Nash, Mark S. PhD, FACSM
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.
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
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
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
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
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.
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
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
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.
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
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
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.
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.
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.
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.
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
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
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.
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.
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.
1 DeVivo MJ, Black KJ, Stover SL. Causes of death during the first 12 years after spinal cord injury. Arch Phys Med Rehabil. 1993;74:248–254.
2 DeVivo MJ, Go BK, Jackson AB. Overview of the national spinal cord injury statistical center database. J Spinal Cord Med. 2002;25:335–338.
3 Hughes JT. The Edwin Smith Surgical Papyrus: an analysis of the first case reports of spinal cord injuries. Paraplegia. 1988;26:71–82.
4 Nash MS, Horton JA. Recreational and therapeutic exercise after SCI. In: Kirshbaum S, Campagnolo DI, DeLisa JS. Spinal Cord Injury Medicine. Philadelphia., Pa: Lippincott, Williams, and Wilkins; 2002:331–337.
5 DeVivo MJ, Rutt RD, Black KJ, Go BK, Stover SL. Trends in spinal cord injury demographics and treatment outcomes between 1973 and 1986. Arch Phys Med Rehabil. 1992;73:424–430.
6 DeVivo MJ, Shewchuk RM, Stover SL, Black KJ, Go BK. A cross-sectional study of the relationship between age and current health status for persons with spinal cord injuries. Paraplegia. 1992;30:820–827.
7 Dearwater SR, LaPorte RE, Robertson RJ, Brenes G, Adams LL, Becker D. Activity in the spinal cord-injured patient: an epidemiologic analysis of metabolic parameters. Med Sci Sports Exerc. 1986;18:541–544.
8 Noreau L, Shephard RJ, Simard C, Pare G, Pomerleau P. Relationship of impairment and functional ability to habitual activity and fitness following spinal cord injury. Int J Rehabil Res. 1993;16:265–275.
9 Washburn RA, Figoni SF. Physical activity and chronic cardiovascular disease prevention in spinal cord injury: a comprehensive literature review. Top Spinal Cord Injury Rehabil. 1998;3:16–32.
10 Bloomfield SA, Mysiw WJ, Jackson RD. Bone mass and endocrine adaptations to training in spinal cord injured individuals. Bone. 1996;19:61–68.
11 Demirel G, Yilmaz H, Paker N, Onel S. Osteoporosis after spinal cord injury. Spinal Cord. 1998;36:822–825.
12 Shields RK. Muscular, skeletal, and neural adaptations following spinal cord injury. J Orthop Sports Phys Ther. 2002;32:65–74.
13 Hjeltnes N, Jansen T. Physical endurance capacity, functional status and medical complications in spinal cord injured subjects with long-standing lesions. Paraplegia. 1990;28:428–432.
14 Kocina P. Body composition of spinal cord injured adults. Sports Med. 1997;23:48–60.
15 Gerhart KA, Bergstrom E, Charlifue SW, Menter RR, Whiteneck GG. Long-term spinal cord injury: functional changes over time. Arch Phys Med Rehabil. 1993;74:1030–1034.
16 Bauman WA, Spungen AM, Adkins RH, Kemp BJ. Metabolic and endocrine changes in persons aging with spinal cord injury. Assist Technol. 1999;11:88–96.
17 Nash MS. Exercise reconditioning of the heart and peripheral circulation after spinal cord injury. Top Spinal Cord Inj Rehabil. 1997;3:1–15.
18 Segatore M. The skeleton after spinal cord injury. Part 2: management of sublesional osteoporosis. SCI Nurs. 1995;12:115–120.
19 Segatore M. The skeleton after spinal cord injury. Part 1. Theoretical aspects. SCI Nurs. 1995;12:82–86.
20 Nash MS. Immune dysfunction and illness susceptibility after spinal cord injury: an overview of probable causes, likely consequences, and potential treatments. J Spinal Cord Med. 2000;23:109–110.
21 Nash MS. Known and plausible modulators of depressed immune functions following spinal cord injuries. J Spinal Cord Med. 2000;23:111–120.
22 Bostom AG, Toner MM, McArdle WD, Montelione T, Brown CD, Stein RA. Lipid and lipoprotein profiles relate to peak aerobic power in spinal cord injured men. Med Sci Sports Exerc. 1991;23:409–414.
23 Ohry A, Shemesh Y, Rozin R. Are chronic spinal cord injured patients (SCIP) prone to premature aging? Med Hypotheses. 1983;11:467–469.
24 Bauman WA, Spungen AM. Metabolic changes in persons after spinal cord injury. Phys Med Rehabil Clin N Am. 2000;11:109–140.
25 Phillips WT, Kiratli BJ, Sarkarati M, et al. Effect of spinal cord injury on the heart and cardiovascular fitness. Curr Probl Cardiol. 1998;23:641–716.
26 Hopman MT, Monroe M, Dueck C, Phillips WT, Skinner JS. Blood redistribution and circulatory responses to submaximal arm exercise in persons with spinal cord injury. Scand J Rehabil Med. 1998;30:167–174.
27 Jacobs PL, Mahoney ET, Robbins A, Nash M. Hypokinetic circulation in persons with paraplegia. Med Sci Sports Exerc. 2002;34:1401–1407.
28 Hjeltnes N. Oxygen uptake and cardiac output in graded arm exercise in paraplegics with low level spinal lesions. Scand J Rehabil Med. 1977;9:107–113.
29 Duckworth WC, Solomon SS, Jallepalli P, Heckemeyer C, Finnern J, Powers A. Glucose intolerance due to insulin resistance in patients with spinal cord injuries. Diabetes. 1980;29:906–910.
30 Karlsson AK. Insulin resistance and sympathetic function in high spinal cord injury. Spinal Cord. 1999; 37:494–500.
31 Karlsson AK, Attvall S, Jansson PA, Sullivan L, Lonnroth P. Influence of the sympathetic nervous system on insulin sensitivity and adipose tissue metabolism: a study in spinal cord-injured subjects. Metabolism. 1995;44:52–58.
32 Rodriguez GP, Claus-Walker J, Kent MC, Garza HM. Collagen metabolite excretion as a predictor of bone-and skin-related complications in spinal cord injury. Arch Phys Med Rehabil. 1989;70:442–444.
33 Segatore M. The skeleton after spinal cord injury. Part 2: management of sublesional osteoporosis. SCI Nurs. 1995;12:115–120.
34 Nash MS, Tehranzadeh J, Green BA, Rountree MT, Shea JD. Magnetic resonance imaging of osteonecrosis and osteoarthrosis in exercising quadriplegics and paraplegics. Am J Phys Med Rehabil. 1994;73:184–192.
35 Lal S. Premature degenerative shoulder changes in spinal cord injury patients. Spinal Cord. 1998;36:186–189.
36 Levi R, Hultling C, Nash MS, Seiger A. The Stockholm spinal cord injury study: 1. Medical problems in a regional SCI population. Paraplegia. 1995;33:308–315.
