor and autonomic effectors. Because spinal mated 179 000 persons having survived their initialcord functions differ by level and structure, injury to injury.[1-4] Thereafter, these individuals experience

2004 Adis Data Information BV. All rights reserved. Sports Med 2004; 34 (11)

Exercise After Spinal Cord Injury 729

unique physical, social and psychological changes cise conditioning, contemporary methods of injuryclassification, exercise options and established ben-throughout their lives, including diminished abilityefits of training, and risks imposed by inappropriateto perform and benefit from exercise condition-exercise recommendations for those with SCI.ing.[5,6] The latter limitation is cause for concern as:

(i) individuals with spinal cord injury (SCI) areusually young and physically active at the time of 1. Neurological Classification of Personsinjury;[3] (ii) profound physical deconditioning is with Spinal Cord Injury (SCI)common after injury;[7-9] and (iii) physical decondi-

If trauma to, or disease of, the spinal cord alwaystioning contributes to multisystem medical compli-resulted in its anatomical or physiological transec-cations,[10-19] activity limitations[7,20,21] and acceler-tion, classification of spinal cord dysfunctions fol-ated aging.[6,7,22-26]lowing SCI would be relatively easy. However, theMany reviews and chapters published over thespinal cord is rarely severed unless penetrated by apast decades have addressed the need for persons bullet or severed by its bony covering during very

with SCI to adopt habitual exercise as part of a high velocity impact. More often the cord remainshealthy lifestyle.[5,6,9,17,18,27-33] Exercise options con-anatomically intact but suffers contusion, infarction

tained in these reports have focused on use of mus-or mechanical deformation that interrupts its local or

cle activities still under voluntary nervous systemrelay circuitry. It also can undergo secondary dam-

control, as well as sequenced contractions of mus-age from inflammatory autodestruction, which ex-

cles stimulated by electrical current. Outcomes of plains the routine administration of high-dose corti-studies cited in these monographs provide credible

costeroids within hours of an SCI.[37] Notwithstand-evidence that exercise performed by persons with ing the cause of spinal damage, more than half of theSCI enhances physical conditioning and reduces

survivors will experience varying degrees of motor,multisystem disease susceptibility. They further

sensory or autonomic sparing at different spinal cordsuggest that habitual exercise might reduce fatigue, levels,[2,38,39] making classification of persons withpain, weakness, joint deterioration and incipient SCI a challenging, yet important, science.[4]neurological deficits that appear as persons age with To assist with accurate and consistent classifica-disability. As these deficits challenge the ability of tion, uniform standards have been developed thatthose with SCI to perform essential daily activities

allow persons with SCI to be systematically ex-first mastered after injury, their prevention will like-

amined and classified, and to document changes inly foster fullest health and life satisfaction for those

sensorimotor function that accompany the passageaging with a disability.

of time, clinical treatments or research interven-Use of exercise as a healthy activity and lifestyle tions. The benchmark system used to classify per-

elective for those with SCI might appear fairly sons with SCI is the International Standards forstraightforward. To the contrary, exercise options Classification of Spinal Cord Injury (revised 2000),available to those with SCI are more limited than which is written by the Neurological Standardsthose without disability,[33] their acute exercise and Committee of the American Spinal Injury Associa-training responses less robust than those of persons tion (ASIA), and endorsed as the recommendedwithout SCI,[28,34,35] and the risks of impudent activi- international standards by the International Spinalty greater and longer lasting.[33,36] This makes an Cord Society (ISCoS; formerly the Internationalunderstanding of neurological classification, exer- Medical Society for Paraplegia, and hereinafter thecise opportunities and risks of activity important if ASIA Guidelines) [figure 1].[40] While a completethose with SCI are to benefit and not be harmed description of spinal column and spinal cord anato-from exercise conditioning. This paper will review my is beyond the scope of this review, the accuratecommon medical problems experienced by persons description of an injury to a given spinal cord seg-with SCI that lend themselves to benefit from exer- ment involves designation of a spinal column region


730 Jacobs & Nash

C2

C3

C4

S4-5

S 3

L2

L2

L3

L3

L4

L4

S1 S1

S2 S2

L5 L5

C2C3

C4

T3T4T5T6T7T8T9T10T11T12

L1 L1

L2 L2

L3 L3

L4 L4

L5 L5

S1 S1

Key sensory points

Dorsum Dorsum

Palm Palm

C5 C5T2 T2

C6 C6T1 T1

C8 C6C7

C8C7

C6

C2C3C4C5C6C7C8T1T2T3T4T5T6T7T8T9T10T11T12L1L2L3L4L5S1S2S3S4-5

C2C3C4C5C6C7C8T1T2T3T4T5T6T7T8T9T10T11T12L1L2L3L4L5S1S2S3S4-5

Elbow flexorsWrist extensorsElbow extensorsFinger flexors (distal phalanx of middle finger)Finger abductors (little finger)

Hip flexorsKnee extensorsAnkle dorsiflexorsLong toe extensorsAnkle plantar flexors

R L R L R L

0 = total paralysis1 = palpable or visible contraction2 = active movement, gravity eliminated3 = active movement, against gravity4 = active movement, against some resistance5 = active movement, against full resistanceNT = not testable

TOTALS(maximum) (50) (50) (100)

0 = absent1 = impaired2 = normalNT = not testable

Motorkey muscles

Lighttouch

Pinprick

Sensorykey sensory points

TOTALS(maximum) (56) (56) (56) (56)

+ = Motor score

Voluntary anal contraction (yes/no)

+ = Light touch score

+ = Pin prick score

(max: 112)

(max: 112)Any anal sensation (yes/no)

Neurological levelThe most caudal segment

with normal function

R LComplete or incomplete?

Incomplete = any sensory or motor funtion in S4-S5

ASIA impairment scale

Zone of partialpreservation

Caudal extent of partiallyinnervated segments

R LSensory

A = Complete: No motor or sensoryfunction is preserved in thesacral segments S4-S5

B = Incomplete: Sensory but notmotor function is preservedbelow the neurological level andincludes the sacral segments S4-S5

C = Incomplete: Motor function ispreserved below the neurologicallevel, and more than half of keymuscles below the neurological levelhave a muscle grade less than 3

D = Incomplete: Motor function ispreserved below the neurologicallevel, and at least half of keymuscles below the neurological levelhave a muscle grade of 3 or more

E = Normal: motor and sensoryfunction are normal

Central cord

Brown-Sequard

Anterior cord

Conus medullaris

Cauda equina

Clinical syndromesASIA impairment scale

Motor

Sensory

Motor

Fig. 1. American Spinal Injury Association (ASIA) classification of spinal cord injury (reproduced from the American Spinal Injury Associa-tion,[41] with permission).

