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Journal of Neurologic Physical Therapy:
doi: 10.1097/01.NPT.0000282514.94093.c6
Article

Exercise as a Health‐Promoting Activity Following Spinal Cord Injury

Nash, Mark S. PhD, FACSM

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Associate Professor, Departments of Neurological Surgery and Physical Therapy & Principal Investigator, Applied Physiology Research, The Miami Project to Cure Paralysis, Miller School of Medicine, University of Miami, Miami, FL (msnash@miami.edu)

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Abstract

Spinal cord injury is a catastrophic event that immeasurably alters activity and health. Depending on the level and severity of injury, functional and homeostatic decline of many body systems can be anticipated in a large segment of the paralyzed population. The level of physical inactivity and deconditioning imposed by SCI profoundly contrasts the preinjury state in which most individuals are relatively young and physically active.

Involvement in sports, recreation, and therapeutic exercise is commonly restricted after SCI by loss of voluntary motor control, as well as autonomic dysfunction, altered fuel homeostasis, inefficient temperature regulation, and early-onset muscle fatigue. Participation in exercise activities also may require special adaptive equipment and, in some instances, the use of electrical current either with or without computerized control. Notwithstanding these limitations, considerable evidence supports the belief that recreational and therapeutic exercise improves the physical and emotional well-being of participants with SCI.

This article will examine multisystem decline and the need for exercise after SCI. It will further examine how exercise might be used as a tool to enhance health by slowing multisystem medical complications unique to those with SCI. As imprudent exercise recommendations may pose avoidable risks of incipient disability, orthopedic deterioration, or pain, the special risks of exercise misuse in those with SCI will be discussed.

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INTRODUCTION

Disruption of sensorimotor and autonomic transmission accompanying spinal cord injury (SCI) is experienced by 8000 to 10,000 Americans annually; with an estimated 179,000 persons having survived their initial injury.1,2 Paralysis resulting from SCI was first described in an ancient text as “…an ailment not to be treated,”3 and until the mid-20th century still predestined a relatively shortened lifespan. Thereafter, advances in injury stabilization, medical treatment, and rehabilitation have allowed many of those with SCI to achieve life spans approaching those of persons without disability. Theirs lives, however, remain filled with unique physical, physiological, psychological, and societal challenges, many of which limit their ability to undertake exercise and fully benefit from physical conditioning.4

A sedentary life adopted after SCI typically contrasts the preinjury lifestyle maintained by many persons with SCI, who are usually young and physically active before injury5,6 and sustain profound physical deconditioning thereafter.7–9 This physical deconditioning causes or contributes to lifelong medical complications such as accelerated cardiovascular disease, insulin resistance, osteopenia, visceral obesity, immune system dysfunction, and accelerated aging.10–21 As a result, health care professionals have widely recommended that persons with SCI undertake habitual exercise as part of a healthy lifestyle, insofar as their disability allows. The question of how they should do so, however, has yet to be universally agreed upon. Unlike persons without disability for whom exercise is readily available and easily accomplished, exercise options for those with SCI are more limited. Depending on level of injury the physiological responses to acute exercise may also be less robust than those accompanying exercise in persons having an intact neuraxis, the magnitude of training benefits diminished, and risks of ill-considered activity both greater and potentially irreversible. This makes an understanding of exercise opportunities and risks important if exercise undertaken by those with SCI will ultimately promote benefit and not harm. The following monograph will thus address common medical problems experienced by persons with SCI, typical modes and benefits of exercise conditioning, and risks posed by unsound exercise practices.

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HEALTH-RELATED CONSEQUENCES OF SCI

Physical Deconditioning after SCI

A sedentary lifestyle either imposed on, or adopted by, persons with SCI has ranked them at the lowest end of the human fitness spectrum.7 In many cases physical deconditioning after SCI results from muscle paralysis extensive enough to make voluntary exercise impossible or ineffective. In other cases persons with SCI simply adopt a sedentary lifestyle, or fail to secure personnel and equipment needed to assist their training. Notwithstanding an identified cause for exercise abstention, 1 in 4 healthy, young persons with SCI fails to satisfy a level of fitness needed to perform many essential activities of daily living.8 While those with sparing of upper extremity sensorimotor functions have far greater capacities for activity and more extensive exercise options, they are barely more fit than persons with tetraplegia.7,22

