The Journal of The American Paraplegia Society
ISSN: 0195-2307 (Print) (Online) Journal homepage: http://www.tandfonline.com/loi/yscm19
Perspectives on Cardiovascular Fitness and SCI Stephen F. Figoni To cite this article: Stephen F. Figoni (1990) Perspectives on Cardiovascular Fitness and SCI, The Journal of The American Paraplegia Society, 13:4, 63-71, DOI: 10.1080/01952307.1990.11735822 To link to this article: http://dx.doi.org/10.1080/01952307.1990.11735822
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PERSPECTIVES ON CARDIOVASCULAR FITNESS AND SCI* Stephen F. Figoni, Ph.D., RKr ABSTRACT The purpose of these papers is to review and discuss the fundamental concepts and problems underlying cardiovascular fitness and spinal cord injury. Particular attention is paid to several modes of exercise available to individuals with spinal cord injury (SCI)- voluntary arm-crank and wheelchair ergometry, electrical stimulation leg cycle ergometry, and combined voluntary arm-cranking and electrical stimulation leg (hybrid) exercise. The effects of level of injury, active muscle mass, and sympathetic dysfunction upon acute central hemodynamic adjustments during exercise testing and chronic training adaptations are discussed for both quadriplegics and paraplegics. Several topics for future research are suggested.
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KEY WORDS: exercise, exertion, physiology, hemodynamic, health, rehabilitation, exercise testing, exercise training, electrical stimulation. INTRODUCTION
One frequent result of spinal cord injury (SCI) is the reduced ability of the individual to perform aerobic exercise with a large muscle mass and to stimulate the cardiovascular system. Therefore, cardiovascular fitness for this population has become a topic of increasing interest among medical/allied health professionals, exercise/ sport scientists, and SCI individuals, especially as the SCI population ages. This concern may stem from the hope that improvements in exercise performance also reflect improved integration of various physiologic systems (cardiovascular, pulmonary, neurologic, muscular, endocrine) that provide energy for movement via aerobic metabolism. Improved physiologic integrity typically produces increased physical work capacity, enhanced performance of activities of daily living (ADL), improved mobility and functional independence, increased capacity for employment, pursuit of an active lifestyle and social/ avocational activities, freedom from SCI-related medical complications, enhanced physical and mental health, reduced risk of coronary disease, and a normal high-quality and productive life span. As with ablebodied individuals, SCI individuals sometimes perceive physical fitness as a panacea for health problems, especially those related to immobility and inactivity. This paper reviews recent literature and discusses the fundamental concepts and problems underlying cardiovascular fitness and SCI. Particular attention is paid to the following modes of exercise available to SCI •Much of the research cited in this paper was supported by the Rehabilitation Research and Development Service, U.S. Department of Veterans Affairs. +Department of Rehabilitation Medicine and Restorative Care, Wright State University School of Medicine Dayton, OH For correspondence and reprints contact: Dr. Stephen Figoni R & D (151) VA Medical Center 4100 W. Third St. Dayton, OH 45428
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individuals: voluntary arm-cranking and wheelchair exercise, electrical stimulation leg cycle ergometry and combined arm+leg (hybrid) exercise. Discussions focus upon cardiovascular (central hemodynamic) responses during exercise testing and subsequent training effects. Many of the physiological, medical, and clinical research issues discussed in these papers are still controversial and unresolved. Much research is still needed to clarify these issues, especially long-term training effects and clinical applications. This overview attempts to offer an objective perspective through which to better understand the potential benefits and limitations of cardiovascular testing and training for the diverse SCI population. Research interest in SCI/ cardiovascular exercise physiology is a fairly recent phenomenon. Comprehensive reviews of research literature concerning the pathophysiology of SCI have covered cardiovascular responses to stressors such as postural tilt, sensory stimuli, autonomic dysreflexia, and pharmacologic agents during rest. 1-4 Conspicuously absent is any mention of acute adjustments or chronic adaptations to exercise training. Review of the literature reveals only six papers on this subject published before 1976, with the total number of papers now over 50. This topic has also been addres.sed in many review papers and book chapters during the last decade suggesting that this subject is gaining recognition in academic and clinical circles.5-25 VOLUNTARY ARM EXERCISE
Traditional rehabilitation medicine for SCI patients with functional levels below C4 has utilized therapeutic exercise to improve function of residual intact musculature. 26•27 Thus, voluntary use of the upper extremities has been emphasized to facilitate independence in wheelchair mobility, pressure relief, transfers, or other activities of daily living (ADL). These
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upper-extremity ADL tasks are necessary for survival in the community but are usually inadequate to promote cardiovascular fitness. 28·29 Preventive maintenance exercise programs at home also tend to emphasize upper-body fitness through weight training, wheelchair-accessible exercise courses, wheelchair aerobics, arm-crank or wheelchair ergometry, wheelchair propulsion, and wheelchair sports, with passive activities for the lower extremities such as stretching and standing in braces or a standing frame. 30 Wheelchair sports in particular have evolved from rehabilitative therapeutic activities to highly competitive events for elite upper-body athletes, 21 The upper-body musculature can clearly be trained for strength and endurance15 but, as will be discussed below, upper-body fitness is not usually synonymous with central cardiovascular fitness. The aforementioned arm exercise modes involve task-specific motor patterns involving small muscle groups that are not primarily designed to stress the normal central cardiovascular system. Generally, upper-body exercise modes do not engage a sufficient muscle m~ss to elicit the classical "maximal oxygen uptake" (V02 max) li.mited by the central circulation (e.g., cardiac output, Q).31 If the ability of the heart and circulation to supply blood and 02 exceeds the 02 demands within the relatively small exercising muscles, then the peak aerobic power will be limited primarily by peripheral factors within the muscles.32 Peripheral fatigue will occur before central hemodynamics are maximally stressed. In deconditioned able-bodied persons, arm exercise training may stress the cardiovascular system sufficiently to induce some beneficial central cardiovascular ch~nges. These may include increased peak arm exercise Q and stroke volume (SV).33 Most of the physiologic benefits, however, should be peripheral in nature (i.e., located within the trained muscles). Such peripheral training effects may include increased concentration of mitochondria, myoglobin and 02 storage, oxidative enzyme activity, muscle fiber size, and capillary density which facilitate 02 utilization at the muscle levei. 34.35 Recent research has contributed greatly to our understanding of acute physiologic responses in SCI individuals during exercise tests. 15 However, the precise nature of the cardiovascular training response to arm exercise is less well understood. Acute and chronic responses should be expected to vary with the level and completeness of SCI because the functional level determines (a) the residual muscle mass available to engage in exercise and (b) the degree of autonomic nervous system (sympathetic) function remaining to regulate the cardiovascular response to exercise.