(e.g. cervical, thoracic, lumber or sacral), a spinal trauma or disease. The long tracts of the spinal cordnerve within that region, and the degree to which the are upper motor neurons. By convention, the lowerinjury is neurologically complete or incomplete. motor neuron system begins in the anterior horn ofShould the injury result in a specific spinal cord the grey matter and exits the intervertebral foramensyndrome this should also be designated. to join the returning sensory axons as a mixed nerve.

The motor portion of this mixed nerve then travels toits target muscle(s). The returning sensory nerve1.1 Upper and Lower Motor Neuron Lesionsfibres travel in this mixed nerve but, upon entry tothe foramen, form a dorsal root that penetrates theIt is clinically important for those working withcord in the dorsal root entry zone and synapses withsubjects having SCI to differentiate between upperthe anterior horn cells of the anterior grey matter.and lower motor neuron injuries. The spinal cord isThis completes the motor-sensory reflex arc. Le-organised in such a way that either upper or lower

motor neuron function, or both, can be disrupted by sions of upper motor neurons result in decentralisa-



tion of the nervous system, spastic paralysis and the level of injury, the trunk, legs and pelvic organsexaggerated sensorimotor reflexes below the injury. may be involved. The term is used when referring toThis means that motor, sensory and autonomic re- cauda equina and conus medullaris injuries, but notflex activities are preserved, but no longer under to lumbosacral plexus lesions or injury to peripheralcommand of the brain. The contrasting injury is a nerves outside the neural canal.[42,43]lower motor neuron lesion, which often accompa-

1.3 Neurological, Sensory and Motor Levelsnies SCI at the T10 level or lower and almost alwaysoccurs at, or caudal to, T12. Persons with these Neurological level refers to the most caudal seg-lesions lose central nervous system control of sen-

ment of the spinal cord with normal sensory andsorimotor functions, as well as sensorimotor reflex

motor function on both sides of the body. Becauseactivity, which causes flaccid paralysis and areflexia

the results of sensorimotor testing often differ by(denervation). This explains the greater loss ofside, up to four different segments may be identifiedlower extremity muscle mass in individuals with in determining the neurological level, i.e. R-sensory,flaccid rather than spastic paralysis. Otherwise, inju- L-sensory, R-motor and L-motor. In such cases it is

ry to the cord at any site resulting in damage to thestrongly recommended that each of these segments

reflex arc can leave a denervated (areflexic) segment be separately recorded and that a single level notamong neighbouring segments that remain spastic. be used, as this can be misleading. When the termIt is important to note that while spastic muscles

sensory level is used, it refers to the most caudalare capable of contracting upon stimulation with

segment of the spinal cord with normal sensorytranscutaneous electrical alternating currents, gener- function on both sides of the body; the motor levelally, flaccid muscles are not. This provides a means is similarly defined with respect to motor function.of discriminating upper from lower motor neuron These levels are determined by neurological ex-lesions and also determining subject or patient can-

amination of: (i) a key sensory point within each ofdidacy for use of electrical prostheses that provide 28 dermatomes on the right and 28 dermatomes onexercise or ambulation in persons with SCI. the left side of the body;[42] and (ii) a key muscle

within each of ten myotomes on the right and ten1.2 Defining Spinal Cord Lesions: Plegias myotomes on the left side of the body. Assessment

of sensory and motor level is key in those withIndividuals with SCI are described as having paraplegia having injuries from T1 through T8,lesions affecting either sensorimotor function of allwhereas motor function is the determining factor inlimbs or the upper extremities alone. The former areclassification of tetraplegia.

said to have tetraplegia (preferred to quadriplegia),which is defined as: A term referring to impairment 1.4 Complete and Incomplete Spinalor loss of motor and/or sensory function in the Cord Lesionscervical segments of the spinal cord due to damageof neural elements within the spinal canal. Te- Confusion and imprecise language surround thetraplegia results in impairment of function in the definitions of neurological completeness and incom-arms as well as in the trunk, legs and pelvic organs. pleteness. Historically, the Functional ClassificationIt does not include brachial plexus lesions or injury scale of Frankel et al.[44] was used to assign a gradeto peripheral nerves outside the neural canal.[42,43] of SCI from A to E. These grades were assigned onParaplegia is defined as: A term referring to im- the basis of sensorimotor sparing below the level ofpairment or loss of motor and/or sensory function in SCI. In contrast, the ASIA scale uses sacral spar-the thoracic, lumbar or sacral (but not cervical) ing as the criterion for determining neurologicalsegments of the spinal cord, secondary to damage of completeness.[39,42,45] This requires a test of motorneural elements within the spinal canal. With para- function examining the presence of voluntary con-plegia, arm functioning is spared, but, depending on traction of the external anal sphincter upon digital


732 Jacobs & Nash

examination. The ASIA definitions of complete and planations for resolution of spinal shock and re-incomplete lesions are: covery of sensorimotor functions, the designation of

neurological completeness within the first year of Complete injury: a term describing absence of

injury leaves open the possibility for erroneous clas-sensory and motor function in the lowest sacralsification of a subject thereafter. This explains whysegment.[42]many investigators use the first anniversary of injury

Incomplete injury: a term describing partial as both a benchmark for neurological stability and apreservation of sensory and/or motor functionscriterion for enrolment of subjects with SCI in re-below the neurological level and including thesearch studies, especially when sensorimotor func-lowest sacral segment. Sacral sensation includestion is under study. Clearly, however, the use of the

sensation at the anal mucocutaneous junction asterm complete written on an initial trauma exami-

well as deep anal sensation.[42]nation might ultimately have little bearing on wheth-

Both ASIA and Frankel methods are useful for er recovery of reflexes or sensorimotor functiondescribing completeness of injuries, as an individual might result. Thus, examination and classification atwith infralesional sensory sparing (i.e. incomplete the beginning of exercise testing and training issensory loss; Frankel Grade B) can still be neuro- needed.logically complete when using the ASIA guidelines.Also, the ASIA C classification is so broad as to 1.5 SCI Syndromessometimes limit useful classification of motor andfunctional abilities of patients with SCI that may be As the various spinal columns transmit differentbetter understood when using Frankel grades. types of information, and because most persons

surviving SCI do not experience complete severanceAccurate descriptions of complete and incom-of their cords, many different patterns of sparedplete lesions are often confounded by recovery ofsensorimotor function are possible. The syndromessensorimotor function within weeks or months afterthat ensue are usually described when defining theinjury, which is not uncommon for some individualslevels and completeness of injury. The major syn-initially presenting without preserved reflex or sen-dromes, their definitions and causations are listed insorimotor functions.[46] This recovery, however, willthe following sections.more likely occur in individuals with very low ve-

locity injuries in which cord bleeding or anatomic 1.5.1 Anterior Cord Syndromedisruption of neural elements are limited. Several An anterior cord syndrome is a lesion that pro-mechanisms have been postulated to explain return duces variable loss of motor function and of sensi-of function after SCI. The first involves a belief that tivity to pain and temperature, while preservinga spinal shock occurs immediately upon SCI in proprioception.[42] An anterior cord syndrome re-some individuals a state of areflexia thought to sults primarily in a profound motor loss below theresult from hyperpolarisation of cord neurons ac- level of injury. Destruction of the anterior portionscompanying injury-related loss of descending facili- of the white and grey matter of the spinal cordtation.[47] Thereafter, those with incomplete lesions affects the corticospinal motor tracts and, to a lesseroften recover reflexes in a caudal to rostral se- extent, sensory tracts that mediate light touch andquence, although the extent of reflex recovery has pressure.questionable value in predicting eventual patterns or