37 Sie IH, Waters RL, Adkins RH, Gellman H. Upper extremity pain in the postrehabilitation spinal cord injured patient. Arch Phys Med Rehabil. 1992;73:44–48.
38 Widerstrom-Noga EG, Turk DC. Types and effectiveness of treatments used by people with chronic pain associated with spinal cord injuries: influence of pain and psychosocial characteristics. Spinal Cord. 2003;41:600–609.
39 Widerstrom-Noga EG, Felipe-Cuervo E, Yezierski R P. Relationships among clinical characteristics of chronic pain after spinal cord injury. Arch Phys Med Rehabil. 2001;82:1191–1197.
40 King ML, Lichtman SW, Pellicone JT, Close RJ, Lisanti P. Exertional hypotension in spinal cord injury. Chest. 1994;106:1166–1171.
41 Lopes P, Figoni SF, Perkash I. Upper limb exercise effect on tilt tolerance during orthostatic training of patients with spinal cord injury. Arch Phys Med Rehabil. 1984; 65:251–253.
42 Figoni SF. Perspectives on cardiovascular fitness and SCI. J Am Paraplegia Soc. 1990;13:63–71.
43 Figoni SF. Cardiovascular and haemodynamic responses to tilting and to standing in tetraplegic patients: a review. Paraplegia. 1984;22:99–109.
44 Kessler KM, Pina I, Green B, et al. Cardiovascular findings in quadriplegic and paraplegic patients and in normal subjects. Am J Cardiol. 1986;58:525–530.
45 Nash MS, Bilsker MS, Kearney HM, Ramirez JN, Applegate B, Green BA. Effects of electrically-stimulated exercise and passive motion on echocardiographically-derived wall motion and cardiodynamic function in tetraplegic persons. Paraplegia. 1995;33:80–89.
46 Davis GM. Exercise capacity of individuals with paraplegia. Med Sci Sports Exerc. 1993;25:423–432.
47 Nash MS, Bilsker S, Marcillo AE, et al. Reversal of adaptive left ventricular atrophy following electrically-stimulated exercise training in human tetraplegics. Paraplegia. 1991;29:590–599.
48 Hopman MT. Circulatory responses during arm exercise in individuals with paraplegia. Int J Sports Med. 1994; 15:126–131.
49 Hopman MT, van Asten WN, Oeseburg B. Changes in blood flow in the common femoral artery related to inactivity and muscle atrophy in individuals with longstanding paraplegia. Adv Exp Med Biol. 1996;388:379–383.
50 Nash MS, Montalvo BM, Applegate B. Lower extremity blood flow and responses to occlusion ischemia differ in exercise-trained and sedentary tetraplegic persons. Arch Phys Med Rehabil. 1996;77:1260–1265.
51 Taylor PN, Ewins DJ, Fox B, Grundy D, Swain ID. Limb blood flow, cardiac output and quadriceps muscle bulk following spinal cord injury and the effect of training for the Odstock functional electrical stimulation standing system. Paraplegia. 1993;31:303–310.
52 Davis GM, Shephard RJ. Cardiorespiratory fitness in highly active versus inactive paraplegics. Med Sci Sports Exerc. 1988;20:463–468.
53 Green D, Hull RD, Mammen EF, Merli GJ, Weingarden SI, Yao JS. Deep vein thrombosis in spinal cord injury. Summary and recommendations. Chest. 1992;102:633S-635S.
54 Boudaoud L, Roussi J, Lortat-Jacob S, Bussel B, Dizien O, Drouet L. Endothelial fibrinolytic reactivity and the risk of deep venous thrombosis after spinal cord injury. Spinal Cord. 1997;35:151–157.
55 Jacobs PL, Mahoney ET, Robbins A, Nash M. Hypokinetic circulation in persons with paraplegia. Med Sci Sports Exerc. 2002;34:1401–1407.
56 Nash MS, Montalvo BM, Applegate B. Lower extremity blood flow and responses to occlusion ischemia differ in exercise-trained and sedentary tetraplegic persons. Arch Phys Med Rehabil. 1996;77:1260–1265.
57 Winther K, Gleerup G, Snorrason K, Biering-Sorensen F. Platelet function and fibrinolytic activity in cervical spinal cord injured patients. Thromb Res. 1992;65:469–474.
58 Le CT. Survival from spinal cord injury. J Chron Dis. 1982;35:487–492.
59 Whiteneck GG, Charlifue SW, Frankel HL, et al. Mortality, morbidity, and psychosocial outcomes of persons spinal cord injured more than 20 years ago. Paraplegia. 1992;30:617–630.
60 Bauman WA, Spungen AM, Raza M, et al. Coronary arter y disease: metabolic risk factors and latent disease in individuals with paraplegia. Mt Sinai J Med. 1992;59:163–168.
61 Bauman WA, Kahn NN, Grimm DR, Spungen AM. Risk factors for atherogenesis and cardiovascular autonomic function in persons with spinal cord injury. Spinal Cord. 1999;37:601–616.
62 Bauman WA, Raza M, Spungen AM, Machac J. Cardiac stress testing with thallium-201 imaging reveals silent ischemia in individuals with paraplegia. Arch Phys Med Rehabil. 1994;75:946–950.
63 Groah SL, Menter RR. Long-term cardiac ischemia leading to coronary artery bypass grafting in a tetraplegic patient. Arch Phys Med Rehabil. 1998;79:1129–1132.
64 Bauman WA, Spungen AM. Disorders of carbohydrate and lipid metabolism in veterans with paraplegia or quadriplegia: a model of premature aging. Metabolism. 1994;43:749–756.
65 Nash MS, Jacobs PL, Mendez AJ, Goldberg RB. Circuit resistance training improves the atherogenic lipid profiles of persons with chronic paraplegia. J Spinal Cord Med. 2001;24:2–9.
66 Karlsson AK, Attvall S, Jansson PA, Sullivan L, Lonnroth P. Influence of the sympathetic nervous system on insulin sensitivity and adipose tissue metabolism: a study in spinal cord-injured subjects. Metabolism. 1995;44:52–58.
67 Maki KC, Briones ER, Langbein WE, et al. Associations between serum lipids and indicators of adiposity in men with spinal cord injury. Paraplegia. 1995;33:102–109.
68 Zlotolow SP, Levy E, Bauman WA. The serum lipoprotein profile in veterans with paraplegia: the relationship to nutritional factors and body mass index. J Am Paraplegia Soc. 1992;15:158–162.
69 Bauman WA, Adkins RH, Spungen AM, et al. Is immobilization associated with an abnormal lipoprotein profile? Observations from a diverse cohort. Spinal Cord. 1999;37:485–493.