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Exercise Response and Quadriplegia Complete quadriplegia is characterized by sensorimotor 33 losses over the majority of the body and by total separation of the peripheral sympathetic nervous system from control by the brain. Thus, the normal sympathetic outflow to heart, blood vessels, skeletal muscles, and adrenal medullae is interrupted at rest and during exercise. Remaining normal neurologic functions usually include diaphragmatic inspiratory control; some proximal upper-extremity innervation and sensation from associated muscles, joints and skin; and parasympathetic (vagal) control of viscera, including the heart. 36.37 Intrinsic tone of arterial and venous blood vessels,38 cardiovascular reflexes through the isolated spinal cord, l.3, 4.39•40 and/ or local metabolic processes in active muscles remain to regulate hemodynamic function throughout the body. Testing Individuals with functional levels of CS-Tl can perform arm ergometry (arm-cranking or wheelchair ergometry) at power outputs (PO's) commensurate with their residual upper-body musculature. During graded exercise tests, respiratory parameters (VD2, VC02,and pulmonary ventilation, VE) increase proportionally with PO, but peak values are usually lower than those of paraplegics during arm exercise and much lower than able-bodied persons performing large-muscle groups exercise (e.g., leg cycling or running).41 It is questionable whether or not the sympathetic nervous system is sufficiently activated to provide central circulatory support for voluntary arm exercise in persons with quadriplegia. In the upright sitting posture, peak heart ~ate (HR) is usually restricted to about 120 bpm, and Q SV and arterial blooq pressure (BP) are often subnormal for given levels of V02. 36AlA 2 Peripheral vascular insufficiency and inactivity of the skeletal muscle venous pump may induce excessive venous pooling in the legs and abdomen, reduce the circulating blood voi.ume and diminish venous return, thereby limiting SV, Q and blood flow to exercising arm muscles. Additionally, blood flow to metabolically less active areas would not be redistributed toward the active musculature. Quadriplegics are frequently hypotensive during upright arm exercise, due to vasodilation in exercising muscles for which peripheral vasoconstriction in the legs and viscera does not adequately compensate.42. 43
This dysfunctional syndrome of inadequate acute hemodynamic responses to increased metabolic demands has been named "circulatory hyp~kines~s" by several investigators.6•14·15·44-46 Values of VD2, Q, SV and HR during peak arm-crank exercise performed in the supine posture have been found to be significantl.(; higher than those in the upright sitting posture. 7
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Therefore, hypokinetic circulatory response may be partially attributable to the upright posture in which the exercise is performed. If upright posture induces pre-exercise central hypovolemia, then cardiac volumeloading becomes an even less likely effect of arm exercise in quadriplegia, further reducing the likelihood of central cardiovascular training effects. During voluntary arm exercise in quadriplegia, it may be impossible to accurately evaluate central cardiovascular fitness due to the inability of small muscles to maximally stress the heart. 18 Thus, the end point during maximal-effort arm exercise stress tests in otherwise healthy quadriplegics probably does not reflect the maximal capacity of the central cardiovascular system (i.e., pumping capacity of the heart, or ability of the heart to deliver blood and to exercising muscles). These tests do measure peak exercise capacity, as limited by the integration of all physiologic support systems under the specific conditions of the test (i.e., exercise mode, posture, etc.). The fatigue end point of these tests may reflect the following peripheral metabolic and/ or circulatory limitations: 13 1) the limited metabolic capacity of small muscles in the presence of a normal Q and muscle blood flow (i.e., where 02 supply exceeds the demand) 2) the inability of the peripheral vasculature to maintain sufficient arterial pressure in the presence of acutely vasodilated muscles and reduced total peripheral resistance, and/ or 3) subnormal venous return, relative to the desired level of 6 (due to impaired muscle pump and excessive venous compliance/venous pooling), resulting in red\}ced circulating blood volume, and inadequate Q and muscle blood flow.
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Training The primary stimulus for central circulatory (cardiac) improvement is an inc~ased volume-load on the heart (i.e., elevated SV and Q), which in able-bodied persons is proportional to the size of the muscle mass active during exercise training. 48 Central cardiovascular !"daptations are manifested by 1) higher peak SV and Q (reflecting an increased capacity to circulate blood) and/ or 2) lower HR and contractility at rest and during submaximal exercise (reflecting an increased cardiovascular reserve and decreased relative exercise intensity). If quadriplegics are unable to recruit a sufficient muscle mass during arm exercise to induce an adequate cardiac volume-load and stress the cardiovascular system, then we should not expect central cardiovascular training adaptations. Training studies have shown that exerci~ tolerance muscular endurance, peak PO, and peak can be improved in quadriplegia, but no evidence is available to support the presence of central cardiovascular training effects from upright voluntary
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arm exercise in quadriplegics. 42•49 Peripheral adaptations would nevertheless be valuable in assisting in performance of those activities of daily living, such as wheelchair propulsion, requiring muscular endurance.50 Given the difficulty of assessing maximal cardiovascular responses to arm exercise in quadriplegia without cardiac disease, it is equally difficult to determine changes in these parameters conseq';lent to training. For example, if a true maximal Q cannot be determined during arm exercise, then central cardiovascular reserve and, indeed, the relative degree of stress of any exercise, cannot be determined. If the previously mentioned peripheral limitations are reduced or removed (i.e., through the use of a horizontal posture, lower-body compression, recruitment of additional muscle mass through electrical stimulation, sympathomimetic agents, etc.), then exercise may be more likely to stress and train the heart. 47 Additional research is 33 needed in this area since the central cardiovascular trainability in quadriplegia (i.e., effect of training upon central hemodynamic function during rest or exercise) is largely unknown. Exercise Response and Paraplegia Compared with quadriplegia, complete paraplegia is characterized by less extensive sensorimotor losses and by only partial separation of the peripheral sympathetic nervous system from control by the brain. The physiologic responses to exercise in paraplegia may be more heterogeneous than in quadriplegia due to more variable innervation of the peripheral sympathetic system. Paraplegics with functional levels from T2-T4 have normal upper extremity muscle mass and partial sympathetic outflow to the heart. However, sympathetic outflow to blood vessels of the viscera, lower extremities and adrenal medullae are usually absent. The degree of sympathetic decentralization is directly dependent upon the level and completeness of SCI. The level of injury and presumed sympathetic function, however, appear to be poor predictors of upper-body exercise capability among paraplegics. For example, peak arm-crank or wheelchair exercise performance, as demonstrated in laboratory tests and wheelchair racing, vary ~atly with level of injury and medical classification. 1-53 In addition to aerobic and cardiovascular fitness, these performances may depend heavily upon proper biomechanical utilization of a large muscle mass that is highly trained for both aerobic and anaerobic work. 22 Testing In the upright sitting posture, paraplegics frequently demonstrate some circulatory hypokinesis during arm-crank exercise. 46 Although HR and arterial BP in paraplegia tend to be more normal than in quad-