1.5.2 Central Cord Syndromeextent of motor recovery.[47] Otherwise, post-synap-tic receptor up-regulation and synaptic growth have A central cord syndrome is a lesion occurringbeen postulated as explanations for neuronal recov- almost exclusively in the cervical region, that pro-ery following SCI,[48,49] although the precise mecha- duces sacral sensory sparing and greater weaknessnisms promoting these changes remain incompletely in the upper limbs than in the lower limbs.[42] Aunderstood. Notwithstanding the controversial ex- person with a central cord syndrome often presents



with greater motor impairment of the upper than bosacral nerve roots within the neural canal result-lower extremities if the damage or disease is prima- ing in areflexic bladder, bowel and lower limbs.[42]rily limited to the central grey and white spinal cord

2. Medical and Health Consequencesmatter. Because upper extremity motor function isof SCIprimarily activated by the medial corticospinal

tracts, sensorimotor functions of the lower extremi- Persons with SCI face unique health challengesties are usually affected to a lessor degree. Central throughout their lives, and their injuries dissociatecord injury is common among individuals having the normally well integrated homoeostatic responsescongenitally narrow spinal canals and in those, espe-

of body systems known to accompany physical ac-cially aging persons, whose osteoarthritic pathology tivity. Nervous system damage disrupts to varyingresults in spinal canal stenosis. degrees the necessary signal integration among mo-

tor, sensory and autonomic targets, and thus has a1.5.3 Brown-Sequard Syndrome profound effect on fitness, exercise capacities andA Brown-Sequard syndrome is a lesion that health. Depending on the level and type of cord

produces relatively greater ipsilateral proprioceptive lesion, persons with SCI are among the most physi-and motor loss and contralateral loss of sensitivity to

cally deconditioned of all humans.[7,50] Not surpris-pain and temperature.[42] The Brown-Sequard syn- ingly, young persons with chronic SCI experiencedrome results from an anterior-posterior hemisec-

accelerated pathological states and conditions nor-tion of the spinal cord often accompanying a pene-

mally associated with physical deconditioning andtrating wound that severs the neural elements. When premature aging, including: dyslipidaemias andthe elements of only one lateral portion of the spinal heart disease;[23,24,51,52] arterial circulatory insuffi-cord are destroyed, the injury results in an unusual

ciency[53-57] and clotting disorders;[58,59] bone andpattern of sensorimotor function with a loss of in- joint diseases;[60-62] and pain of musculoskeletal andfralesional motor function, proprioception, fine

neuropathic origins.[63-68]touch and vibration discrimination on the same side Notwithstanding their physical limitations, manyof injury, but loss of pain, temperature, crude touch persons with SCI can still undergo exercise recondi-and deep pressure on the opposite side of injury. The tioning. Those who retain upper extremity functionsyndrome is explained by decussation of motor

can participate in a wide variety of exercise activi-tracts in the brain stem before they descend in the ties and sports,[6,69] and ambulate with the assistancecord. In contrast, ascending sensory tracts of the

of orthoses and computer-controlled electricalanterolateral systems cross to the opposite side at (or

neuroprostheses.[70-76] Individuals with upper motornear) the level in which the dorsal roots enter the

neuron lesions can pedal cycle ergometers by sur-cord. This explains why same side motor deficits face electrical stimulation of selected lower extremi-are common in patients with Brown-Sequard syn- ty muscle groups under computer control.[30,31,33]drome, but sensory preservation is greater on the Many body organs and tissues acutely respond tocontralateral side of injury.

exercise despite their decentralised or denervatedstates, and because many survivors of SCI experi-

1.5.4 Conus Medullaris and Caudaence complete sensory loss or significantly dimin-

Equina Syndrome ished nociceptive responses, electrically stimulatedA conus medullaris syndrome involves an injurymuscle contractions can often be utilised without

of the sacral cord (conus) and lumbar nerve roots pain.within the spinal canal, which usually results in anareflexic bladder, bowel and lower limbs.[42] Sacral 2.1 Physical Deconditioningsegments may occasionally show preserved reflexes(e.g. bulbocavernosus and micturition reflexes). A Persons with SCI usually live sedentarycauda equina syndrome involves injury to the lum- lives,[7,9,68,77] which explains their poor physical fit-


734 Jacobs & Nash

ness and heightened risk of cardiovascular morbidi- a number of noxious stimuli unrelated to musclety and mortality.[9,22,51,78] Nearly one in four healthy stretch, including urinary voiding, venous thrombo-young persons with paraplegia fails to achieve levels sis, thermal dysregulation, occult fracture or infec-of oxygen consumption ( VO2) on an arm exercise tion.[96] In contrast, damage to lower motor neuronstest sufficient to perform many essential activities of involving injury below T10 usually results in flacciddaily living.[8] While those with paraplegia have far paralysis and loss of neuromuscular response togreater capacities for activity and more extensive administration of alternating electrical currents.choices for exercise participation than persons with Rapid bone demineralisation is expected duringtetraplegia, they are only marginally more fit.[7,11] the first year after SCI, after which bone density

levels continue to slowly decay. Increased urinary2.2 Musculoskeletal Decline excretion of calcium and hydroxyproline,[97]and pro-

gressive rarefying of bone on radiographs are evi-Altered structural and contractile properties of dent throughout this period. About one-third to one-

muscle after SCI limit the ability of totally paralysed half of bone mineral density is lost by 1 year afterand weakened muscle to sustained intense contrac- injury, with primary losses occurring in thetions for extended durations. Most studies of suble-

supracondylar femur. The inevitable course of SCIsional muscle after SCI in humans report fibres that: leads to underhydroxylated and hypocalcific are smaller than those above the lesion and those bone[98,99] with permanently heightened susceptibili-

of persons without SCI;[79-83] ty to fracture, even following trivial or impercepti- have less contractile protein;[84] ble trauma.[100] Joints experience similar deteriora- produce lower peak contractile forces;[85,86] tion[60] and heightened injury susceptibility brought transform toward fast phenotypic protein expres- on by cartilage atrophy[101] and joint space deformi-

sion;[81,87-90] ties.[102-104] increase myosin heavy chain isoforms;[90,91]

decrease their resistance to fatigue.[19,79,84,92,93] 2.3 Cardiovascular Disease, DyslipidaemiaMuscle fibre cross-sectional area declines within and Comorbidities