70 Zlotolow SP, Levy E, Bauman WA. The serum lipoprotein profile in veterans with paraplegia: the relationship to nutritional factors and body mass index. J Am Paraplegia Soc. 1992;15:158–162.
71 Karlsson AK, Attvall S, Jansson PA, Sullivan L, Lonnroth P. Influence of the sympathetic nervous system on insulin sensitivity and adipose tissue metabolism: a study in spinal cord-injured subjects. Metabolism. 1995;44:52–58.
72 Maki KC, Briones ER, Langbein WE, et al. Associations between serum lipids and indicators of adiposity in men with spinal cord injury. Paraplegia. 1995;33:102–109.
73 Washburn RA, Figoni SF. High density lipoprotein cholesterol in individuals with spinal cord injury: the potential role of physical activity. Spinal Cord. 1999; 37:685–695.
74 Zhong YG, Levy E, Bauman WA. The relationships among serum uric acid, plasma insulin, and serum lipoprotein levels in subjects with spinal cord injury. Horm Metab Res. 1995;27:283–286.
75 Grundy SM. Atherogenic dyslipidemia: lipoprotein abnormalities and implications for therapy. Am J Cardiol. 1995;75:45B–52B.
76 Noreau L, Shephard RJ. Spinal cord injury, exercise and quality of life. Sports Med. 1995;20:226–250.
77 Aksnes AK, Hjeltnes N, Wahlstrom EO, Katz A, Zierath JR, Wallberg-Henriksson H. Intact glucose transport in morphologically altered denervated skeletal muscle from quadriplegic patients. Am J Physiol. 1996;271:E593-E600.
78 Jones LM, Goulding A, Gerrard DF. DEXA: a practical and accurate tool to demonstrate total and regional bone loss, lean tissue loss and fat mass gain in paraplegia. Spinal Cord. 1998;36:637–640.
79 Spungen AM, Bauman WA, Wang J, Pierson RN Jr. Measurement of body fat in individuals with tetraplegia: a comparison of eight clinical methods. Paraplegia. 1995;33:402–408.
80 Kuhne S, Hammon HM, Bruckmaier RM, Morel C, Zbinden Y, Blum JW. Growth performance, metabolic and endocrine traits, and absorptive capacity in neonatal calves fed either colostrum or milk replacer at two levels. J Anim Sci. 2000;78:609–620.
81 Ragnarsson KT. The Cardiovascular System. In: Aging with Spinal Cord Injury. New Yo rk, NY: 1993:73–92.
82 Ohry A, Shemesh Y, Rozin R. Are chronic spinal cord injured patients (SCIP) prone to premature aging? Med Hypotheses. 1983;11:467–469.
83 Burstein R, Zeilig G, Royburt M, Epstein Y, Ohry A. Insulin resistance in paraplegics–effect of one bout of acute exercise. Int J Sports Med. 1996;17:272–276.
84 Karlsson AK. Insulin resistance and sympathetic function in high spinal cord injury. Spinal Cord. 1999;37:494–500.
85 Cominacini L, Zocca I, Garbin U, et al. High-density lipoprotein composition in obesity: interrelationships with plasma insulin levels and body weight. Int J Obes. 1988;12:343–352.
86 Hashimoto R, Adachi H, Tsuruta M, Tashiro H, Toshima H. Association of hyperinsulinemia and serum free fatty acids with serum high density lipoprotein-cholesterol. J Atheroscler Thromb. 1995;2:53–59.
87 Jeppesen J, Facchini FS, Reaven GM. Individuals with high total cholesterol/HDL cholesterol ratios are insulin resistant. J Intern Med. 1998;243:293–298.
88 Gerrits HL, de Haan A, Sargeant AJ, Dallmeijer A, Hopman MT. Altered contractile properties of the quadriceps muscle in people with spinal cord injury following functional electrical stimulated cycle training. Spinal Cord. 2000;38:214–223.
89 Levy M, Mizrahi J, Susak Z. Recruitment, force and fatigue characteristics of quadriceps muscles of paraplegics isometrically activated by surface functional electrical stimulation. J Biomed Eng. 1990;12:150–156.
90 Burnham R, Martin T, Stein R, Bell G, MacLean I, Steadward R. Skeletal muscle fibre type transformation following spinal cord injury. Spinal Cord. 1997;35:86–91.
91 Castro MJ, Apple DF Jr, Staron RS, Campos GE, Dudley GA. Influence of complete spinal cord injury on skeletal muscle within 6 mo of injury. J Appl Physiol. 1999; 86:350–358.
92 Castro MJ, Apple DF Jr, Hillegass EA, Dudley GA. Influence of complete spinal cord injury on skeletal muscle cross-sectional area within the first 6 months of injury. Eur J Appl Physiol Occup Physiol. 1999;80:373–378.
93 Greve JM, Muszkat R, Schmidt B, Chiovatto J, Barros Filho TE, Batisttella LR. Functional electrical stimulation (FES): muscle histochemical analysis. Paraplegia. 1993;31:764–770.
94 Grimby G, Broberg C, Krotkiewska I, Krotkiewski M. Muscle fiber composition in patients with traumatic cord lesion. Scand J Rehabil Med. 1976;8:37–42.
95 Rochester L, Chandler CS, Johnson MA, Sutton RA, Miller S. Influence of electrical stimulation of the tibialis anterior muscle in paraplegic subjects. 1. Contractile properties. Paraplegia. 1995;33:437–449.
96 Andersen JL, Mohr T, Biering-Sorensen F, Galbo H, Kjaer M. Myosin heavy chain isoform transformation in single fibres from m. vastus lateralis in spinal cord injured individuals: effects of long-term functional electrical stimulation (FES). Pflugers Arch. 1996;431:513–518.
97 Lotta S, Scelsi R, Alfonsi E, et al. Morphometric and neurophysiological analysis of skeletal muscle in paraplegic patients with traumatic cord lesion. Paraplegia. 1991; 29:247–252.
98 Scelsi R, Marchetti C, Poggi P, Lotta S, Lommi G. Muscle fiber type morphology and distribution in paraplegic patients with traumatic cord lesion. Histochemical and ultrastructural aspects of rectus femoris muscle. Acta Neuropathol (Berl). 1982;57:243–248.
99 Talmadge RJ, Castro MJ, Apple DF Jr, Dudley GA. Phenotypic adaptations in human muscle fibers 6 and 24 wk after spinal cord injury. J Appl Physiol. 2002; 92:147–154.
100 Talmadge RJ, Roy RR, Bodine-Fowler SC, Pierotti DJ, Edgerton VR. Adaptations in myosin heavy chain profile in chronically unloaded muscles. Basic Appl Myol. 1995;5:117–137.
101 Shields RK. Fatigability, relaxation properties, and electromyographic responses of the human paralyzed soleus muscle. J Neurophysiol. 1995;73:2195–2206.