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riplegia, Q _:md SV appear to be subnormal for given levels of V02. 46.54-56 Peak exercise performance is probably also limited by the same peripheral mechanisms as in quadriplegia, but to a lesser degree. Therefore, principles of ann exercise physiology and training for able-bodied individuals are likely to be more applicable to paraplegia than to quadriplegia. 15,32 Relatively little is known about cardiovascular and hemodynamic responses during wheelchair ergometry or racing. 57 However,. given similarities in active muscle mass and peak V02, acute and chronic responses to wheelchair exercise are not likely to differ markedly from responses to ann-cranking.58 Research is now in progress to evaluate wheelchair graded exercise testing as a tool to assess cardiopulmonary fitness and disease in disabled subjects using their own wheelchairs on stationary rollers.59
Training As is true for able-bodied persons, paraplegics may be able to use voluntary upright ann exercise to recruit a sufficient muscle mass to induce adequate volume and pressure loads on the heart to induce cardiac adaptations and improve cardiovascular fitness. Research has clearly show~! that arm strength, endurance, peak PO, and peak V02 can improve through arm training. 15•42. 60 To date, no specific central cardiovascular adaptations at rest or during exercise have been documented in paraplegics who have completed their acute rehabilitation. Moderate intensity wheelchair ergometer training has been shown, however, to increase high-density lipoprotein cholesterol (HDLC) concentration, as well as reduce triglycerides, low-density lipoprotein cholesterol, and the ratio of triglycerides to HDLC61 - changes that may lower the risk of eventual coronary heart disease. ELECTRICAL STIMULATION LEG CYCLE ERGOMETRY (ES·LCE)
In the quest for more effective techniques for cardiovascular testing and training of SCI individuals, the concept of using electrically induced contractions of paralyzed leg muscles has great physiologic appeal. Recruitment of the large lower extremity muscle mass and reactivation of the leg muscle pump to facilitate venous return may provide the SCI population with an aerobic exercise mode comparable to able-bodied bicycling or jogging.16 Research to evaluate the cardiovascular safety of two commercially available ergometers, the "ERGYS I" and "REGYS 1" (Therapeutic Technologies, Inc., TAMPA, FL), has elucidated several advantages and limitations of ES-LCE as currently used. These systems allow stationary leg cycle ergometry with 300 muscle contractions/min through microprocessor-controlled electrical stimulation delivered via skin surface electrodes to bilateral quad-
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riceps, hamstring, and gluteal muscle groups. The SCI user population to which ES-LCE is applicable is restricted to relatively healthy individuals with functional levels above T12, i.e., upper motor neuron SCI, with minimal residual skin sensation, and with no medical contraindication to ES-LCE.62 It should be remembered that this exercise technology is still in early development, and that any limitations or problems found regarding its use may be overcome with subsequent technological advancements.
Testing Metabolic studies using available ES-LCE instrumentation (i.e., ERGYS 1 and REGYS 1 ergometers) have revealed that this exercise mode is mechanically inefficient comgared with able-bodied cycling at equivalent PO's. 2.63 This energy wastefulness helps account for the low PO's used by SCI individuals even after several months of training. Physiologic responses, however, are high relative to the PO's, which is advantageous in terms of stimula!ing hem~dynarnic responses. ES-LCE typically elevates V02 and Q to approximately 1 1/min and 9 1/min, respectively, at a PO of about 10 W (i.e., 0.25 Kp load @ 42 RPM cadence).56·63-67 These responses correspond to disabled individuals performing wheelchair ergometry at 35 W or arm-cranking at 70 WP or to able-bodied persons walking at 3 MPH (4 METS, 300 kcal/hr). Aerobic exercise at this absolute intensity generally provides mild central cardiovascular conditioning with potential for significant caloric expenditure if performed regularly for sufficient periods of time (e.g., 60 min/session, 3-4 sessions/week). Compared with paraplegics, quadriplegics generally perform ES-LCE at slightly lower PO's which elicit proportionally lower levels of physiologic responses.54•676? However, mean peak hemodynamic responses (SV and Q) of quadriplegics during ES-LCE are significantly higher than those elicited during sub-peak and peak arm-crank exercise at equivalent V02levels, especially for quadriplegics with functional levels above C7.68•70 Therefore, ES-LCE appears to be more effective than arm-crank exercise for cardiac volume-loading quadriplegics. For paraplegics, sympathetically mediated responses such as HR and BP increase moderately during ES-LCE, suggesting that sympathetic nervous system activity is stimulated either by the peripherally applied (FNS-induced) muscular contractions and/ or through intact central command pathways.40.66·69 Whereas voluntary arm-cranking generates a higher peak HR in paraplegics, ES-LCE appears hemodynamically superior in terms of cardiac volume-loading. For both quadriplegics and paraplegics, this may be due to activation of the leg muscle venous pump, facilitation of venous return, and enhancement of cardiac preload and SV through the Frank-Starling mechanism56,69-71
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Training . Signific;ant training-induced increases in peak PO, V02 and VE have been reported by several inve.stigators, with little or no change in peak HR, SV, Q, MAP, and TPR after several weeks or months of ES-LCE training. 67·71 -74 Therefore, improved exercise performance following ES-LCE training appears to be due to peripheral adaptations that enhance muscular strength and endurance. ES-LCE training has also been reported to have minimal effects upon resting physiology. For example, some investigators have reported small increases in supine resting hemodynamic respon~s after an ESLCE training program (i.e., increased Q, HR and SBP by 0.33 1/min, 3-4 bpm, and 7 mmHG, respectively)?5·76 Others have found no changes in resting HR, BP, metabolic and respiratory parameters. 72 In summary, some individuals may benefit from ES-LCE training that utilizes the currently available technology. However, scientific research has yet to generalize the efficacy of ES-LCE as a central cardiovascular training tool for the SCI population. Although not the primary focus of this paper, several possible peripheral physiolo~c effects have been hypothesized by ES-LCE users. Most of these effects on skin, muscles, bones and joints await scientific documentation. However, they deserve attention due to their potential for preventing or treating specific SCI medical complications and improving the health of ES-LCE users. Peripheral effects which merit scientific investigation include the following: 1) Skin: skin blood flow, altered sitting pressure distribution, incidence of pressure sores, e.ffect on
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wound healing. 2) Muscle: muscular hypertrophy and its sequelae, ef-
fect on metabolic rate, utility as a measure for weight control/ obesity management and cosmesis, effect on paretic muscle strength for lower-extremity ADL, effect on spasticity. 3) Bone: rate of bone resorption or density; incidence of pathological fractures, hypercalciuria, renal calculi, and heterotropic ossification. 4) Joints: long-term effect on joint integrity, range of motion and incidence of contracture. 5) Lower extremity circulation: effect on lymphatic and venous circulation, on normalization of fluid content and distribution on reduced venous pooling/ stasis and on decreased blood coagulation; incidence of deep venous thrombosis, pulmonary embolism, orthostatic hypotension, edema and acrocyanosis; effect on cosmesis. COMBINED ARM+LEG (HYBRID) EXERCISE