It is widely reported that young persons with SCI sustain diseases and disorders often associated with accelerated aging.15,23 Characteristic conditions of this accelerated state occurring early after SCI include atherogenic dyslipidemia and vascular disease,15,24,25 arterial circulatory insufficiency26–28 diabetes and related endocrine disorders,16,29–31 bone and joint diseases,32 immune dysfunction,19–21,33,34 and pain of musculoskeletal and neuropathic origins.35–39

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Alterations in Cardiac Structure and Function

Circulatory dysregulation is a common finding among persons with SCI,17 as injuries occurring above the T1 spinal level disrupt sympathetic nervous system functions and result in resting hypotension.40 Low mean arterial pressures challenge the ability of persons with cervical SCI to regulate systemic blood pressure during orthostatic challenge and physical activity,41–43 and diminish cardiac ventricular chamber sizes and functions.44 In those with tetraplegia, a chronic reduction of cardiac preload and myocardial volume coupled with chronic hypotension cause the left ventricle to atrophy, which further limits their ability to mount a cardiac output response needed for blood pressure regu-lation.44,45 By contrast, long-term survivors of paraplegia have normal blood pressure, left ventricular mass, and resting cardiac output, although the cardiac output has elements of elevated resting heart rate and depressed resting stroke volume.46,47 This lowered stroke volume is attributed to decreased venous return from the immobile lower extremities accompanying loss or diminished efficiency of venous pumps, or to frank venous insufficiency of the paralyzed limbs.48,49

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Peripheral Vascular Structure and Function

Blood volume and velocity of lower extremity arterial circulation are significantly lowered after SCI, with volume flow of about half to two-thirds that reported in healthy individuals without paralysis.50,51 This so-called “circulatory hypokinesis”28,52 results from loss of autonomic control of blood flow as well as diminished regulation of local blood flow by vascular endothelium.50 The lowering of volume and velocity contribute to heightened thrombosis susceptibility most often reported in those with acute and subacute SCI.53 A contributing factor to thrombosis disposition also appears to be a markedly hypofibrinolytic response to venous occlusion of the paralyzed lower extremities,54 a poor response explained by low blood flow conditions in the paralyzed lower extremities,55,56 or interruption of adrenergic pathways that normally regulate fibrinolysis in the intact neuraxis.57

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Cardiovascular Disease, Atherogenic Dyslipidemia, and their Co-Morbidities

Epidemiological studies published in the early 1980s first reported emergence of cardiovascular disease (CVD) as a major cause of death in persons with SCI.1,15,58 While genitourinary complications accounted for 43% of deaths in the 1940s and 1950s, mortality from these causes were reduced to 10% of cases in the 1980s and 1990s.15,59 Cardiovascular diseases currently represent the most frequent cause of death among persons surviving more than 30 years after injury (46% of deaths) and among persons more than 60 years of age (35% of deaths).59–61

The CVD risks sustained by persons with SCI are similar to those experienced by persons who age without SCI, but occur at an accelerated rate.16 Thus, asymptomatic CVD appears at earlier ages after SCI,62 and may have symptoms masked by interruption of sensory pain fibers that normally convey warnings of cardiac ischemia and impending cardiac damage.62,63 Several major risk factors commonly reported in persons with SCI have been linked with their accelerated course of CVD; these include an atherogenic dyslipidemia,64,65 hyperinsulinemia,30,64,66 and visceral obesity.67,68

An atherogenic lipid profile has been widely reported in persons with chronic SCI.16,68–72 The most consistent finding of this dyslipidemia is a depressed blood plasma concentration of the high-density lipoprotein cholesterol (HDL-C)16,64,68,73,74 whose functions include protection against development of vascular disease.75 More than 40% of young persons with SCI have HDL-C levels that are classified as deficient. Unfortunately, an isolated low high density lipoproteinemia is not the sole CVD risk common among those with SCI. Visceral obesity,68,72 elevated body mass indices,72 physical inactivity,8,9,76 reduced lean body mass,61,77–79 diabetes,16,29 insulin resistance with obesity and dyslipidemia (metabolic syndrome X),80 and advancing age81,82 represent additional risks for disease that account for accelerated disease progression and early CV morbidity.