1 month of SCI,[80,89] while electrical stimulation ofEpidemiological studies conducted in the earlymuscle paralysed for more than 1 year evokes forces

1980s, and thereafter, reported emergence of cardio-only one-seventh to one-third those of subjects with-vascular disease as a major cause of death in personsout SCI.[85,86,94] Physiological and contractilewith SCI.[1,3,24,105] While genitourinary complica-properties adopted after SCI further compromise thetions accounted for 43% of deaths in the 1940s andability of muscle without motor sparing to optimally1950s, mortality from these causes were reduced toincrease in size and metabolic activity after exercise10% of cases in the 1980s and 1990s.[24,106,107] Car-reconditioning,[95] which has adverse consequencesdiovascular diseases currently represent the mostfor cardiovascular, musculoskeletal and comorbidfrequent cause of death among persons survivingdiseases to which those with SCI are highly suscep->30 years after injury (46% of deaths) and amongtible.persons >60 years of age (35% of deaths)[107,108]Persons sustaining SCI develop muscles below

the level of the lesion that are either hypertonic or Decline of cardiovascular function in personsatonic depending on the level and type of SCI. aging with SCI mirrors that experienced by personsHypertonia is the more common condition in which who age without SCI, although at an acceleratedexaggerated rate-dependent stretch results in spastic rate.[23] Asymptomatic cardiovascular disease alsocontraction. This results from damage to the upper occurs at earlier ages after SCI[108,109] and its symp-motor neurons alone, in which descending inhibition toms may be masked by interruption of ascendingof reflex response in interrupted by cord injury. afferent pain fibres conveying warnings of impend-Hypertonia in these individuals can by worsened by ing heart damage or death.[108-110] Several major risk



factors commonly reported in persons with SCI have been firmly identified, although physical inactivi-ty,[127] truncal obesity[113,114] and sympathetic dys-been linked with their accelerated course of cardio-function[111,112] have been suggested as causes. Anvascular disease; these include dyslipidaemia[7,22,78]association may also exist between their abnormaland a sedentary lifestyle imposed by muscle paraly-lipid profiles and insulin resistance. Such an associ-sis and limited exercise options.[8,9] The cardiovas-ation has been identified in persons without SCIcular disease risks of individuals without SCI arehaving depressed serum HDL-C, as they are alsoworsened by hyperinsulinaemia[22,111,112] and elevat-especially prone to insulin resistance.[128-130] Thised percentages of body fat,[113,114] which are com-risk profile closely matches that of persons withmon among persons with SCI.[24]SCI, in whom isolated low HDL-C and insulin resis-An atherogenic lipid profile is commonly report-tance are often comorbid.[51]

ed in persons with chronic SCI.[22,78,112-115] This lipidprofile satisfies criteria for designation as dys-

2.4 Cardiac Structure and Functionlipidaemic, i.e. elevated total cholesterol (TC), trig-lyceridaemia and plasma low density lipoprotein- Individuals with chronic SCI experience variouscholesterol (LDL-C) or depressed high density lipo- types of circulatory dysregulation depending on theprotein-cholesterol (HDL-C).[116] All have all been level of their cord lesion.[96] When injury occursreported in sedentary persons with SCI, although above the level of sympathetic outflow at the T1elevated TC is not observed in all of these stud- spinal level, resting hypotension with mean arterialies,[115,117] and LDL-C concentrations, while some- pressures of 70mm Hg are common.[131] In additiontimes elevated, show patterns of elevation typical of to challenging effective orthostatic pressure regula-

tion, low pressures also instigate altered heart struc-those reported in the general population.[115] Theture and function observed after SCI.[132] As size andmost consistent finding of reports examining thearchitecture of the human heart are known to belipid profiles of persons with SCI is a depressedinfluenced by peripheral circulatory volume andblood plasma concentration of the cardioprotectivesystemic pressures, withdrawal from normal activityHDL-C[22,78,114,115,118,119] whose levels are inverselylevels and altered circulatory dynamics transformassociated with cardiovascular risk.[120] More thanthe structure of the heart and alter its pumping40% of persons with SCI have HDL-C levels belowefficiency.[133] For those with tetraplegia, a chronicthe earlier criterion score for high cardiovascularreduction of cardiac preload and myocardial volumerisk (HDL >35 mg/dL). When combined with othercoupled with pressure underloading causes the leftknown risks factors for vascular disease in personsventricle to atrophy.[132,134] In contrast, long-termwith SCI (e.g. prevalent truncal obesity,[114] elevatedsurvivors of paraplegia are normotensive and havebody mass indices,[113] physical inactivity[8,9] re-normal left ventricular mass and resting cardiacduced lean body mass,[95,113,121-123] diabetes,[124,125]output, but experience a cardiac output comprised ofmetabolic syndrome X[126] and advancing age),[18]elevated resting heart rate (HR) and depressed rest-the risks of abnormal lipid profile on disease pro-ing stroke volume (SV).[28,134] This lowered SV isgression become magnified.attributed to decreased venous return from the im-Insulin resistance occurring in a high percentagemobile lower extremities or frank venous insuffi-

of persons with SCI was first reported more than twociency of the paralysed limbs.[135,136]decades ago.[125] Since that time, others have con-

firmed this finding and included insulin resistance 2.5 Vascular Structure and Functionamong the cardiovascular risks sustained by personsaging with SCI.[22,111,112,114,127] Almost half the per- The volume and velocity of lower extremity arte-sons with SCI live in a state of carbohydrate intoler- rial circulation is significantly diminished after SCI,ance or insulin resistance.[22,125] A reason for preva- with volume flow of about half to two-thirds thatlent insulin resistance in persons with SCI have not reported in matched subjects without paraly-


736 Jacobs & Nash

sis.[56,137] This circulatory hypokinesis[138] results sence of, or meagre catecholamine responses to,from loss of autonomic control of blood flow as well exercise in these individuals have been reported[161]as diminished regulation of local blood flow by and explains their suppressed HR responses to exer-vascular endothelium.[56] The lowering of volume cise. Thus, cardiac acceleration during exercise im-and velocity contribute to heightened thrombosis plies withdrawal of vagal tone and not increasedsusceptibility commonly reported in those with sympathetic drive.acute and subacute SCI.[58] A contributing factor to Few direct clinical comparisons can be madethrombosis disposition appears to be a markedly between persons having SCI above and below thehypofibrinolytic response to venous occlusion of the highest level of sympathetic outflow at T1 (i.e. be-paralysed lower extremities,[139] a poor response tween those persons whose motor status results inlikely attributable to low blood flow conditions in tetraplegia and paraplegia). Testing of subjects hav-the paralysed lower extremities[54,56] or interruption ing inhomogeneous lesion levels usually leads toof adrenergic pathways that regulate fibrinolysis in widely variable chronotropic, pressor, fuel, periph-the intact neuraxis.[59] eral circulatory, thermal and work capacity re-

sponses. For those with paraplegia from T2 to T5 (orT6), sparing of sympathetic efferents to the heart2.6 Autonomic Dysregulationwith resulting noradrenergic-mediated cardiac ac-