In an attempt to further stress the cardiovascular system, initial a·ttempts have been made to combine volunta7a arm exercise with electrical stimulation leg exercise. S..SJ The combined arm+leg (hybrid) exercise may have the potential advantages of a) utilization of larger muscle mass, which may promote higher physiologic responses and improve fitness training capability, and b) the voluntary arm-crank component may elicit higher cardiovascular sympathetic activity and facilitate leg exercise performance. 82 Figure 1 illustrates a research hybrid exercise system consisting of a Monark Rehab Trainer TM arm-crank ergometer mounted on a specially built table to allow arm-crank-
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ing while pedaling the "ERGYS 1" ergometer. 17 Other arm+leg ergometers for disabled individuals are also commercially available with the paralyzed leg muscles driven actively by electrical stimulation ("Power Trainer," Sinties Scientific Corp., Tulsa, OK) or passively by mechanical linkage to the arm cranks ("Pedal-InPlace," Thoele Mfg., Montrose, IL). At present, physiologic responses to use of these devices have yet to be clinically or scientifically evaluated.
with possible dizziness, nausea, and extreme fatigue. In summary, while hybrid exercise can induce higher peak physiologic responses acutely in some individuals, the two exercise modes may interact with each other and may not be tolerated by some quadriplegics. As with therapeutic exercise, the optimal combinations of arm and leg exercise may need to be individualized according to the tolerance and needs of each person.
Testing
Training
Recent research findings are redefining the upper limits of peak exercise performance for SCI individuals, especially for quadriplegics. For example, in a group of untrained quadriplegics who performed a maximal-effort graded arm-cran}< exercise test during "0" -W ESLCE, peak values of VCh Q, SV and JR were increased significantly by 35, 46, 26 and 18%, respectively, above levels observed during peak arm-cranking witl}out ESLCE.81 Therefore, the ability to increase peak Q above that for arm-cranking alone strongly suggests that peak vo2 is limited more by peripheral factors such as active muscle mass and venous insufficiency rather than by central cardiac factors. The increments of the peak arm+leg physiologic responses above resting levels appeared to be an additive function of the arm and leg exercises performed separately. On the other hand, untrained paraplegics responded to combined peak arm-crank exercise and 0-W ES-LCE with an increased peak VOl but with little or no increment in peak Q, suggesting a central circulatory limitation during peak hybrid exercise (unpublished observations). It may be possible to drive peak physiologic responses during arm+leg exercise to even higher levels with a more effective form of electrical stimulation involving additional muscle groups, use of "gravity-eliminated" posture or environment, or hybrid exercise training. Systemic sympathetic impairment may ultimately limit exercise performance with relatively large muscle groups, especially in quadriplegics. Combining peak voluntary arm-cranking with increasing amounts of voluntary and/ or electrically induced leg cycling has been shown to induce increasing degrees of exercise hypotension. 83 The arterial pressure gradient (represented by the mean arterial pressure, MAP) and total peripheral resistance (TPR) are the basic hemodynamic determinants of cardiac output (Q =MAP I TPR). Extensive vasodilation of a large proportion of the muscle mass (i.e., decreased total peripheral resistance, TPR), combined with impaired compensatory ability to vasoconstrict other arterial vessels and increases HR and myocardial contractility (i.e., increase mean arterial presspre, MAP), will preclude maintenance of BP.84 Hence, Q and perfusion of vital organs such as the brain will decrease, resulting in exercise hypotension
Training studies with hybrid exercise are currently in progress at the VA Medical Center and Wright State University School of Medicine in Dayton, OH. 85 While an earlier studyll2 found that voluntary arm exercise facilitated electrically induced knee extension resistance exercise, more recent research indicates that simultaneous voluntary arm and ES-LCE may interfere with each other when performed in the upright sitting posture. That is, when moderate-intensity arm-cranking is added to a bout of relatively high-level ES-LCE, some SCI individuals respond with a decrease in ESLCE performance. At the present time, it is speculative if the nature of the limitation is mechanical (upperbody exercise interfering with lower-body exercise), circulatory (legs not competing successfully with the arms for their limited share of blood flow, especially in the presence of orthostatic hypotension or excessive venous pooling), humoral (increased metabolic acidosis from the arms interfering with the legs), or a combination of the above or other unknown factors. Some evidence from able-bodied subjects supports the circulatory hypothesis. 86 When arm exercise was added to leg exercise, Q increased but leg blood flow decreased. Apparently the heart could not supply both the legs and the arms with blood because the combined demands exceeded the pumping capacity of the heart. 87 It is not known if this interaction will be a function of training status, level of injury, sympathetic impairment, medications or other specific characteristics of SCI individuals. Individuals who can tolerate activation of a very large muscle mass will be able to take advantage of the greater metabolic and circulatory loads that hybrid exercise can generate. FUTURE RESEARCH In the future, researchers need to investigate several major questions in SCI/ cardiovascular exercises physiology. First, what exercise mode will enable high-level, yet safe, cardiac volume-loading in SCI individuals? Can the sympathetic nervous system be stimulated to provide appropriate support of highlevel aerobic metabolism? A challenge for future research is to develop techniques to maintain arterial pressure and increase peripheral resistance in inactive areas of the body, so that Q can be maintained during
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large muscle group exercise in SCI subjects with profound sympathetic impairment. Secondly, a major thrust of future research should address the central versus peripheral trainability in quadriplegics and paraplegics for various modes of voluntary and/or electrically induced exercise training. We need to define the relationships between physiologic training effects and specific parameters of health and functional independence. What level of exercise metabolism and central circulation must be achieved to develop and maintain general physical fitness and wellness? Is the arm muscle mass large enough to provide sufficient training stimulus to improve resting peripheral and central circulatory function? Thirdly, what are the clinical benefits of increased cardiovascular fitness? Can it help control orthostatic hypotension, increase skin blood flow and pressure tolerance of skin, prevent excessive venous pooling and lymphedema, and reduce the incidence of deep venous thrombosis and other circulatory disorders? Can exercise training play the same role in preventative health care as in the able-bodied population88primary and secondary prevention of heart disease through modification of coronary risk factors such as obesity, hypertension and hyperlipidemia; and prevention of osteoporosis? Does exercise enhance mental health, improve affect, and increase self-esteem? Given the pathophysiologic diversity within the SCI population, the use of single-subject experimental research designs should be considered along with traditional group research designs to better evaluate the effects of training upon specific medical conditions/ dysfunctions and patient-treatment interactions. 89 This approach can generate clinically relevant information for immediate use by practitioners. Scientific documentation of medical indications may facilitate acceptance or rejection of these exercise modalities for more widespread clinical use.