Insulin resistance occurring in a high percentage of persons with SCI was first reported in 198029 and has since been confirmed by other investigators.64,83,84 As many as half the persons with SCI live in a state of carbohydrate intolerance or insulin resistance.29,64 A reason for prevalent insulin resistance in persons with SCI have not been firmly identified, although physical inactivity,83 obesity,67,68 and sympathetic dysfunction71,84 have all been suggested as causes. An association may also exist between abnormal lipid profiles and insulin resistance, as persons without disability having low HDL-C are also especially prone to insulin resistance.85–87

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Alterations of Muscle Mass, Fiber Morphology, and Tone

Both structure and contractile properties of skeletal muscles are altered after SCI, which may limit the ability of paralyzed and paretic muscles to sustained intense contractions for extended intervals.88,89 Most studies of sublesional muscle report fibers that are smaller than those above lesion and those of persons without SCI,90–94 with less contractile protein91 and lower peak contractile forces.89,95 These fibers also transform toward fast phenotypic protein expression,96–98 increase fast myosin heavy chain iso-forms,99,100 and become more rapidly fatigued.12,90,101 Muscle fiber cross-sectional area declines within one month of SCI,91 and yields forces in response to electrically-stimulated activation only one-seventh to one-third those of persons without SCI.95,102

In addition to altered muscle fiber morphology and contractile properties, muscles below level of spinal lesion develop hypertonia, hypotonia, or atonia depending on the level and type of SCI. Hypertonia accompanying upper motor neuron damage is the more common condition, in which exaggerated rate-dependent stretch results in spastic contraction.103 Spastic muscle contractions can be invoked, or hypertonia exaggerated, by sudden muscle stretch, urinary voiding, venous thrombosis, thermal dysregulation, occult fracture, or infection.104 Hypertonic muscles can also be sent into spasm by electrical current used to generate muscle contractions and exercise.105 By contrast, damage to lower motor neurons often involving injury below T10 commonly results in flaccid paralysis. This confers greater muscle and bone atrophy than upper motor neuron lesion, as well as loss of neuromuscular response to administration of alternating electrical currents.

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EXERCISE OPPORTUNITIES FOR PERSONS WITH SCI

Atypical Physiological Responses to Acute Exercise

Damage to the spinal cord dissociates homoeostatic mechanisms whose integrated functions regulate physiological responses needed to sustain exercise. To varying degrees it further disrupts essential signal integration among motor, sensory, and autonomic targets, and thus profoundly influences acute adjustments to activity and peak exercise capacity. Thus, physiological responses to exercise in persons with SCI differ from those of persons without injury.106,107 Exercise limitations are also associated with the level of SCI, and are explained by various factors:

Progressively higher levels of injury cause greater loss of muscle mass in those muscles that serve as prime movers and stabilizers of the trunk. This requires that the arms simultaneously generate propulsive forces and steady the trunk during exercise.

Progressively higher levels of injury are associated with greater degrees of adrenergic dysfunction, and at key spinal levels totally dissociate adrenal, cardiac, and sympathetic nervous system regulation from central command. Because the adrenergic and nor-adrenergic systems normally adjust key metabolic functions during physical activity, their diminished regulatory input alters the cardiovascular and metabolic efficiencies achieved by individuals who exercise in the presence of an intact neuraxis.

Evidence strongly supports a direct relationship among level of injury, peak workload, and peak oxygen uptake (VO2peak) attained during arm crank testing. Peak work under exercise conditions is delimited by suboptimal circulatory adjustments,28,107–111 as individuals with injuries below the level of sympathetic outflow at T6 have significantly lower resting stroke volumes and higher resting heart rates than persons without disability.109,110,112 The significant elevation of resting and exercise heart rate is thus thought to compensate for a lower cardiac stroke volume imposed by pooling of blood in the lower extremity venous circuits, diminished venous return and cardiac end-diastolic volumes, or frank circulatory insufficiency.113,114 Compensatory upregulation of the intact adrenergic system after SCI may also invoke excessive heart rate responses observed during exercise, which have been observed in persons with paraplegia having middle thoracic (T5) cord injuries.115 These heart rate responses exceed resting and exercise levels of both high-level paraplegics and healthy persons without SCI.110,116 Hypersensitivity of the supralesional spinal cord is believed to regulate this atypical adrenergic state and dynamic, which contrasts the downregulation of adrenergic functions observed in persons with high thoracic and cervical cord lesions.117 The exaggerated heart rate response to endurance exercise in persons with paraplegia118 may limit their ability to achieve high work intensities, as these persons consume higher levels of oxygen to perform at the same work intensity as persons without SCI.52,110,119 As the sympathetic nervous system regulates hemodynamic and metabolic changes during activity, the elevated oxygen consumption and HR response to endurance exercise in persons with paraplegia having injuries below T5 may be due to adrenergic overactivity accompanying their paraplegia.116–118