Like those of the motor system, sympathetic celeration will be observed. A relatively normalnerve tracts descend in the spinal cord, albeit within response is observed below T5 or T6,[162] as centralthe intermediolateral columns and not the corticos- inhibitory control of the adrenals (normally inner-pinal tracts, and exit with motor nerves in the vated from T6T9) is regained below thesethoracolumbar segments. As no sympathetic auto- levels.[158]nomic tracts exit the cord above the T1 spinal level,individuals with cervical injuries often sustain 3. Volitional Upper Extremity Exercise indecentralisation of their sympathetic nervous sys- Persons with SCItem. Loss of autonomic outflow to the adrenals isalso observed in persons with paraplegia above theT6 spinal level. Injury above the sacral cord seg- 3.1 Acute Physiological Responses toments abolishes central parasympathetic regulation Exercise Stressof genitourinary organs (S2-4), which explains thecommon occurrences of neurogenic bowel and blad- SCI blunt the expected physiological responsesder after SCI, as well as erectile dysfunction in to exercise and diminish peak exercise capacity.[163]males.[140] Autonomic dysfunction that results from These limitations are associated with the level ofinjury above the thoracolumbar levels of sympathet- SCI, and are explained by various factors. First,ic nerve outflow is associated with cardiac and cir- ascending levels of injury cause greater loss of mus-culatory dysfunction,[34,132] clotting disorders,[58] al- cle mass necessary to serve as prime movers andtered insulin metabolism,[112,125] resting and exercise stabilisers of trunk position. This requires that theimmunodysfunction,[65,141-151] orthostatic incompe- arms simultaneously generate propulsive forces andtence,[152] osteoporosis and joint deterioration,[60,153] steady the trunk during exercise. Secondly, increas-and thermal dysregulation at rest and during exer- ing levels of injury are associated with increasingcise.[154-157] A blunted chronotropic response to ex- adrenergic dysfunction, and at key spinal levelsercise in persons with tetraplegia is well document- dissociate adrenal, cardiac and total sympatheticed,[158-160] and usually yields peak HRs in the nervous system control from the brain. As the adren-mid-120 beats/min range, similar in magnitude to ergic and noradrenergic systems play key roles inpersons without SCI who exercise under conditions cardiovascular regulation and fuel homeostasis dur-of pharmacological adrenergic blockade. The ab- ing exercise, their loss attenuates the cardiovascular



and metabolic efficiencies achieved in persons with injuries below T5 may be due to adrenergic overac-tivity accompanying their paraplegia.[158,161,169]an intact neuraxis.

Many studies have observed a direct association3.2 Cardiorespiratory Testingamong level of injury, peak workload attained and

peak oxygen uptake ( VO2peak) reached during arm Assessment of cardiorespiratory fitness in per-crank testing. This association serves as the basis for

sons with SCI requires specialised knowledge ofsports classification used during paralympic and both exercise testing procedures and the uniqueother sports events for persons competing with physiology that ensues SCI. Exercise testing modal-physical disability. Exercise performance after SCI ities for these individuals commonly employ over-is limited by circulatory dysregulation accompany- ground wheelchair propulsion on a treadmill oring thoracic injuries.[138,156,159,164-166] Individuals

wheelchair rollers, cyclical arm ergometry and vari-with injuries below the level of sympathetic outflow

ations of electrically stimulated exercise. Exerciseat T6 have a significantly lower resting SV and testing by wheelchair propulsion offers the advan-higher resting HR than persons without paraple- tage of comparison to many wheelchair-based dailygia.[156,159,167] The significant elevation of resting tasks. However, wheelchair propulsion testing gen-and exercise HR is thought to compensate for a erally requires specialised equipment. Also, it is notlower cardiac SV imposed by pooling of blood in the known whether testing is best when using a singlelower extremity venous circuits, diminished venous standardised wheelchair, in which the usual wheel-return and cardiac end-diastolic volumes, or frank chair-used interface is compromised, or having sub-circulatory insufficiency.[138,168] Adjustments to the jects use their habitual chair, in which some individ-adrenergic systems after SCI may also regulate the uals may be advantaged by better equipment. Theseexcessive chronotropic response to work, as higher factors limit use of wheelchair ergometry as a re-resting catecholamine levels and exaggerated cat- search and clinical testing tool.echolamine responses to physical work have been The exercise test mode most commonly used inreported in individuals with paraplegia with middle the cardiorespiratory testing of persons with SCI isthoracic (T5) cord injuries. These exceed resting and the arm crank ergometer. The lack of task specificityexercise levels of both high level paraplegics and to wheelchair mobility has been considered a limita-healthy persons without SCI.[155,169] Hypersensitivi- tion to their usefulness. However, as these devicesty of the supralesional spinal cord is believed to are generally found in the rehabilitation environ-regulate this atypical adrenergic state and dynamic, ment and allow standardised application of testingwhich contrasts the downregulation of adrenergic stresses, it represents the most frequently usedfunctions observed in persons with high thoracic and means for clinical or fitness assessment of wheel-cervical cord lesions.[155,161] chair users. Reliable test results require consistent

An exaggerated HR response is experienced dur- positioning of the test subject and the ergometer.ing physical activity by persons with paraplegia,[158] The test subject and the cranking ergometer shouldwhich may be performance delimiting. This belief is be positioned so that the axis of the crank arm is

horizontally aligned with the subjects shoulderconsistent with reports in which subjects with para-joint and the elbows are slightly flexed at the pointplegia require higher levels of VO2 to performof furthest reach. To ensure enhanced reliability ofthe same work intensity as subjects withouttest results, care should be taken to replicate subjectSCI[32,138,156,170] and may represent a limiting factorpositioning and to use the same wheelchair andin the performance of activities of daily liv-cushion. The latter may affect seating stability anding.[21,156,171] As the sympathetic nervous systemexercise efficiency.regulates haemodynamic and metabolic changes ac-

companying exercise, the elevated VO2 and HR Cardiorespiratory exercise testing of personsresponse to work in individuals with paraplegia with with SCI follows the same general protocols as


738 Jacobs & Nash

testing in the general population. In most cases, the cardiac output [ Q]) adaptations or increases in pe-graded multi-stage tests proceed in 2- to 3-minute ripheral oxygen extraction (a- VO2 difference), orstages until volitional exhaustion. As VO2peak is whether central adaptations take place at all. Onlydependent on level of SCI, lower intensity loads are one endurance training study examining 16 weeks ofapplied than those used in standard exercise testing. intense arm exercise observed clear evidence ofThese workloads have been detailed in several pub- central cardiovascular benefit.[176] Notwithstandinglications,[172-175] although no particular advantage the mechanisms contributing to increased VO2peakfor a single testing strategy has been tested or estab- after arm exercise training, many studies report indi-lished. However, accurate and valid results require viduals with paraplegia improve their VO2peak bythat testing utilise metabolic monitoring to establish 1020% following 812 weeks of training. Thesethe VO2peak, as prediction equations normally used gains are inversely proportional to the level of SCI,to estimate maximal responses in persons without as those with higher levels of injury attain lowerdisability have not been validated in those with SCI. peak exercise capacities on arm exercise test than

those with lower-level SCI, and both groups lowerthan persons without disability tested by arm3.3 Endurance Trainingergometry.