SUMMARY SCI often impairs the ability of individuals to perform large-muscle-group aerobic exercise. The exercise modes currently being studied include voluntary armcranking and wheelchair exercise, electrical stimulation leg cycle ergometry, and combined voluntary arm and electrical stimulation leg (hybrid) exercise. When paralyzed muscle can be activated electrically and added to the residual voluntary muscle mass, the intensity and duration of exercise may be limited by sympathetic nervous system impairment, which is more severe in individuals with higher-level and more complete SCI. However, hybrid exercise shows promise in terms of volume-loading the heart and inducing central cardiovascular training effects in SCI individuals. Ongoing research aims to develop hybrid exercise instrumentation that maximizes appropriate physiologic
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responses, that is tolerated by and available to more SCI individuals, and that provides beneficial general cardiovascular conditioning as well as a therapeutic modality for selected medical conditions. More research is needed to establish the medical efficacy of electrical stimulation in the treatment of specific pathologies and dysfunctions.
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16. Glaser RM. Functional neuromuscular stimulation for physical fitness training of the disabled. In: Kaneko M, ed. Fitness for the aged, disabled and industrial worker. International series on sport sciences. Champaign, IL: Human Kinetics Books, 1990;127-34. 33 17. Glaser RM. Spinal cord injuries and neuromuscular stimulation exercise. In: Torg JS, Welsh RP, Shephard RJ, eds. Current therapy in sports medicine. Toronto: B.C. Decker, Inc., 1990:166-70. 18. Glaser RM. Cardiovascular problems of the wheelchair disabled. In: Shephard RJ, Miller H, eds. Exercise and the heart in health and cardiac disease. Toronto: B.C. Decker, Inc. (in press). 19. Glaser RM. Exercise conditioning of the spinal cord injured via functional electrical stimulation. In: Torg JS, ed. Athletic injuries to the head, neck and face (2nd ed.). Chicago: Yearbook Medical Publishers (in press). 20. Glaser RM. Functional neuromuscular stimulation. In: Enders A, Hall M, eds. Assistive technology sourcebook. Washington, DC: RESNA Press Publisher, 1990:438-41. 21. Hedrick B, Morse M, Hedrick S. A guide for wheelchair sports training. Colorado Springs: National Wheelchair Athletic Association, 1988. 22. Hedrick B, Morse M, Hedrick S, Figoni SF. Wheelchair sports training: basic principles. Washington, DC: Paralyzed Veterans of America (in press). 23. Hoffman MD. Cardiorespiratory fitness and training in quadriplegics and paraplegics. Sports Med 1986;3:312-30. 24. Shephard RJ. Sports medicine and the wheelchair athlete. Sports Med 1988;4:226-247. 25. Wells CL, Hooker SP. The spinal injured athlete. Adapted Phys Activity Quart (in press). 26. Abramson AS. Exercise in paraplegia. In: Basmajian JV, ed. Therapeutic exercise, 3rd ed. Baltimore: The Williams & Wilkins Co., 1976. 27. Long C. Congenital and traumatic lesions of the spinal cord. In: Krusen FH, Kottke FJ, Ellwood PM, eds. Handbook of physical medicine and rehabilitation. Philadelphia: WB Saunders Company, 1971:566-78. 28. Clarke KC. Caloric costs of activity in paraplegic persons. Arch Phys Med Rehabi11966;47:427-35. 29. Hjeltnes N, Vokac Z. Circulatory strain in everyday life of paraplegics. Scand J. Rehabil Med 1979; 111:67-73. 30. Lasko PM, Knopf KG. Adapted and corrective exercise for the disabled adult. Dubuque, lA: Eddie Bowers Publishing Co., 1984:220-2. 31. Taylor HL, Buskirk E, Henschel A. Maximal oxygen intake as an objective measure of cardiorespiratory performance. J Appl Physiol1955;2:223-9. 32. SawkaMN. Physiology of upper body exercise. In: PandolfKB, ed. Exercise and sports science reviews. New York: Macmillan, 1986:175-210. 33. Clausen JP, Klausen K, Rasmussen B, Trap-Jensen J. Central and peripheral circulatory changes after training of the arms or legs. Am J Physiol1973;225:675-82. 34. Gaffney FA, Grimby G, Danneskiold-Samsoe B, Halskov 0. Adaptation to peripheral muscle training. Scand J Rehabil Med 1981;13:11-16. 35. Franklin BA, Rubenfrre M. Exercise training coronary heart disease. Practical Cardiol1980;6:84-99. 36. Figoni SF, Boileau RA, Massey BH, Larsen JR. Physiological responses of quadriplegic and able-bodied men during exercise at the same V02. Adapted Phys Activity Quart 1988;5:130-9.