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Arm Endurance Training

Despite experiencing physical and homeostatic limitations, many persons with SCI can still undertake and benefit from exercise reconditioning. Those who retain upper extremity function have the opportunity to participate in a wide variety of exercise activities and sports,4,120 and ambulate with the assistance of orthoses and computer-controlled electrical neuroprostheses.121–123 Individuals with upper motor neuron lesions have pedaled ergometers using surface electrical stimulation of selected lower extremity muscle groups delivered under computer control.124,125 Further, many body organs and tissues respond to exercise despite dissociation of their control from central command, and because many survivors of SCI experience complete sensory loss or significantly diminished nociceptive responses, electrically-stimulated muscle contractions can often be involved without pain.

In most cases SCI leaves the lower limbs either entirely paralyzed, or with insufficient strength, endurance, or motor control to support safe and effective physical training. This explains why most exercise training after SCI employs the upper extremity exercise modes of arm crank ergometry, wheelchair ergometry, and swimming. All of these training modes improve physical conditioning in those with SCI by an average of 15% to 25%,119,126–131 with a magnitude of fitness improvement usually inversely proportional to level of spinal lesion. While it is possible for persons with low levels of tetraplegia to train on an arm ergometer, special measures must be taken to affix the hands to an ergometer, and their gains in peak oxygen uptake fail to approach those of counterparts with paraplegia.132 Thus, level of injury is a key to predicting benefits obtained from endurance training.133,134

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Resistance Training After SCI

Prevalent upper extremity weakness and pain after SCI justifies a need for increased strength of the shoulders, upper back, chest, and arms. Surprisingly, however, far less is known about resistance than endurance training for persons with SCI. In a study of Scandinavian men (most having incomplete low thoracic lesions) a weight training program emphasizing triceps strengthening needed for crutch walking yielded modest but significant increases in peak exercise capacity accompanied by increased strength of the triceps brachii.135 Others136 have examined effects of arm cycle ergometry in subjects assigned to 70% or 40% of their peak work capacity. Strength gains were limited to subjects assigned to high-intensity training, and occurred only in the shoulder extensor and elbow flexor muscles. Otherwise, no changes in shoulder abductor or adductor muscle strengths were reported, and none of the muscles that move or stabilize the scapulothoracic articulation or chest were stronger following training. These results suggest that arm crank cycle exercise is a poor choice for use as a training mode for upper extremity strengthening because it fails to target the muscles most involved in performance of daily activities. Similar limitations in strengthening were reported following conditioning of 5 persons with paraplegia and 5 with tetraplegia who trained 3 times weekly for 9 weeks using a hydraulic fitness machine. Exercises performed were chest press and row, shoulder press, and latissimus pull.137 Significant increases in upper extremity work and power output were observed, although direct measurement of strength in muscle groups undergoing training was not performed. A recent study observed reduced shoulder pain following a series of shoulder resistance exercises using elastic bands.138

As both endurance and resistance exercises benefit those without SCI, the effects of circuit resistance training (CRT)139 on various attributes of fitness, dyslipidemia, and shoulder pain have been studied in young and middle-aged subjects with paraplegia. The exercise program incorporated periods of low intensity high-paced movements interposed within activities performed at a series of resistance training stations (Figures 1 and 2). The CRT exercise program adapted for individuals with paraplegia consisted of 3 circuits of 6 resistance stations encompassing 3 pairs of agonist/antagonist movements (eg, overhead press and pull) and three 2-minute periods of free-wheeling arm cranking performed between resistance maneuvers. No true rest periods were allowed during the performance of CRT, with active recovery limited to the time necessary for the subject to propel the wheelchair to the next exercise station. Three weekly sessions were completed with each session lasting approximately 45 minutes. Subjects undergoing 16 weeks of mixed resistance and endurance exercise increased their upper extremity oxygen consumption by 29%, with accompanying upper extremity strength gains of 13% to 40%, depending on the site tested.140 Subjects undergoing CRT also lowered their total and low-density lipoprotein cholesterol while increasing their high-density lipoprotein cholesterol by nearly 10%.65 Subjects aged over 40 years undergoing the same treatment for 12 weeks experienced significant gains in all of endurance, strength, and anaerobic power, even though training did not specifically target the latter (M.S. Nash, PhD, FACSM, unpublished data, 2005). Shoulder pain reported in these subjects before training was significantly reduced, and in 4 of 10 individuals eliminated. This circuit has been replicated using elastic bands,141 so that access to expensive weight lifting equipment would not impose a limitation to participation in training. Evidence thus supports health and fitness advantages of CRT over either endurance or resistance exercises alone for persons with paraplegia.