In most cases, injury to the spinal cord renders Endurance training recommendations for thosethe lower extremities without sufficient strength, with SCI do not vary dramatically from advice di-endurance or motor control to support safe and rected to the general population.[192-194] The Ameri-effective physical training. This explains why most can College of Sports Medicine recommended train-exercise training after SCI employs upper extremity ing frequencies, durations and intensities are con-exercise modes including arm crank ergometry, tained in Exercise Management for Persons withwheelchair ergometry and swimming. All of these Chronic Diseases and Disabilities.[192] Generally,training modes improve VO2peak in those with three to five weekly exercise sessions of 2060SCI,[27,32,172,176-186] with the magnitude of improve- minutes in duration and at an intensity of 5080%ment inversely proportional to level of spinal lesion. VO2peak is the recommended exercise prescriptionWhile it is possible for persons with low tetraplegia for persons with paraplegia using the followingto train on an arm ergometer, special measures must modes of exercise:be taken to affix the hands to an ergometer and their

arm crankinggains in VO2peak fail to match those of their SCI wheelchair propulsion

counterparts with paraplegia.[187] Therefore, the lev- swimmingel of injury is a key to predicting outcome from arm wheelchair sportsendurance training.[188,189] Guidelines for training circuit resistance training (CRT)after SCI have been published by several authori- electrically stimulated cyclingties,[32,52,172] although testing for superiority of train- electrically stimulated walking.ing algorithms has not been performed. However,

given that most persons with SCI are sedentary long This reference suggests that target exercise inten-after injury and the accepted dictum that training sities should produce HR responses equivalent tobest benefits the most deconditioned individuals, 5080% of the individuals peak HR. As in thethese methods are nonetheless successful in achiev- general population, excessive exercise volume hasing higher levels of fitness. been associated with increase pain and injury. Thus,

Benefits of arm conditioning are widely reported exercise frequency and duration should be carefullyfor persons with SCI, with many studies reporting monitored and gradually increased with the input ofsignificant increases in VO2peak after train- certified exercise professionals familiar with theing.[27,185-187,190,191] It is less clear whether the unique physiological responses of persons with SCIchanges in VO2peak result from central (HR, SV, to exercise. As long-term compliance and injury



avoidance are major goals of training, erring on the were limited to subjects assigned high-intensityconservative side of selected exercise durations and training, and occurred only in the shoulder jointintensities are prudent and more important for per- extensor and elbow flexor muscles. Otherwise, nosons training with a disability than those without. changes in shoulder joint abduction or adduction

strengths were reported, and none of the musclesthat move or stabilise the scapulothoracic articula-3.4 Resistance Training for Persons with SCItion or chest were stronger following training. These

Far less is known about effects of resistance than results suggest that arm crank exercise is ineffectiveendurance training in persons with SCI. This might as a training mode for upper extremity strengtheningseem counterintuitive, as muscle weakness has been because it fails to target the muscles most involvedreported to precipitate pain and dysfunction as per- in performance of daily activities.sons with SCI age with their disability. Moreover, Conditioning of five paraplegic and five te-the most commonly reported symptom of upper traplegic subjects three times weekly for 9 weeksextremity physical dysfunction among persons with

was reported using a hydraulic fitness machine.[205]SCI is pain of the shoulder joint and girdle.[66,195-200] Exercises were limited to two manoeuvres: (i) chestWhile a single cause for shoulder pain has not been press/chest row; and (ii) shoulder press/latisimusidentified, deterioration and injury resulting from pull.[205] Significant increases in peak values of VO2insufficient shoulder strength is one commonly citedand power output measured by arm ergometry test-

source.[63,199-202] Pain that accompanies wheelchair ing were observed at the conclusion of the study,locomotion and other wheelchair activities reported-although no testing was conducted that directly mea-ly interferes with functional activities including up-sured strength gain in any muscle groups undergo-per extremity weight bearing for transfers, high re- ing training. Another study focused their training on

sistance muscular activity in extremes of range ofstrengthening of the scapular muscles, although this

motion, wheelchair propulsion up inclines and fre-study focused solely on the scapular retractor mus-quent overhead activity.[196,198-200] Onset of pain iscles when comparing seated rowing and a

common during body transfer activities and severitystandardised scapular retraction exercise, and did soincreases as time following injury lengthens.[196]only for concentric actions.[206] The authors foundGiven evidence that wheelchair locomotion is athat higher levels of retractor activation were ob-

major source of pain and dysfunction for personstained during backward compared with forwardwith SCI, incorporation of resistance training intowheelchair locomotion and suggested that rowingthe healthcare plan of those with SCI appears bothwas effective for improving scapular retractor activ-justified and essential.ity and cardiorespiratory fitness. A recent studySeveral investigators have studied effects of re-observed reduced shoulder pain following a series ofsistance exercise in persons with paraplegia. In ashoulder resistance exercises using elastic bands.[63]study of Scandinavian men (most of whom had

As both endurance and resistance exercise bene-incomplete low thoracic lesions) a weight-trainingfit those without SCI, the effects of CRT[207] onprogramme emphasising triceps strengthening forvarious attributes of fitness, dyslipidaemia andcrutch walking was undertaken for 7 weeks withshoulder pain have been studied in young and mid-modest but significant increases in VO2peak ob-dle-aged subjects with paraplegia. This exercise pro-served following training. These endurance gainsgramme incorporates periods of low-intensity high-were accompanied by increased strength of the tri-paced movements interposed within activities per-ceps brachii.[203] Another study[204] examined theformed at a series of resistance training stations. Theeffects of arm ergometry in subjects assigned toCRT exercise programme adapted for persons withhigh-intensity (70% of their VO2peak) or low-inten-paraplegia consisted of three circuits of six resis-sity training (40% of their VO2peak) for 20 or 40

minutes per session, respectively. Strength gains tance stations encompassing three pairs of agonist/