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37. Freyschuss U. Autonomic nervous mediation of the heart rate acceleration on an isometric muscle contraction in tetraplegic men. Acta Physiol Scand 1970;57(Suppl. 342):28-33. 38. Sommers DK. Reactivity of the cardiovascular system in the tetraplegic patient. Clin Pharm Ther 1979;26:344-53. 39. Corbett U, Frankel HL, Harris PJ. Cardiovascular reflex responses to cutaneous and visceral stimuli in spinal man. J Physiol 1971 ;215 :395-409. 40. Petrofsky JS, Phillips CA, Hendershot DM. The cardiorespiratory stresses which occur during dynamic exercise in paraplegics and quadriplegics. J Neurol Orthop Med Surg 1985;6:252-8. 41. Van Loan MD, McCluer S, Loftin JM, Boileau RA. Comparison of physiological responses to maximal arm exercise among ablebodied, paraplegics and quadriplegics. Paraplegia 1987;25 :397405. 42. Hjeltnes N. Capacity for physical work and training after spinal injuries and strokes. Scand J Rehabil Med 1982;29:245-51. 43. Hjeltnes N. Control of medical rehabilitation of para and tetraplegics by repeated evaluation of endurance capacity. Int J Sports Med 1984;5:171-4. 44. Strandell T. Circulatory studies in healthy old men: with special reference to the limitation of the maximal physical working capacity. Acta Med Scand 1964;175(Supp. 414). 45. Malmborg RO. Clinical and hemodynamic analysis of factors limiting the cardiac performance in patients with coronary heart disease. Acta Med Scand 1965; 177(Suppl. 426). 46. Hjeltnes N. Oxygen uptake and cardiac output in graded arm exercise in paraplegics with low level spinal lesions. Scand J Rehabil Med 1977;9:107-13. 47. Figoni SF, Gupta SC, Glass RM, Suryaprasad AG, Rodgers MM, Ezenwa BN. Exercise hemodynamics of quadriplegics: a pilot study. Rehabil Res Dev Progr Rep (Ann Suppl to J Rehabil Res Dev) 1989;26:111-12. 48. Clausen JP. Effect of physical training on cardiovascular adjustments to exercise in man. Physiol Rev 1977;57:779-815. 49. Figoni SF. Circulorespiratory effects of arm training and detraining in one C5-6 quadriplegic man. Phys Ther 1986;66:779. 50. DiCarlo SE. Effect of arm ergometry training on wheelchair propulsion endurance of individuals with quadriplegia. Phys Ther 1988;68:404. 51. Gass GC, Camp EM. Physiological characteristics of trained Australian paraplegic and tetraplegic subjects. Med Sci Sports Exerc. 1979; 11:256-65. 52. Wicks JR, Oldridge NB, Cameron NB, Jones NL. Arm cranking and wheelchair ergometry in elite spinal cord injured athletes. Med Sci Sports Exerc 1983;15:224-31. 53. Hooker SP, Wells CL. Aerobic capacity of elite American paraplegic road racers. Med Sci Sport Exerc. (unpublished manuscript in review). 54. Davis GM, Shephard RJ, Leenen FHH. Cardiac effects of short term arm crank training paraplegics: echocardiographic evidence. Eur J Appl Physiol1987;56:90-6. 3:3 55. Davis GM, Shephard RJ. Cardiorespiratory fitness in highly active versus inactive paraplegics. Med Sci Sports Exerc 1988;20:463-468. 56. Hooker SP, Figoni SF, Glaser RM, et al. Physiologic responses to arm cranking and electrical stimulation leg cycling, part I: paraplegics. Med Sci Sport Exerc 1990;22(Suppl.): S43. 57. Sawka MN, Glaser RM, Wilde SW, von Lulrrte TC. Metabolic and circulatory responses to wheelchair and arm crank exercise. J Appl Physiol: Respirat Environ Exerc Physiol1980;49:784-788.
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58. 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- 9. 59. Langbein WE, Hwang MH, Reid CA, Robinson CJ, Nemchausky BA. Wheelchair graded exercise test for patients with lower limb disabilities. Rehabilitation R & D Progress Reports (Ann Suppl to J Rehabil Res Dev) 1989;26: 108-9. 60. Gass GC, Watson J, Cam EM, Court HJ, McPherson LM, Redhead P. The effects of physical training on high level spinal lesion patients. Scand J Rehabil Med 1980;12:61-5. 61. Hooker SP, Wells CL. Effects of low and moderate intensity training in spinal cord-injured persons. Med Sci Sports Exerc 1989;21:18-22. 62. Therapeutic technologies Inc. ERG YS 1 operator's manual #043112. Ft. Lauderdale, FL: Therapeutic Technologies Inc., 1986. 63. Glaser RM, Figoni SF, Collins SR, et al. Physiologic responses of SCI subjects to electrically induced leg cycle ergometry. In: Harris G, Walker C, eds. Proceedings of the tenth annual international conference of the IEEE Engineering in Medicine and Biology Society. New York: Institute of Electrical and Electronics Engineers, Inc., 1988:1638-40. 64. Glaser RM, Figoni SF, Hooker SP, et al. Efficiency of FNS leg cycle ergometry. In: Kim Y, Spelman FA, eds. Proceedings of the eleventh annual international conference of the IEEE Engineering in Medicine and Biology Society. New York: Institute of Electrical and Electronics Engineers, Inc., 1989:961-3. 65. Faghri PD, Glaser RM, Figoni SF, Miles DS, Gupta SC. Feasibility of using two FNS exercise modes for spinal cord injured patients. Clin Kinesiol1989;43:62-8. 66. Hooker SP, Figoni SF, Glaser RM, Rodgers MM, Ezenwa BN, Faghri PD. Physiologic responses to prolonged electricallystimulated leg cycle exercise in the spinal cord injured. Arch Phys Med Rehabil (in press). 67. Ragnarsson KT, O'Daniel W, Edgar R, Pollack S, Petrofsky J, Nash MS. Clinical evaluation of computerized functional electrical stimulation after spinal cord injury: a multicenter study. Arch Phys Med Rehabil 1988;69:672-7. 68. Figoni SF, Glaser RM, Hooker SP, eta!. Physiologic responses of paraplegics and quadriplegics to passive and active leg cycle ergometry. J Amer Paraplegia Soc (in press). 69. Figoni SF, Glaser RM, Hooker SP, et a!. Peak physiologic responses of SCI subjects during FNS leg cycle ergometry. In: Presperin JJ, ed. Proceedings of the twelfth annual conference of the Rehabilitation Engineering Society of North America. Washington, DC: Rehabilitation Engineering Society of North America, 1989:97-8. 70. Figoni SF, Hooker SP, Glaser RM, eta!. Physiologic responses to arm cranking and electrical stimulation leg cycling, part II: quadriplegics. Med Sci Sports Exerc 1990;22(Suppl.):S43. 71. Hooker SP, Glaser RM, Figoni SF, et al. Physiologic training effects of functional neuromuscular stimulation leg cycle exercise in the spinal cord injured. Proceedings of the 13th annual conference of the Rehabilitation Engineering Society of North America. Washington, DC:RESNA Press, 1990:165-6. 72. Polack SF, Axen K, Spielholz N, Levin N, Haas F, Ragnarsson KT. Aerobic training effects of electrically induced lower extremity exercises in spinal cord injured people. Arch Phys Med Rehabil1989;70:214-219. 73. Ragnarsson KT. Physiologic effects of functional electrical stimulation-induced exercises in spinal cord injured individuals. Clin Orthop Related Res 1988;233:53-63.