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ELECTRICALLY-STIMULATED EXERCISE AFTER SCI

Electrically-Stimulated Muscle Contractions

The use of electrical current to initiate purposeful movement in individuals with SCI dates to 1963, when Kantrowitz used a developing technology called “functional electrical stimulation” to contract the quadriceps and glutei of an individual with T3 paraplegia.142 Since that time, many forms of electrically-stimulated exercise have been used by persons with SCI. These include site-specific stimulation of the lower extremities143–146 and upper extremities,147–150 leg cycling,125,151–154 leg exercise with simultaneous assistance of the upper extremities,155–157 lower body rowing,158 electrically-assisted arm cycle ergometry,159,160 electrically stimulated stand-ing,123,161 and electrically stimulated bipedal ambulation when using an orthosis162–164 or without an orthosis.165,166

Most forms of electrically-stimulated exercise require that the lower motor neuron system remains functionally intact following injury, as muscle activation occurs via indirect electrical stimulation of the intact peripheral nerve and not muscle.167 This excludes most individuals having cauda equina or conus medullaris syndromes from use of electrically-stimulated exercise. It may also compromise the efficiency of muscle activation in spinal segments sustaining injury to the anterior horn cells, or those experiencing spinal degeneration from injured adjacent spinal areas. Many applications of electrical stimulation to individuals with SCI target muscle strengthening of limb segments whose motor function is partially spared by injury,123 while others use electrical current as a neuroprosthesis for the lower extremities168,169 and upper extremities.170–173 Qualifications to safely participate in these exercise programs have been described in the literature.122,167,168,174

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Leg Cycling Exercise

Multi-limb segmental exercise in the form of cycling can be invoked in persons with SCI using commercially available equipment. Pedaling is initiated by electrically-stimulated contractions of the bilateral quadriceps, hamstrings, and gluteus muscles sequenced under computer microprocessor command.124 Pedal cadence and muscle stimulation intensity is controlled by feedback from position sensors integrated within the pedal gear.175 When combined with simultaneous upper extremity arm ergometry, the acute cardiovascular metabolic responses to electrically-stimulated cycling are more intense, and the gains in fitness greater than observed with lower extremity cycling alone.156

Persons with SCI who wish to undergo electrically-stimulated cycling usually start their training by strengthening of the quadriceps muscles, which is needed to reverse severe muscle atrophy or diminished muscle endurance.143,153 These factors generally slow success in training, especially for those individuals with longstanding deconditioning, low muscle tone, and flexor patterns of spasticity. Despite limited muscle strength and endurance first encountered in most training programs, and despite limited ability to exercise against intense workloads, enhanced levels of fit-ness,156,176,177 improved gas exchange kinetics,178,179 and increased muscle mass150 have been reported following exercise training using electrically-stimulated cycling. For those with neurologically incomplete injuries, gains in lower extremity mass, as well as isometric strength and endurance under conditions of voluntary and electrically stimulated exercise have also been observed.150 Reversal of the adaptive left ventricular atrophy reported in persons with tetraplegia has accompanied conditioning exercise, with near normalization of pretraining cardiac mass.47 This adaptation may be caused by significantly improved lower extremity circulation obtained following training,180,181 which is also accompanied by a more robust response of lower extremity blood flow accompanying an occlusive stimulus.50,182 Attenuation of paralytic osteopenia has been observed by several inves-tigators,183,184 and an increased rate of bone turnover by another,10 with sites benefiting from training at the lumbar spine and proximal tibia.184 Not all studies have found a post-training increase in mineral density for bones located below the level of the lesion,185 but those failing to do so have usually studied subjects with longstanding paralysis, which lowers the likelihood that osteogenesis will occur. Even absent improved bone mineral density, a study examining the appearance of lower extremity joints and joint surfaces using magnetic resonance imaging reported no degenerative changes induced by cycling, and less joint surface necrosis than previously reported in sedentary persons after injury.186 Training has improved body composition by increasing body lean mass and decreasing fat mass,187 and enhanced whole-body insulin uptake, insulin-stimulated 3–0-methyl glucose transport, expression of the quadriceps GLUT4 transport protein,188 and insulin sensitivity.189