102 Rochester L, Barron MJ, Chandler CS, Sutton RA, Miller S, Johnson MA. Influence of electrical stimulation of the tibialis anterior muscle in paraplegic subjects. 2. Morphological and histochemical properties. Paraplegia. 1995;33:514–522.
103 Priebe MM, Sherwood AM, Thornby JI, Kharas N F, Markowski J. Clinical assessment of spasticity in spinal cord injury: a multidimensional problem. Arch Phys Med Rehabil. 1996;77:713–716.
104 McKinley WO, Jackson AB, Cardenas DD, DeVivo MJ. Long-term medical complications after traumatic spinal cord injury: a regional model systems analysis. Arch Phys Med Rehabil. 1999;80:1402–1410.
105 Norton JA, Wood DE, Marsden JF, Day BL. Spinally generated electromyographic oscillations and spasms in a low-thoracic complete paraplegic. Mov Disord. 2003; 18:101–106.
106 Sawka MN, Latzka WA, Pandolf KB. Temperature regulation during upper body exercise: able-bodied and spinal cord injured. Med Sci Sports Exerc. 1989;21:S132-S140.
107 Hopman MT, Oeseburg B, Binkhorst RA. Cardiovascular responses in persons with paraplegia to prolonged arm exercise and thermal stress. Med Sci Sports Exerc. 1993;25:577–583.
108 Hjeltnes N. Cardiorespiratory capacity in tetra- and paraplegia shortly after injury. Scand J Rehabil Med. 1986;18:65–70.
109 Hooker SP, Greenwood JD, Hatae DT, Husson R P, Matthiesen TL, Waters AR. Oxygen uptake and heart rate relationship in persons with spinal cord injury. Med Sci Sports Exerc. 1993;25:1115–1119.
110 Hopman MT, Oeseburg B, Binkhorst RA. Cardiovascular responses in paraplegic subjects during arm exercise. Eur J Appl Physiol. 1992;65:73–78.
111 Hopman MT, Kamerbeek IC, Pistorius M, Binkhorst RA. The effect of an anti-G suit on the maximal performance of individuals with paraplegia. Int J Sports Med. 1993;14:357–361.
112 Van Loan MD, McCluer S, Loftin JM, Boileau RA. Comparison of physiological responses to maximal arm exercise among able-bodied, paraplegics and quadriplegics. Paraplegia. 1987;25:397–405.
113 Houtman S, Thielen JJ, Binkhorst RA, Hopman MT. Effect of a pulsating anti-gravity suit on peak exercise performance in individual with spinal cord injuries. Eur J Appl Physiol. 1999;79:202–204.
114 Hjeltnes N. Oxygen uptake and cardiac output in graded arm exercise in paraplegics with low level spinal lesions. Scand J Rehab Med. 1979;9:107–113.
115 Bloomfield SA, Jackson RD, Mysiw WJ. Catecholamine response to exercise and training in individuals with spinal cord injury. Med Sci Sports Exerc. 1994;26:1213–1219.
116 Schmid A, Huonker M, Barturen JM, et al. Catecholamines, heart rate, and oxygen uptake during exercise in persons with spinal cord injury. J Appl Physiol. 1998; 85:635–641.
117 Schmid A, Huonker M, Stahl F, et al. Free plasma catecholamines in spinal cord injured persons with different injury levels at rest and during exercise. J Auton Nerv Syst. 1998;68:96–100.
118 Bloomfield SA, Jackson RD, Mysiw WJ. Catecholamine response to exercise and training in individuals with spinal cord injury. Med Sci Sports Exerc. 1994;26:1213–1219.
119 Hoffman MD. Cardiorespiratory fitness and training in quadriplegics and paraplegics. Sports Med. 1986;3:312–330.
120 Curtis KA, McClanahan S, Hall KM, Dillon D, Brown K F. Health, vocational, and functional status in spinal cord injured athletes and nonathletes. Arch Phys Med Rehabil. 1986;67:862–865.
121 Davis R, Houdayer T, Andrews B, Emmons S, Patrick J. Paraplegia: prolonged closed-loop standing with implanted nucleus FES-22 stimulator and Andrews' foot-ankle orthosis. Stereotact Funct Neurosurg. 1997; 69:281–287.
122 Klose KJ, Jacobs PL, Broton JG, et al. Evaluation of a training program for persons with SCI paraplegia using the Parastep 1 ambulation system: part 1. Ambulation performance and anthropometric measures. Arch Phys Med Rehabil. 1997;78:789–793.
123 Triolo RJ, Bieri C, Uhlir J, Kobetic R, Scheiner A, Marsolais EB. Implanted Functional Neuromuscular Stimulation systems for individuals with cervical spinal cord injuries: clinical case reports. Arch Phys Med Rehabil. 1996;77:1119–1128.
124 Glaser RM. Functional neuromuscular stimulation. Exercise conditioning of spinal cord injured patients. Int J Sports Med. 1994;15:142–148.
125 Ragnarsson KT. Physiologic effects of functional electrical stimulation-induced exercises in spinal cord-injured individuals. Clin Orthop. 1988;53–63.
126 Cowell LL, Squires WG, Raven PB. Benefits of aerobic exercise for the paraplegic: a brief review. Med Sci Sports Exerc. 1986;18:501–508.
127 Davis GM, Kofsky PR, Kelsey JC, Shephard RJ. Cardiorespiratory fitness and muscular strength of wheelchair users. Can Med Assoc J. 1981;125:1317–1323.
128 Franklin BA. Exercise testing, training and arm ergome-try. Sports Med. 1985;2:100–119.
129 Gass GC, Watson J, Camp EM, Court HJ, McPherson LM, Redhead P. The effects of physical training on high level spinal lesion patients. Scand J Rehabil Med. 1980;12:61–65.
130 Hooker SP, Wells CL. Effects of low- and moderate-intensity training in spinal cord-injured persons. Med Sci Sports Exerc. 1989;21:18–22.
131 Taylor AW, McDonell E, Brassard L. The effects of an arm ergometer training programme on wheelchair subjects. Paraplegia. 1986;24:105–114.
132 Yim SY, Cho KJ, Park CI, et al. Effect of wheelchair ergometer training on spinal cord-injured paraplegics. Yonsei Med J. 1993;34:278–286.
133 DiCarlo SE. Effect of arm ergometry training on wheelchair propulsion endurance of individuals with quadriplegia. Phys Ther. 1988;68:40–44.
134 Drory Y, Ohry A, Brooks ME, Dolphin D, Kellermann JJ. Arm crank ergometry in chronic spinal cord injured patients. Arch Phys Med Rehabil. 1990;71:389–392.
135 Nilsson S, Staff PH, Pruett ED. Physical work capacity and the effect of training on subjects with long-standing paraplegia. Scand J Rehabil Med. 1975;7:51–56.