740 Jacobs & Nash

antagonist movements (e.g. overhead press and pull) include site-specific stimulation of the lower ex-and three 2-minute periods of free wheeling arm tremities[82,209-212] and upper extremities,[65,213-218]cranking performed between resistance ma- leg cycling,[30,34,134,219-222] leg exercise with uppernoeuvres. No true rest periods were allowed during extremity assist,[222-225] lower body rowing,[50] elec-the performance of CRT, with active recovery limit- trically assisted arm ergometry,[226,227] electricallyed to the time necessary for the subject to propel the stimulated standing[76,217] and electrically stimulatedwheelchair to the next exercise station. Three week- bipedal ambulation either with[74-76,228,229]or withoutly sessions were completed with each session lasting an orthosis.[55,70,72,173,230-232] Most forms of exerciseapproximately 45 minutes. Young subjects undergo- require that the lower motor neuron system remaining 16 weeks of mixed resistance and endurance intact following injury, as direct activation of theexercise increased their arm VO2peak by an average peripheral nerve and not the muscle by electricalof 29%, with accompanying strength gains of current ultimately results in muscle activation.[233]1340%, depending on the upper extremity site test- This reality excludes most individuals having caudaed.[174] Subjects undergoing CRT lowered their total equina or conus medullaris syndromes from electri-and LDL-C while increasing their HDL-C by nearly cally stimulated exercise. It may also compromise10%.[175] Subjects aged over 40 years undergoing the efficiency of a muscle having a denervated seg-the same treatment for 12 weeks experienced signif- ment from injury to its anterior horn cells or spinalicant gains in all of endurance, strength and anaerob- (Wallnerian) degeneration from injured adjacentic power, even though the latter was not specifically spinal areas. Many applications of SCI target muscletargeted by training (Nash MS, unpublished data). strengthening of limb segments whose motor func-Shoulder pain present in these subjects before train- tion is partially spared by injury,[76] while others useing was assessed by a pain instrument validated in electrical current as a neuroprosthesis for the lowerthe population and significantly reduced. Pain was extremities[71,229] and upper extremities.[234-238]eliminated in four of ten subjects. Most electrical stimulation devices currently ap-

In a separate study, the effects of circuit training proved for use by the US FDA employ surface, notperformed on an adapted multi-exercise system implanted, electrical stimulation. The most commoncould be replicated by use of elastic bands.[208] Evi- uses of surface electrical stimulation for systemdence therefore supports health and fitness advan- exercise in those with SCI include electrically stim-tages of CRT over either endurance or resistance ulated cycling, either with or without upper extremi-exercises alone for persons with paraplegia. ty assistive propulsion and electrically stimulated

ambulation. Qualifications necessary to safely par-General recommendations for strength trainingticipate in exercise programmes have been de-exercise prescription include three sets of 812 repe-scribed[71,72,233,239,240] and risks of participation aretitions per exercise movement for two sessions perincluded in the section of this monograph addressingweek at moderate to high intensity using the follow-adverse events associated with exercise by thoseing modes of exercise:with SCI. free weights

weight machines4.2 Leg Cycling Exercise elastic tubing and bands.

The simplest form of multi-limb segmental exer-4. Electrically Stimulated Exercise incise for persons with SCI employs a cycling motionPersons with SCIperformed in a slightly recumbent seated position.This electrically stimulated cycling uses electrically4.1 Basis of Electrically Stimulated Movementactivated contractions of the bilateral quadriceps,

Many forms of electrically stimulated exercise hamstrings and gluteus muscles under computerare available for use by persons with SCI. These microprocessor command.[31] Control of pedal ca-



dence and muscle stimulation intensity is exerted by creased rate of bone turnover by another,[10] al-feedback provided from position sensors placed in though the sites benefiting from training are thethe pedal gear.[241] lumbar spine and proximal tibia, not the proximal

femur.[249] Not all studies have found a post-trainingTraining with electrically stimulated cycling isincrease in mineral density for bones located belowoften preceded with electrically stimulated strength-the level of the lesion.[250] Those that fail to do soening of the quadriceps muscles, which is necessaryhave usually studied subjects with longstanding pa-in cases of severe muscle atrophy or diminishedralysis, in which attenuation or reversal of oste-muscle endurance.[209,221] Responses to electricallyopaenia by any treatment has yet to be reported.stimulated exercise are variable, ranging from poorNotwithstanding, a study examining the appearanceto robust. As noted, poor muscle strength and endur-of lower extremity joints and joint surfaces usingance and altered muscle contractile properties nor-magnetic resonance imaging reported no degenera-mally accompany SCI. In general, these factors willtive changes induced by cycling, and less joint sur-slow success in training, especially in those individ-face necrosis than previously reported in sedentaryuals with longstanding paralysis, absent spasticitypersons with SCI.[60] Improved body compositionand flexor patters of spasticity. Electrically stimulat-favouring increased lean mass and decreased fated strength training programmes are capable of al-mass[251] and an enhancement of whole-body insulintering the strength, resistance to fatigue and contrac-uptake, insulin-stimulated 3-0-methyl glucose trans-tile properties of the muscles undergoing the train-port and increased expression of GLUT4 transporting. Dudley and associates,[209] demonstrated theprotein in the quadriceps muscle have been report-effectiveness of a simple programme of electricallyed.[252] In a recent report, this training has resulted ininduced knee extensions, performed twice weeklyimproved profiles of insulin resistance.[253] Whenover an 8-week period, dramatically reversed mus-combined with simultaneous upper extremity armcular atrophy of the quadriceps muscles.ergometry, the acute cardiovascular metabolic re-Notwithstanding poor levels of muscle strengthsponses to electrically stimulated cycling are moreand endurance early in most training programmesintense and the gains in fitness greater than observedand despite limited ability to exercise against intensewith lower extremity cycling alone.[224,253]workloads, enhanced levels of fitness,[224,242,243] im-

proved gas exchange kinetics[244,245] and increasedmuscle mass[218] have been reported following exer- 4.3 Bipedal Ambulationcise training using electrically stimulated cycling.For those with neurologically incomplete injuries, Complex electrical stimulation to achieve bipe-gains in lower extremity mass, as well as isometric dal ambulation has been used as a neuroprosthesisstrength and endurance under conditions of volunta- for those with motor-complete injuries[71,72,228,239,254]ry and electrically stimulated cycling have been and an assistive neuroprosthesis for persons withreported.[218] Reversal of the adaptive left ventricu- incomplete SCI who lack necessary strength to sup-lar atrophy reported in persons with tetraplegia has port independent ambulation.[255-263] Surface and im-also been observed, with near normalisation of pre- plantable neuroprostheses for those without sparedtraining cardiac mass.[134] This change may be asso- motor function have both been fabricated,[76,264] al-ciated with significantly improved lower extremity though the sole method currently approved by thecirculation following training,[246,247] which is also FDA (Parastep-1)1 uses surface electrical stimula-accompanied by a more robust hyperaemic response tion of the quadriceps and gluteus muscles.[72,230]to experimental occlusion ischaemia.[55,56] Muscle activation is sequenced by a microprocessor

Attenuation of paralytic osteopaenia has been worn on the belt, with activation of step initiated byobserved by several investigators[248,249] and an in- a finger-sensitive control switch located on a rolling