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Electrical Stimulation Ambulation Neuroprostheses

Sequenced electrical stimulation has been used as an ambulation neuroprosthesis for those with complete motor injuries,174,190 and as an assistive neuroprosthesis for persons with incomplete SCI who lack strength to support independent ambulation.191–193 Implantable neuroprostheses for those without spared motor function have been used experimentally,123 and brought to market using surface electrical stimulation of the quadriceps and gluteus muscles. (Figure 3.)165,194 Muscle activation for the latter system is sequenced by a microprocessor worn on the belt, with activation of step initiated by a finger-sensitive control switch located on a rolling walker used by ambulating subjects. When on, the electrical stimulator sends current to the stance limb that initiates contraction of the quadriceps and gluteus muscles. Contralateral hip flexion is then achieved by pressing a trigger to activate an ipsilateral flexor withdrawal reflex using a nociceptive electrical stimulus introduced over the common peroneal nerve at the fibular head. This allows the hip, knee, and ankle to move into flexion followed by extension of the knee joint initiated by electrical stimulation to the quadriceps. As muscle fatigue occurs, a switch mounted on the handle of the rolling walker can provide increasing levels of stimulation.

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Success in using an electrically stimulated ambulation neuroprostheses is opposed by postinjury muscle weakness and poor endurance, much like the challenges experienced in early electrically-stimulated cycling. These limitations need to be overcome before ambulation training is undertaken. In cases where independent electrically-stimulated ambulation is achieved, the walking velocities are relatively slow and ambulation distances short.195 Thus, community use of these devices remains limited to a small percentage of training subjects, although ambulation distances of up to one mile have been reported in some individuals.196

Ambulation training enhances upper extremity fitness.168,197 Other beneficial adaptations to training include enhanced lower extremity muscle mass,198 improved resting blood flow,199 and an augmented hyperemic response to an ischemic stimulus.199 Ambulation training has failed to increase lower extremity bone mineralization160 although most subjects begin training after substantial bone demineralization had already occurred.

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LIMITATIONS AND RISKS OF EXERCISE AFTER SCI

Special precautions must be taken when persons with SCI undertake exercise programs for physical conditioning. While typical risks of exercise injury and overuse apply, the consequences of imprudent exercise may be far more serious, potentially irreversible, and will likely compromise daily activities to a far greater extent than similar injuries arising in persons without SCI. A summary of these potential hazards is shown in Table 1.

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Adrenergic Dysregulation After SCI

Limitations in physical function after SCI are typically explained by profound sensorimotor deficits accompanying cord damage, although tracts of the sympathetic nervous system also descend in the spinal cord within the intermediolateral columns and exit with motor nerves in the thoracolumbar segments. This makes these nerve tracts equally susceptible to damage, and the targets they control highly vulnerable to dysregulation after injury. As sympathetic autonomic tracts exit the cord at T1-L2 spinal levels, individuals with complete cervical level injuries often lose all central command over sympathetic nervous system functions, while loss of autonomic outflow to the adrenals and their sympathomedullary cell targets is also observed in persons with paraplegia above the T6 spinal level.