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74. Phillips PA, Petrofsky JS, Hendershot D, Stafford D. Functional electrical exercise: comprehensive approach for physical conditioning of spinal cord injured patient. Orthop 1984;7: 1112-23. 75. Danopulos D, Kezdi P, Petrofsky JS, Stacy RW, Phillips CA, Meyer LS. Changes in cardiovascular circulatory dynamics after a twelve week active bicycle rehabilitation in young tetraplegics. J Neurol Orthop Med Surg 1986;7: 179-84. 76. Phillips CA, Danopulos D, Kezdi P, Hendershot D. Muscular, respiratory and cardiovascular responses of quadriplegics to an F.E.S. bicycle ergometer conditioning program. Int J Rehabil Res 1989;12:147-57. 77. Sipski ML, DelisaJA, SchweerS. Functional electrical stimulation bicycle ergometry: patient perceptions. Amer J Phys Med Rehabil1989;68:147-9. 78. Robinson DE, Triolo RJ, Betz RR. Physiological responses to FNS exercise in SCI children. In: Kim Y, Spelman FA, eds. Proceedings of the twelfth annual international conference ofthe IEEE Engineering Medicine and Biology Society. New York: Institute of Electrical and Electronics Engineers, Inc., 1989;12:1498-9. 79. Davis GM, Servedio FJ, Glaser RM, Gupta SC, Suryaprasad AG. Cardiovascular responses to arm cranking and electricallyinduced leg exercise in paraplegics. J Appl Physiol, in press. 80. Hooker SP, Figoni SF, Glaser RM, eta!. Physiologic responses to simultaneous voluntary arm crank and electrically stimulated leg cycle exercise in quadriplegics. In: Presperin JJ, ed. Proceedings of the twelfth annual conference of the Rehabilitation Engineering Society of North America. Washington, DC:RESNA Press, 1989:99-100. 81. Figoni SF, Glaser RM, Rodgers MM, et a!. Hemodynamic responses of quadriplegics to arm, ES-leg, and combined arm+ ES-leg ergometry. Med Sci Sports Exerc 1989;21(Suppl. 2):S96. 82. Glaser RM, Strayer JR, May KP. Combined PES leg and voluntary arm exercise of SCI patients. In: Lin JC, Feinberg BN, eds. Proceedings of the seventh annual international conference of the IEEE Engineering in Medicine and Biology Society. Washington, DC: Institute of Electrical and Electronics Engineers, Inc., 1985;7:308-11. 83. Figoni SF. Arm and leg exercise stress testing in a quadriparetic patient. Clin Kinesiol1089;43:108. 84. Rowell, LB. Human cardiovascular adjustments to thermal stress. Physiol Rev 1976;54:75-159. 85. Mathews T, Glaser RM, Figoni SF, et al. Evaluation of PES Techniques for Exercise. Rehabilitation R & D Progress Reports (Ann Suppl to J Rehabil Res Dev). 1989;26:198-9. 86. Secher NH, Clausen JP, Klausen K, Noer I, Trap-Jensen J. Central and regional circulatory effects of adding arm exercise to leg exercise. Acta Physiol Scand 1977;100:288-97. 87. Rowell LB. Human circulationregulationduring physical stress. New York: Oxford University Press, 1986. 88. Anonymous. Exercise counseling. In: Fisher M, ed. Guide to clinical preventive services: an assessment of the effectiveness of 169 interventions. Report of the U.S. Preventive Services Task Force. Baltimore: Williams & Wilkins, 1989:297-303. 89. Figoni SF. Single-subject clinical research: bridging the gap between therapy and science. Clin Kinesiol (in press).
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ISSN: 0195-2307 (Print) (Online) Journal homepage: http://www.tandfonline.com/loi/yscm19
Perspectives on Cardiovascular Fitness and SCI Stephen F. Figoni To cite this article: Stephen F. Figoni (1990) Perspectives on Cardiovascular Fitness and SCI, The Journal of The American Paraplegia Society, 13:4, 63-71, DOI: 10.1080/01952307.1990.11735822 To link to this article: http://dx.doi.org/10.1080/01952307.1990.11735822
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PERSPECTIVES ON CARDIOVASCULAR FITNESS AND SCI* Stephen F. Figoni, Ph.D., RKr ABSTRACT The purpose of these papers is to review and discuss the fundamental concepts and problems underlying cardiovascular fitness and spinal cord injury. Particular attention is paid to several modes of exercise available to individuals with spinal cord injury (SCI)- voluntary arm-crank and wheelchair ergometry, electrical stimulation leg cycle ergometry, and combined voluntary arm-cranking and electrical stimulation leg (hybrid) exercise. The effects of level of injury, active muscle mass, and sympathetic dysfunction upon acute central hemodynamic adjustments during exercise testing and chronic training adaptations are discussed for both quadriplegics and paraplegics. Several topics for future research are suggested.