1 The use of trade names is for product identification purposes only and does not imply endorsement.


742 Jacobs & Nash

walker used by ambulating subjects. When pressed, augmented hyperaemic response to an experimentalischaemic stimulus.[55] No change in lower extremi-the electrical stimulator sends a current to the stancety bone mineralisation following has been report-limb that initiates contraction of the quadriceps anded,[232] although most subjects participating in re-gluteus muscles. Contralateral hip flexion is thensearch trials of electrically stimulated exercise areachieved by exploiting an ipsilateral flexor with-beyond the duration of injury at which reversal ofdrawal reflex obtained by introducing a nociceptivetheir neurogenic osteoporosis is expected.[232]electrical stimulus over the common peroneal nerve

at the head of the fibula. This allows the hip, knee5. Risks of Exercise When Performed byand ankle to move into flexion followed by exten-Persons with SCIsion of the knee joint by electrical stimulation to the

quadriceps. As muscle fatigue occurs increasing Special attention is required when designing, in-levels of stimulation can be provided by a switch stituting or performing exercise programmes formounted on the handle of the rolling walker. persons with SCI. Some of the risks encountered

As in the case of electrically stimulated cycling, will be similar to those experienced by personsfunctional use of ambulation neuroprostheses by without paralysis, although complications such asthose with paraplegia are compromised by post- general overuse may be exaggerated in persons withinjury muscle weakness and poor endurance. These SCI, and their occurrence will likely compromiseneed to be addressed in subject preparation before daily activities to a far greater extent than similarambulation training is initiated. Electrically activat- injuries arising in persons without SCI.ed knee extensions against progressively increased

5.1 Autonomic Dysreflexiaresistance (sandbag at ankle) is the standard trainingexercise. While not as commonly addressed, condi- Individuals having cord injuries at or above thetioning of the gluteal muscles with electrically pro- T6 spinal level are prone to episodes of autonomicduced hip bridging (in supine position) prior to hyperreflexia when exposed to noxious stimuli.[266]bodyweight-supported gait training will enhance the The neurological basis for these episodes involvesresponse of the hip extensors to electrical stimula- loss of supralesional sympathetic inhibition that nor-tion. A single most effective protocol to satisfy

mally suppresses the unrestricted autonomic reflexrequisite strength and endurance needs for upright

accompanying such exposure. This allows the ad-ambulation training has not been reported. Howev-

renals to release high concentrations of epinephrineer, it is inadvisable to undertake electrically stimu- (adrenaline) under reflex control and infralesionallated ambulation training until the ability to stand

adrenergic targets to experience the full measure ofwith electrical stimulation for at least 35 minutes

reflex noradrenergic stimulation.[267] The most com-has been demonstrated.

mon stimuli evoking autonomic dysreflexia areOnce training is initiated, rates of ambulation are bladder and bowl distention before their emptying.

relatively slow and distances of ambulation relative- Other stimuli include venous thromboembolism,ly limited when using the system,[229] and the com- bone fracture, sudden temperature change, febrilemunity use of these devices remains limited to a episodes and exercise. The disposition to autonomicsmall percentage of training subjects. Despite the dysreflexia during exercise is especially heightenedlimitations of ambulation velocity and distance, am- when an electrical current is used to generate musclebulation distances of up to 1.6km (1 mile) have been movement, or when exercising while febrile or dur-reported after training in some subjects[229] and up- ing bladder emptying. Episodes of autonomic dys-per extremity fitness is enhanced following ambula- reflexia are characterised by hypertension andtion training.[71,173] Other adaptations to training in- bradycardia, supralesional erythema, piloerectionclude significantly increased lower extremity mus- and headache. In some cases, hypertension can risecle mass,[265] improved resting blood flow[55] and an to the point where crisis headache results, and cere-



bral haemorrhage and death might ensue. Recogni- vironment controlled for temperature and humidi-tion of these episodes, withdrawal of the offending ty.[278,282] Thus, attention should be paid to hydrationstimulus, and the possible administration of a fast- and, if possible, limiting the duration and intensityacting peripheral vasodilator may be critical in of activities performed in intemperate environ-preventing serious medical complications. Prophy- ments.laxis with a slow calcium channel antagonist or1-selective adrenergic antagonist may be needed 6. Conclusionsprior to exercise.[268-270] It is known that wheelchair

Multisystem organ dysfunction is common afterracers have intentionally induced dysreflexia as anSCI. Depending on the level of injury, alterations ofergogenic aid by restricting urine outflow through acardiac function, peripheral circulation, autonomicFoley catheter,[271] which represents a dangerousfunction, skeletal integrity, muscle composition andand possibly life-threatening practice.genitourinary functions all accompany an SCI. The

5.2 Musculoskeletal Injury fact that many of these pathological system changesare reversible permits better understanding of theFracture and joint dislocation of the lower ex-roles played by central innervation and physicaltremities is a risk of participation in exercise byactivity on organ system function in persons withthose with SCI, and may be caused by asynergisticintact neuraxes. As levels of injury, types of injurymovement of limbs against the force imposed byand the extent of organ system dysfunction varyeither electrical stimulation or the device used foramong persons with SCI, careful attention must beexercise.[36] This explains why these activities arepaid to accurate classification of individuals beforecontraindicated for individuals with severe spastici-entry into clinical treatment or study. The use ofty or spastic response to the introduction of electri-homogeneous subject populations based on similarcal current. Precautions to prevent overuse injurieslevels, types and durations of injury is especiallyof the arms and shoulders must be taken for thoseimportant if conclusions concerning deconditioningparticipating in upper extremity exercise.[201,206,272]and reconditioning in these persons are to beAs the shoulder joints are mechanically ill-suited toreached.perform locomotor activities, but must do so in

Despite these special needs and warnings, manyindividuals using a manual wheelchair for transpor-persons with SCI benefit from sustained therapeutictation, these injuries may ultimately compromiseand recreational exercise. Individuals with higherperformance of essential daily activities includinglevels of cord injury may require electrical stimula-wheelchair propulsion, weight relief and depressiontion to perform exercise, which poses special restric-transfers.[273,274]tions on use and unique risks from participation.Qualified individuals safely improved cardiovascu-5.3 Hypotensionlar and musculoskeletal functions. Positive benefits

Small risks of post-exercise hypotension[131,275] of training on bone density, regulation of orthostaticare associated with lost vasomotor responses to or- tolerance and affect have been reported in studiesthostatic repositioning,[276] although these episodes with limited numbers of subjects and require wellcan abate after upper limb training. controlled investigations for confirmation. Individu-

als with spared motor control of the upper extremity5.4 Thermal Dysregulation

can perform arm or wheelchair exercises and partici-Individuals with SCI often lack sudomotor re- pate in recreational sports. Greater emphasis needs

sponses below their level of injury and are thus to be placed on strengthening of the upper extremitychallenged to maintain thermal stability.[154,277-279] to preserve shoulder and arm functions for perform-These responses are less pronounced as the level of ance of daily living as these individuals age withSCI descends,[280,281] and when exercising in an en- their paralysis. Risks of injury or illnesses associat-


744 Jacobs & Nash

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