136 Davis GM, Shephard RJ. Strength training for wheelchair users. Br J Sports Med. 1990;24:25–30.
137 Cooney MM, Walker JB. Hydraulic resistance exercise benefits cardiovascular fitness of spinal cord injured. Med Sci Sports Exerc. 1986;18:522–525.
138 Curtis KA, Tyner TM, Zachary L, et al. Effect of a standard exercise protocol on shoulder pain in long-term wheelchair users. Spinal Cord. 1999;37:421–429.
139 Gettman LR, Ayres JJ, Pollock ML, Jackson A. The effect of circuit weight training on strength, cardiorespiratory function, and body composition of adult men. Med Sci Sports. 1978;10:171–176.
140 Jacobs PL, Nash MS, Rusinowski JW. Circuit training provides cardiorespiratory and strength benefits in persons with paraplegia. Med Sci Sports Exerc. 2001;33:711–717.
141 Nash MS, Jacobs PL, Woods JM, Clark JE, Pray TA, Pumarejo AE. A comparison of 2 circuit exercise training techniques for eliciting matched metabolic responses in persons with paraplegia. Arch Phys Med Rehabil. 2002;83:201–209.
142 Crago PE, Mortimer JT, Peckham PH. Closed-loop control of force during electrical stimulation of muscle. IEEE Trans Biomed Eng. 1980;27:306–312.
143 Dudley GA, Castro MJ, Rogers S, Apple DF Jr. A simple means of increasing muscle size after spinal cord injury: a pilot study. Eur J Appl Physiol Occup Physiol. 1999;80:394–396.
144 Figoni SF, Glaser RM, Rodgers MM, et al. Acute hemodynamic responses of spinal cord injured individuals to functional neuromuscular stimulation-induced knee extension exercise. J Rehabil Res Dev. 1991;28:9–18.
145 Rodgers MM, Glaser RM, Figoni SF, et al. Musculoskeletal responses of spinal cord injured individuals to functional neuromuscular stimulation-induced knee extension exercise training. J Rehabil Res Dev. 1991;28:19–26.
146 Gruner JA, Glaser RM, Feinberg SD, Collins SR, Nussbaum NS. A system for evaluation and exercise-conditioning of paralyzed leg muscles. J Rehabil R D. 1983;20:21–30.
147 Bryden AM, Memberg WD, Crago PE. Electrically stimulated elbow extension in persons with C5/C6 tetraplegia: a functional and physiological evaluation. Arch Phys Med Rehabil. 2000;81:80–88.
148 Billian C, Gorman PH. Upper extremity applications of functional neuromuscular stimulation. Assist Technol. 1992;4:31–39.
149 Klefbeck B, Mattsson E, Weinberg J. The effect of trunk support on performance during arm ergometry in patients with cervical cord injuries. Paraplegia. 1996;34:167–172.
150 Scremin AM, Kurta L, Gentili A, et al. Increasing muscle mass in spinal cord injured persons with a functional electrical stimulation exercise program. Arch Phys Med Rehabil. 1999;80:1531–1536.
151 Glaser RM. Exercise and locomotion for the spinal cord injured. Exerc Sport Sci Rev. 1985;13:263–303.
152 Hooker SP, Figoni SF, Glaser RM, Rodgers MM, Ezenwa BN, Faghri PD. Physiologic responses to prolonged electrically stimulated leg-cycle exercise in the spinal cord injured. Arch Phys Med Rehabil. 1990;71:863–869.
153 Ragnarsson KT, Pollack S, O'Daniel W Jr, Edgar R, Petrofsky J, Nash MS. Clinical evaluation of computerized functional electrical stimulation after spinal cord injury: a multicenter pilot study. Arch Phys Med Rehabil. 1988;69:672–677.
154 Raymond J, Davis GM, Climstein M, Sutton JR. Cardiorespiratory responses to arm cranking and electrical stimulation leg cycling in people with paraplegia. Med Sci Sports Exerc. 1999;31:822–828.
155 Krauss JC, Robergs RA, Depaepe JL, et al. Effects of electrical stimulation and upper body training after spinal cord injury. Med Sci Sports Exerc. 1993;25:1054–1061.
156 Mutton DL, Scremin AM, Barstow TJ, Scott MD, Kunkel CF, Cagle TG. Physiologic responses during functional electrical stimulation leg cycling and hybrid exercise in spinal cord injured subjects. Arch Phys Med Rehabil. 1997;78:712–718.
157 Phillips W, Burkett LN. Arm crank exercise with static leg FNS in persons with spinal cord injury. Med Sci Sports Exerc. 1995;27:530–535.
158 Laskin JJ, Ashley EA, Olenik LM, et al. Electrical stimulation-assisted rowing exercise in spinal cord injured people. A pilot study. Paraplegia. 1993;31:534–541.
159 Cameron T, Broton JG, Needham-Shropshire B, Klose KJ. An upper body exercise system incorporating resistive exercise and neuromuscular electrical stimulation (NMS). J Spinal Cord Med. 1998;21:1–6.
160 Needham-Shropshire BM, Broton JG, Cameron TL, Klose KJ. Improved motor function in tetraplegics following neuromuscular stimulation-assisted arm ergometry. J Spinal Cord Med. 1997;20:49–55.
161 Mulcahey MJ, Betz RR, Smith BT, Weiss AA, Davis SE. Implanted functional electrical stimulation hand system in adolescents with spinal injuries: an evaluation. Arch Phys Med Rehabil. 1997;78:597–607.
162 Phillips CA. Functional electrical stimulation and lower extremity bracing for ambulation exercise of the spinal cord injured individual: a medically prescribed system. Phys Ther. 1989;69:842–849.
163 Moynahan M, Mullin C, Cohn J, et al. Home use of a functional electrical stimulation system for standing and mobility in adolescents with spinal cord injury. Arch Phys Med Rehabil. 1996;77:1005–1013.
164 Thoumie P, Le Claire G, Beillot J, et al. Restoration of functional gait in paraplegic patients with the RGO-II hybrid orthosis. A multicenter controlled study. II: Physiological evaluation. Paraplegia. 1995;33:654–659.
165 Brissot R, Gallien P, Le Bot MP, et al. Clinical experience with functional electrical stimulation-assisted gait with Parastep in spinal cord-injured patients. Spine. 2000;25:501–508.
166 Klose KJ, Jacobs PL, Broton JG, et al. Evaluation of a training program for persons with SCI paraplegia using the Parastep 1 ambulation system: part 1. Ambulation performance and anthropometric measures. Arch Phys Med Rehabil. 1997;78:789–793.
167 Phillips CA. Medical criteria for active physical therapy. Physician guidelines for patient participation in a program of functional electrical rehabilitation. Am J Phys Med. 1987;66:269–286.
168 Graupe D, Kohn KH. Functional neuromuscular stimulator for short-distance ambulation by certain thoracic-level spinal-cord-injured paraplegics. Surg Neurol. 1998;50:202–207.