Autonomic dysfunction that results from injury above the thoracolumbar levels of sympathetic nerve outflow is associated with cardiac and circulatory dysfunction, 200,201 clotting disorders,53 altered insulin metabolism,71 resting and exercise immunodysfunction,20,21,202 orthostatic incompetence,203 osteoporosis and joint deterioration,204 and thermal dysregulation at rest and during exercise.205,206 A blunted heart rate response to exercise in persons with tetraplegia is well documented, and usually yields peak heart rates in the mid-120 beat per minute range–similar in magnitude to persons without SCI who exercise under conditions of pharmacological beta-adrenergic blockade.201 Absence of, or limited catecholamine responses to exercise207 explain attenuated heart rate responses to exercise, and also the widely variable pressor, fuel, peripheral circulatory, thermal, and work capacity responses after SCI. When compared with individuals exercising after sustaining paraplegia, the combination of diminished muscle mass and adrenergic dysfunction experienced by individuals with tetraplegia roughly halves their peak exercise capacity.25,208 For those with paraplegia from T2 to T5 (or T6), sparing of sympathetic efferents to the heart with resulting noradrenergic-mediated cardiac acceleration will be observed. A more typical exercise response is observed in persons having injuries below the T6 level,209 as central inhibitory control of the adrenal glands (innervated from T6-T9) is maintained below these levels.210

Perhaps the most worrisome of adverse responses to exercise involves potentially-life-threatening episodes of autonomic hyper-reflexia in persons having injuries above the T6 spinal level.211,212 The neurological basis for these episodes involves loss of supralesional sympathetic inhibition after injury, which normally suppresses the unrestricted autonomic reflex in persons having an intact neuraxis. The most common stimuli evoking autonomic dysreflexia are bladder and bowel distention before their emptying. Other stimuli include venous thromboembolism, bone fracture, sudden temperature change, febrile episodes, and exercise. The disposition to autonomic dysreflexia during exercise is especially heightened when electrical current is used to generate muscle movement, or when exercising while febrile or during bladder emptying. Episodes of autonomic dysreflexia are characterized by hypertension and bradycardia, supralesional erythema, piloerection, and headache.213 In some cases hypertension can rise to the point where crisis headache results, and cerebral hemorrhage and death ensue. Recognition of these episodes, withdrawal of the offending stimulus, and the possible administration of a fast acting peripheral vasodilator may be critical in preventing serious medical complications. It is known that wheelchair racers have intentionally induced dysreflexia as an ergogenic aid by restricting urine outflow through a Foley catheter.214 Such so-called “boosting” of performance represents a dangerous and potentially life-threatening practice.

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Fracture Precautions for Persons with SCI

Postinjury osteopenia is a common concern after SCI, and may result in bone fracture following nominal skeletal stress or trauma.19,215–218 The magnitude of the clinical problem posed by osteopenia and fracture is best revealed by the many attempts to increase sublesional bone-mineral density (BMD) using physical activity,184,185,219,220 weight bear-ing,221,150 physical agents222,223 and drugs.224,225 Despite best attempts to slow bone loss and reduce fracture after SCI, none of these methods has been shown sufficiently effective to justify their widespread use in clinical practice.

Considerable sublesional bone demineralization is expected in the first year after SCI,11,217,226,227 after which bone density levels continue to slowly decay. Bone loss is likely the result of physical, endocrine, and nervous system changes accompanying injury.228 Contributing factors may include depression of serum growth hormone and insulinlike growth factor 1 accompanying SCI,229 as well as low levels of serum testosterone229 and a suppressed Parathyroid Hormone (PTH)-vitamin D axis resulting in lowered PTH, 1, 25-dihydroxyvitamin D, and nephrogenous cyclic adenosine monophosphate levels.230,231 Nutritional deficiencies of vitamin D, deprivation of sunlight, or vitamin D loss from medication effects on accelerated hepatic vitamin D metabolism may contribute to widespread osteopenia after SCI.232

Notwithstanding the known causes for osteopenia, early urinary excretion of calcium and hydroxyproline, and progressive rarefying of sublesional bone on radiographs are clearly evident after SCI.233–235 During the initial period after SCI markers of bone formation remain in the reference range, although at 10 to 16 weeks postinjury resorption is elevated to 10 times the typical level.236 During these times decreased osteoblastic activity is associated with a rapid increase in bone resorption.237,238 While bone of most persons with SCI remains innervated,239 the differentiation of bone marrow osteoprogenitor cells becomes impaired.240 Thus, about one-third to one-half of bone mineral density is lost by one year after injury, with primary losses occurring in the supracondylar femur and proximal tibia.33,216,217,226 During this time bone becomes underhydroxylated and hypocalcific237,238,241 with permanently heightened susceptibility to fracture, even accompanying trivial or imperceptible trauma.242–244 Joints suffer similar deterioration and heightened injury susceptibility brought on by cartilage atrophy and joint space deformities.186

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Musculoskeletal Injury

Persons with SCI risk fracture and joint dislocation of the lower extremities and serious injury to the upper extremities. The former might be caused by asynergistic movement of spastic limbs against co-contractive forces imposed by electrical stimulation of paralyzed muscles, or by inertia developed by devices used for exercise.245 This explains why these activities are contraindicated for individuals having severe spasticity when at rest, or uncontrolled spastic responses when electrical current is introduced. Precautions to prevent overuse injuries of the arms and shoulders are essential for those participating in upper extremity exercise.138,246,247 As the shoulder joints are mechanically ill-suited to perform locomotor activities, but must do so in individuals using a manual wheelchair for transportation, these injuries may ultimately compromise performance of essential daily activities including wheelchair propulsion, weight relief, and depression transfers.248,249

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Thermal Dysregulation

Loss of sublesional vasomotor and sudomotor control after SCI poses a special challenge to temperature regulation during exercise, and often results in hyperther-mia.106,205,250,251 Hyperthermia is more pronounced in persons with higher level injuries,252,253 and when exercising in a hot, humid environment.251,254 Thus, attention should be paid to clothing, hydration, limiting the duration and intensity of activities performed in intemperate environments.

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Pain as a Common Problem After SCI

Both nociceptive and neuropathic pain are highly prevalent after SCI. Upper limb pain is the most common symptom of physical dysfunction reported by those with SCI,37,255–257 and the shoulder the most common site for pain.258,259 It is also the location for commonly experienced rotator cuff dysfunction and tears, and impingement.35,260 A large segment of the paralyzed population lives with pain in the shoulders, arms and wrists, with complaints reported in 35%261 to 73%257 of persons with chronic paraplegia. These figures cause special concern because onset of pain occurs earlier than observed in persons without disability, and as pain from muscle and joint overuse worsens with passing time and advancing age.255 Upper limb pain must be prevented if function is to be enhanced by exercise and incipient disability avoided.

While a single cause for shoulder pain has not been identified, many studies attribute pain to deterioration and injury resulting from insufficient shoulder strength, range, and muscle endurance.138,246,259,262 Pain that accompanies wheelchair locomotion and other wheelchair activities interferes with functional performance including upper extremity weight bearing for transfers, high resistance muscular activity in extremes of limb range, wheelchair propulsion up inclines, and frequent overhead activity.263–265 Wheelchair propulsion and transfers requiring shoulder girdle depression cause the most pain and increase the intensity of existing pain more than other daily activities.266 As many as half of persons with SCI experience significant shoulder pain intensified by wheelchair propulsion and body transfers,263 which represent activities critical to activity and health maintenance. The severity of upper limb pain increases during common transfer activities and increases as time following injury lengthens,255 although exercises focusing on the posterior shoulder and upper back appear to lessen the pain.138

Persons with paraplegia must depend on their upper extremities for transportation, body transfers, and other activities. Thus, the consequences and necessary treatments for shoulder pain and injury ultimately dictate the degree of their independence. While some report that surgical repair of the shoulder results in full recovery of musculoskeletal function and remedy of pain,267 others report not.258 Regardless, upper extremity surgery would require special postoperative and rehabilitative convalescent strategies, and deny personal independence in performing many essential daily functions. These factors make injury prevention an essential part in planning for exercise by those with SCI.

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CONCLUSIONS

Many persons with SCI already benefit from a lifestyle that incorporates habitual physical activity. Despite special needs, equipment, qualifications and risks, evidence collected across the spectrum of available training modes supports the ability of exercise to reduce multisystem disease in persons with SCI. Evidence further suggests that habitual exercise reduces fatigue, pain, weakness, musculoskeletal decline, and incipient neurological deficits that accompany aging with disability. Because these deficits challenge the ability of those with SCI to perform essential daily activities first mastered after injury, their prevention likely fosters fullest health and life satisfaction when aging with a disability. Thus, health care professionals should encourage persons with SCI to adopt or continue their use of therapeutic or recreational exercise as a health-enhancing strategy after SCI. Risks of injury associated with imprudent exercise must be managed to ensure that physical activity and daily activities can be sustained without interruption. If carefully prescribed, exercise has the demonstrated ability to enhance the activity, life satisfaction, and health of those with disability from SCI.

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Keywords:

exercise; SCI; fitness

© 2005 Neurology Section, APTA

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