169 Phillips CA, Gallimore JJ, Hendershot DM. Walking when utilizing a sensory feedback system and an electrical muscle stimulation gait orthosis. Med Eng Phys. 1995;17:507–513.
170 Peckham PH, Creasey GH. Neural prostheses: clinical applications of functional electrical stimulation in spinal cord injury. Paraplegia. 1992;30:96–101.
171 Scott TR, Peckham PH, Keith MW. Upper extremity neuroprostheses using functional electrical stimulation. Baillieres Clin Neurol. 1995;4:57–75.
172 Dimitrijevic MM. Mesh-glove. 1. A method for whole-hand electrical stimulation in upper motor neuron dysfunction. Scand J Rehabil Med. 1994;26:183–186.
173 Mulcahey MJ, Smith BT, Betz RR. Evaluation of the lower motor neuron integrity of upper extremity muscles in high level spinal cord injury. Spinal Cord. 1999;37:585–591.
174 Graupe D. An overview of the state of the art of noninvasive FES for independent ambulation by thoracic level paraplegics. Neurol Res. 2002;24:431–442.
175 Petrofsky JS, Phillips CA. The use of functional electrical stimulation for rehabilitation of spinal cord injured patients. Cent Nerv Syst Trauma. 1984;1:57–74.
176 Hooker SP, Figoni SF, Rodgers MM, et al. Physiologic effects of electrical stimulation leg cycle exercise training in spinal cord injured persons. Arch Phys Med Rehabil. 1992;73:470–476.
177 Hooker SP, Scremin AM, Mutton DL, Kunkel CF, Cagle G. Peak and submaximal physiologic responses following electrical stimulation leg cycle ergometer training. J Rehabil Res Dev. 1995;32:361–366.
178 Barstow TJ, Scremin AM, Mutton DL, Kunkel CF, Cagle TG, Whipp BJ. Gas exchange kinetics during functional electrical stimulation in subjects with spinal cord injury. Med Sci Sports Exerc. 1995;27:1284–1291.
179 Barstow TJ, Scremin AM, Mutton DL, Kunkel CF, Cagle TG, Whipp BJ. Changes in gas exchange kinetics with training in patients with spinal cord injury. Med Sci Sports Exerc. 1996;28:1221–1228.
180 Gerrits HL, de Haan A, Sargeant AJ, van Langen H, Hopman MT. Peripheral vascular changes after electrically stimulated cycle training in people with spinal cord injury. Arch Phys Med Rehabil. 2001;82:832–839.
181 Schmidt-Trucksass A, Schmid A, Brunner C, et al. Arterial properties of the carotid and femoral artery in endurance-trained and paraplegic subjects. J Appl Physiol. 2000;89:1956–1963.
182 Nash MS, Jacobs PL, Montalvo BM, Klose KJ, Guest RS, Needham-Shropshire BM. Evaluation of a training program for persons with SCI paraplegia using the Parastep 1 ambulation system: part 5. Lower extremity blood flow and hyperemic responses to occlusion are augmented by ambulation training. Arch Phys Med Rehabil. 1997;78:808–814.
183 BeDell KK, Scremin AME, Perell KL, Kunkel CF. Effects of functional electrical stimulation-induced lower extremity cycling on bone density of spinal cord-injured patients. Am J Phys Med Rehabil. 1996;75:29–34.
184 Mohr T, Podenphant J, Biering-Sorensen F, Galbo H, Thamsborg G, Kjaer M. Increased bone mineral density after prolonged electrically induced cycle training of paralyzed limbs in spinal cord injured man. Calcif Tissue Int. 1997;61:22–25.
185 Leeds EM, Klose KJ, Ganz W, Serafini A, Green BA. Bone mineral density after bicycle ergometry training. Arch Phys Med Rehabil. 1990;71:207–209.
186 Nash MS, Tehranzadeh J, Green BA, Rountree MT, Shea JD. Magnetic resonance imaging of osteonecrosis and osteoarthrosis in exercising quadriplegics and paraplegics. Am J Phys Med Rehabil. 1994;73:184–192.
187 Hjeltnes N, Aksnes AK, Birkeland KI, Johansen J, Lannem A, Wallberg-Henriksson H. Improved body composition after 8 wk of electrically stimulated leg cycling in tetraplegic patients. Am J Physiol. 1997;273:R1072-R1079.
188 Hjeltnes N, Galuska D, Bjornholm M, et al. Exercise-induced overexpression of key regulatory proteins involved in glucose uptake and metabolism in tetra-plegic persons: molecular mechanism for improved glucose homeostasis. FASEB J. 1998;12:1701–1712.
189 Mohr T, Dela F, Handberg A, Biering-Sorensen F, Galbo H, Kjaer M. Insulin action and long-term electrically induced training in individuals with spinal cord injuries. Med Sci Sports Exerc. 2001;33:1247–1252.
190 Gallien P, Brissot R, Eyssette M, et al. Restoration of gait by functional electrical stimulation for spinal cord injured patients. Paraplegia. 1995;33:660–664.
191 Field-Fote EC. Combined use of body weight support, functional electric stimulation, and treadmill training to improve walking ability in individuals with chronic incomplete spinal cord injury. Arch Phys Med Rehabil. 2001;82:818–824.
192 Ladouceur M, Barbeau H. Functional electrical stimulation-assisted walking for persons with incomplete spinal injuries: changes in the kinematics and physiological cost of overground walking. Scand J Rehabil Med. 2000;32:72–79.
193 Stein RB, Belanger M, Wheeler G, et al. Electrical systems for improving locomotion after incomplete spinal cord injury: an assessment. Arch Phys Med Rehabil. 1993;74:954–959.
194 Klose KJ, Jacobs PL, Broton JG, et al. Evaluation of a training program for persons with SCI paraplegia using the Parastep 1 ambulation system: part 1. Ambulation performance and anthropometric measures. Arch Phys Med Rehabil. 1997;78:789–793.
195 Phillips CA, Gallimore JJ, Hendershot DM. Walking when utilizing a sensory feedback system and an electrical muscle stimulation gait orthosis. Med Eng Phys. 1995;17:507–513.
196 Jacobs PL, Nash MS. Modes, benefits, and risks of voluntary an delectrically induced exercise in persons with spinal cord injury. J Spinal Cord Med. 2001;24:10–18.
197 Jacobs PL, Nash MS, Klose KJ, Guest RS, Needham-Shropshire BM, Green BA. Evaluation of a training program for persons with SCI paraplegia using the Parastep 1 ambulation system: part 2. Effects on physiological responses to peak arm ergometry. Arch Phys Med Rehabil. 1997;78:794–798.
198 Jaeger RJ. Lower extremity applications of functional neuromuscular stimulation. Assist Technol. 1992;4:19–30.
199 Nash MS, Jacobs PL, Montalvo BM, Klose KJ, Guest RS, Needham-Shropshire BM. Evaluation of a training program for persons with SCI paraplegia using the Parastep 1 ambulation system: part 5. Lower extremity blood flow and hyperemic responses to occlusion are augmented by ambulation training. Arch Phys Med Rehabil. 1997;78:808–814.
200 Kessler KM, Pina I, Green B, et al. Cardiovascular findings in quadriplegic and paraplegic patients and in normal subjects. Am J Cardiol. 1986;58:525–530.
201 Nash MS, Bilsker MS, Kearney HM, Ramirez JN, Applegate B, Green BA. Effects of electrically-stimulated exercise and passive motion on echocardiographically-derived wall motion and cardiodynamic function in tetraplegic persons. Paraplegia. 1995;33:80–89.
202 Campagnolo DI, Bartlett JA, Keller SE. Influence of neurological level on immune function following spinal cord injury: a review. J Spinal Cord Med. 2000;23:121–128.
203 King ML, Freeman DM, Pellicone JT, Wanstall ER, Bhansali LD. Exertional hypotension in thoracic spinal cord injury: case report. Paraplegia. 1992;30:261–266.
204 Minaire P. Immobilization osteoporosis: a review. Clin Rheumatol. 1989;8 Suppl 2:95–103.
205 Gass GC, Camp EM, Nadel ER, Gwinn TH, Engel P. Rectal and rectal vs. esophageal temperatures in paraplegic men during prolonged exercise. J Appl Physiol. 1988; 64:2265–2271.
206 Hopman MT, Oeseburg B, Binkhorst RA. The effect of an anti-G suit on cardiovascular responses to exercise in persons with paraplegia. Med Sci Sports Exerc. 1992; 24:984–990.
207 Schmid A, Huonker M, Barturen JM, et al. Catecholamines, heart rate, and oxygen uptake during exercise in persons with spinal cord injury. J Appl Physiol. 1998; 85:635–641.
208 Franklin BA. Exercise testing, training and arm ergometry. Sports Med. 1985;2:100–119.
209 Gass GC, Camp EM. The maximum physiological responses during incremental wheelchair and arm cranking exercise in male paraplegics. Med Sci Sports Exerc. 1984;16:355–359.
210 Bloomfield SA, Jackson RD, Mysiw WJ. Catecholamine response to exercise and training in individuals with spinal cord injury. Med Sci Sports Exerc. 1994;26:1213–1219.
211 Erickson RP. Autonomic hyperreflexia: pathophysiology and medical management. Arch Phys Med Rehabil. 1980;61:431–440.
212 Ashley EA, Laskin JJ, Olenik LM, et al. Evidence of autonomic dysreflexia during functional electrical stimulation in individuals with spinal cord injuries. Paraplegia. 1993;31:593–605.
213 Comarr AE, Eltorai I. Autonomic dysreflexia/hyper-reflexia. J Spinal Cord Med. 1997;20:345–354.
214 Webborn AD. “Boosting” performance in disability sport. Br J Sports Med. 1999;33:74–75.
215 Hunt AH, Civitelli R, Halstead L. Evaluation of bone resorption: a common problem during impaired mobility. SCI Nurs. 1995;12:90–94.
216 Garland DE, Adkins RH, Stewart CA, Ashford R, Vigil D. Regional osteoporosis in women who have a complete spinal cord injury. J Bone Joint Surg Am. 2001;83-A:1195–1200.
217 Garland DE, Stewart CA, Adkins RH, et al. Osteoporosis after spinal cord injury. J Orthop Res. 1992;10:371–378.
218 Kiratli BJ, Smith AE, Nauenberg T, Kallfelz CF, Perkash I. Bone mineral and geometric changes through the femur with immobilization due to spinal cord injury. J Rehabil Res Dev. 2000;37:225–233.
219 Bloomfield SA, Mysiw WJ, Jackson RD. Bone mass and endocrine adaptations to training in spinal cord injured individuals. Bone. 1996;19:61–68.
220 Hangartner TN, Rodgers MM, Glaser RM, Barre PS. Tibial bone density loss in spinal cord injured patients: effects of FES exercise. J Rehabil Res Dev. 1994;31:50–61.
221 Kaplan PE, Roden W, Gilbert E, Richards L, Goldschmidt JW. Reduction of hypercalciuria in tetraplegia after weight-bearing and strengthening exercises. Paraplegia. 1981;19:289–293.
222 Sloan KE, Bremner LA, Byrne J, Day RE, Scull ER. Musculoskeletal effects of an electrical stimulation induced cycling programme in the spinal injured. Paraplegia. 1994;32:407–415.
223 Belanger M, Stein RB, Wheeler GD, Gordon T, Leduc B. Electrical stimulation: can it increase muscle strength and reverse osteopenia in spinal cord injured individuals? Arch Phys Med Rehabil. 2000;81:1090–1098.
224 Sniger W, Garshick E. Alendronate increases bone density in chronic spinal cord injury: a case report. Arch Phys Med Rehabil. 2002;83:139–140.
225 Chappard D, Minaire P, Privat C, et al. Effects of tilu-dronate on bone loss in paraplegic patients. J Bone Miner Res. 1995;10:112–118.
226 Dauty M, Perrouin Verbe B, Maugars Y, Dubois C, Mathe JF. Supralesional and sublesional bone mineral density in spinal cord-injured patients. Bone. 2000;27:305–309.
227 de Bruin ED, Frey-Rindova P, Herzog RE, Dietz V, Dambacher MA, Stussi E. Changes of tibia bone properties after spinal cord injury: effects of early intervention. Arch Phys Med Rehabil. 1999;80:214–220.
228 Bauman WA, Spungen AM. Metabolic changes in persons after spinal cord injury. Phys Med Rehabil Clin N Am. 2000;11:109–140.
229 Tsitouras PD, Zhong YG, Spungen AM, Bauman WA. Serum testosterone and growth hormone/insulin-like growth factor-I in adults with spinal cord injury. Horm Metab Res. 1995;27:287–292.
230 Campagnolo DI, Bartlett JA, Chatterton R Jr, Keller SE. Adrenal and pituitary hormone patterns after spinal cord injury. Am J Phys Med Rehabil. 1999;78:361–366.
231 Mechanick JI, Pomerantz F, Flanagan S, Stein A, Gordon WA, Ragnarsson KT. Parathyroid hormone suppression in spinal cord injury patients is associated with the degree of neurologic impairment and not the level of injury. Arch Phys Med Rehabil. 1997;78:692–696.
232 Bauman WA. Endocrinology and Metabolism After Spinal Cord Injury. Kirshblum S, Campagnolo DI, DeLisa JA. In: Spinal Cord Medicine. Philadelphia, Pa: Lippincott Williams and Wilkins; 2002:164–180.
233 Claus-Walker J, Halstead LS. Metabolic and endocrine changes in spinal cord injury: IV. Compounded neurologic dysfunctions. Arch Phys Med Rehabil. 1982;63:632–638.
234 Garland DE, Adkins RH, Matsuno NN, Stewart CA. The effect of pulsed electromagnetic fields on osteoporosis at the knee in individuals with spinal cord injury. J Spinal Cord Med. 1999;22:239–245.
235 Lazo MG, Shirazi P, Sam M, Giobbie-Hurder A, Blacconiere MJ, Muppidi M. Osteoporosis and risk of fracture in men with spinal cord injury. Spinal Cord. 2001;39:208–214.
236 Roberts D, Lee W, Cuneo RC, et al. Longitudinal study of bone turnover after acute spinal cord injury. J Clin Endocrinol Metab. 1998;83:415–422.
237 Uebelhart D, Demiaux-Domenech B, Roth M, Chantraine A. Bone metabolism in spinal cord injured individuals and in others who have prolonged immobilisation. A review. Paraplegia. 1995;33:669–673.
238 Uebelhart D, Hartmann D, Vuagnat H, Castanier M, Hachen HJ, Chantraine A. Early modifications of biochemical markers of bone metabolism in spinal cord injury patients. A preliminary study. Scand J Rehabil Med. 1994;26:197–202.
239 Iversen PO, Nicolaysen A, Hjeltnes N, Nja A, Benestad HB. Preserved granulocyte formation and function, as well as bone marrow innervation, in subjects with complete spinal cord injury. Br J Haematol. 2004;126:870–877.
240 Iversen PO, Hjeltnes N, Holm B, et al. Depressed immunity and impaired proliferation of hematopoietic progenitor cells in patients with complete spinal cord injury. Blood. 2000;96:2081–2083.
241 Chantraine A, Nusgens B, Lapiere CM. Bone remodeling during the development of osteoporosis in paraplegia. Calcif Tissue Int. 1986;38:323–327.
242 Naftchi NE, Viau AT, Sell GH, Lowman EW. Mineral metabolism in spinal cord injury. Arch Phys Med Rehabil. 1980;61:139–142.
243 Ragnarsson KT, Sell GH. Lower extremity fractures after spinal cord injury: a retrospective study. Arch Phys Med Rehabil. 1981;62:418–423.
244 Vestergaard P, Krogh K, Rejnmark L, Mosekilde L. Fracture rates and risk factors for fractures in patients with spinal cord injury. Spinal Cord. 1998;36:790–796.
245 Hartkopp A, Murphy RJ, Mohr T, Kjaer M, Biering-Sorensen F. Bone fracture during electrical stimulation of the quadriceps in a spinal cord injured subject. Arch Phys Med Rehabil. 1998;79:1133–1136.
246 Burnham RS, May L, Nelson E, Steadward R, Reid DC. Shoulder pain in wheelchair athletes. The role of muscle imbalance. Am J Sports Med. 1993;21:238–242.
247 Olenik LM, Laskin JJ, Burnham R, Wheeler GD, Steadward RD. Efficacy of rowing, backward wheeling and isolated scapular retractor exercise as remedial strength activities for wheelchair users: application of electromyography. Paraplegia. 1995;33:148–152.
248 Ballinger DA, Rintala DH, Hart KA. The relation of shoulder pain and range-of-motion problems to functional limitations, disability, and perceived health of men with spinal cord injury: a multifaceted longitudinal study. Arch Phys Med Rehabil. 2000;81:1575–1581.
249 Bayley JC, Cochran TP, Sledge CB. The weight-bearing shoulder. The impingement syndrome in paraplegics. J Bone Joint Surg [Am]. 1987;69:676–867.
250 Gerner HJ, Engel P, Gass GC, Gass EM, Hannich T, Feldmann G. The effects of sauna on tetraplegic and paraplegic subjects. Paraplegia. 1992;30:410–419.
251 Ishii K, Yamasaki M, Muraki S, et al. Effects of upper limb exercise on thermoregulatory responses in patients with spinal cord injury. Appl Human Sci. 1995;14:149–154.
252 Gass EM, Gass GC, Pitett K. Thermoregulatory responses to exercise and warm water immersion in physically trained men with tetraplegia. Spinal Cord. 2002;40:474–480.
253 Muraki S, Yamasaki M, Ishii K, Kikuchi K, Seki K. Relationship between core temperature and skin blood flux in lower limbs during prolonged arm exercise in persons with spinal cord injury. Eur J Appl Physiol. 1996;72:330–334.
254 Price MJ, Campbell IG. Thermoregulatory responses of spinal cord injured and able-bodied athletes to prolonged upper body exercise and recovery. Spinal Cord. 1999;37:772–779.
255 Gellman H, Sie I, Waters RL. Late complications of the weight-bearing upper extremity in the paraplegic patient. Clin Orthop. 1988;233:132–135.
256 Sie IH, Waters RL, Adkins RH, Gellman H. Upper extremity pain in the postrehabilitation spinal cord injured patient. Arch Phys Med Rehabil. 1992;73:44–48.
257 Subbarao JV, Klopfstein J, Turpin R. Prevalence and impact of wrist and shoulder pain in patients with spinal cord injury. J Spinal Cord Med. 1995;18:9–13.
258 Goldstein B, Young J, Escobedo EM. Rotator cuff repairs in individuals with paraplegia. Am J Phys Med Rehabil. 1997;76:316–322.
259 Pentland WE, Twomey LT. Upper limb function in persons with long term paraplegia and implications for independence: Part I. Paraplegia. 1994;32:211–218.
260 Burnham RS, May L, Nelson E, Steadward R, Reid DC. Shoulder pain in wheelchair athletes. The role of muscle imbalance. Am J Sports Med. 1993;21:238–242.
261 Silfverskiold J, Waters RL. Shoulder pain and functional disability in spinal cord injury patients. Clin Orthop. 1991;141–145.
262 Curtis KA, Drysdale GA, Lanza RD, Kolber M, Vitolo RS, West R. Shoulder pain in wheelchair users with tetraplegia and paraplegia. Arch Phys Med Rehabil. 1999;80:453–457.
263 Nichols PJ, Norman PA, Ennis JR. Wheelchair user's shoulder? Shoulder pain in patients with spinal cord lesions. Scand J Rehabil Med. 1979;11:29–32.
264 Pentland WE, Twomey LT. The weight-bearing upper extremity in women with long term paraplegia. Paraplegia. 1991;29:521–530.
265 Pentland WE, Twomey LT. Upper limb function in persons with long term paraplegia and implications for independence: Part I. Paraplegia. 1994;32:211–218.
266 Ta ylor AW, McDonell E, Brassard L. The effects of an arm ergometer training programme on wheelchair subjects. Paraplegia. 1986;24:105–114.
267 Robinson MD, Hussey RW, Ha CY. Surgical decompression of impingement in the weightbearing shoulder. Arch Phys Med Rehabil. 1993;74:324–327.