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KEY WORDS: exercise, exertion, physiology, hemodynamic, health, rehabilitation, exercise testing, exercise training, electrical stimulation. INTRODUCTION
One frequent result of spinal cord injury (SCI) is the reduced ability of the individual to perform aerobic exercise with a large muscle mass and to stimulate the cardiovascular system. Therefore, cardiovascular fitness for this population has become a topic of increasing interest among medical/allied health professionals, exercise/ sport scientists, and SCI individuals, especially as the SCI population ages. This concern may stem from the hope that improvements in exercise performance also reflect improved integration of various physiologic systems (cardiovascular, pulmonary, neurologic, muscular, endocrine) that provide energy for movement via aerobic metabolism. Improved physiologic integrity typically produces increased physical work capacity, enhanced performance of activities of daily living (ADL), improved mobility and functional independence, increased capacity for employment, pursuit of an active lifestyle and social/ avocational activities, freedom from SCI-related medical complications, enhanced physical and mental health, reduced risk of coronary disease, and a normal high-quality and productive life span. As with ablebodied individuals, SCI individuals sometimes perceive physical fitness as a panacea for health problems, especially those related to immobility and inactivity. This paper reviews recent literature and discusses the fundamental concepts and problems underlying cardiovascular fitness and SCI. Particular attention is paid to the following modes of exercise available to SCI •Much of the research cited in this paper was supported by the Rehabilitation Research and Development Service, U.S. Department of Veterans Affairs. +Department of Rehabilitation Medicine and Restorative Care, Wright State University School of Medicine Dayton, OH For correspondence and reprints contact: Dr. Stephen Figoni R & D (151) VA Medical Center 4100 W. Third St. Dayton, OH 45428
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individuals: voluntary arm-cranking and wheelchair exercise, electrical stimulation leg cycle ergometry and combined arm+leg (hybrid) exercise. Discussions focus upon cardiovascular (central hemodynamic) responses during exercise testing and subsequent training effects. Many of the physiological, medical, and clinical research issues discussed in these papers are still controversial and unresolved. Much research is still needed to clarify these issues, especially long-term training effects and clinical applications. This overview attempts to offer an objective perspective through which to better understand the potential benefits and limitations of cardiovascular testing and training for the diverse SCI population. Research interest in SCI/ cardiovascular exercise physiology is a fairly recent phenomenon. Comprehensive reviews of research literature concerning the pathophysiology of SCI have covered cardiovascular responses to stressors such as postural tilt, sensory stimuli, autonomic dysreflexia, and pharmacologic agents during rest. 1-4 Conspicuously absent is any mention of acute adjustments or chronic adaptations to exercise training. Review of the literature reveals only six papers on this subject published before 1976, with the total number of papers now over 50. This topic has also been addres.sed in many review papers and book chapters during the last decade suggesting that this subject is gaining recognition in academic and clinical circles.5-25 VOLUNTARY ARM EXERCISE
Traditional rehabilitation medicine for SCI patients with functional levels below C4 has utilized therapeutic exercise to improve function of residual intact musculature. 26•27 Thus, voluntary use of the upper extremities has been emphasized to facilitate independence in wheelchair mobility, pressure relief, transfers, or other activities of daily living (ADL). These
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upper-extremity ADL tasks are necessary for survival in the community but are usually inadequate to promote cardiovascular fitness. 28·29 Preventive maintenance exercise programs at home also tend to emphasize upper-body fitness through weight training, wheelchair-accessible exercise courses, wheelchair aerobics, arm-crank or wheelchair ergometry, wheelchair propulsion, and wheelchair sports, with passive activities for the lower extremities such as stretching and standing in braces or a standing frame. 30 Wheelchair sports in particular have evolved from rehabilitative therapeutic activities to highly competitive events for elite upper-body athletes, 21 The upper-body musculature can clearly be trained for strength and endurance15 but, as will be discussed below, upper-body fitness is not usually synonymous with central cardiovascular fitness. The aforementioned arm exercise modes involve task-specific motor patterns involving small muscle groups that are not primarily designed to stress the normal central cardiovascular system. Generally, upper-body exercise modes do not engage a sufficient muscle m~ss to elicit the classical "maximal oxygen uptake" (V02 max) li.mited by the central circulation (e.g., cardiac output, Q).31 If the ability of the heart and circulation to supply blood and 02 exceeds the 02 demands within the relatively small exercising muscles, then the peak aerobic power will be limited primarily by peripheral factors within the muscles.32 Peripheral fatigue will occur before central hemodynamics are maximally stressed. In deconditioned able-bodied persons, arm exercise training may stress the cardiovascular system sufficiently to induce some beneficial central cardiovascular ch~nges. These may include increased peak arm exercise Q and stroke volume (SV).33 Most of the physiologic benefits, however, should be peripheral in nature (i.e., located within the trained muscles). Such peripheral training effects may include increased concentration of mitochondria, myoglobin and 02 storage, oxidative enzyme activity, muscle fiber size, and capillary density which facilitate 02 utilization at the muscle levei. 34.35 Recent research has contributed greatly to our understanding of acute physiologic responses in SCI individuals during exercise tests. 15 However, the precise nature of the cardiovascular training response to arm exercise is less well understood. Acute and chronic responses should be expected to vary with the level and completeness of SCI because the functional level determines (a) the residual muscle mass available to engage in exercise and (b) the degree of autonomic nervous system (sympathetic) function remaining to regulate the cardiovascular response to exercise.
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Exercise Response and Quadriplegia Complete quadriplegia is characterized by sensorimotor 33 losses over the majority of the body and by total separation of the peripheral sympathetic nervous system from control by the brain. Thus, the normal sympathetic outflow to heart, blood vessels, skeletal muscles, and adrenal medullae is interrupted at rest and during exercise. Remaining normal neurologic functions usually include diaphragmatic inspiratory control; some proximal upper-extremity innervation and sensation from associated muscles, joints and skin; and parasympathetic (vagal) control of viscera, including the heart. 36.37 Intrinsic tone of arterial and venous blood vessels,38 cardiovascular reflexes through the isolated spinal cord, l.3, 4.39•40 and/ or local metabolic processes in active muscles remain to regulate hemodynamic function throughout the body. Testing Individuals with functional levels of CS-Tl can perform arm ergometry (arm-cranking or wheelchair ergometry) at power outputs (PO's) commensurate with their residual upper-body musculature. During graded exercise tests, respiratory parameters (VD2, VC02,and pulmonary ventilation, VE) increase proportionally with PO, but peak values are usually lower than those of paraplegics during arm exercise and much lower than able-bodied persons performing large-muscle groups exercise (e.g., leg cycling or running).41 It is questionable whether or not the sympathetic nervous system is sufficiently activated to provide central circulatory support for voluntary arm exercise in persons with quadriplegia. In the upright sitting posture, peak heart ~ate (HR) is usually restricted to about 120 bpm, and Q SV and arterial blooq pressure (BP) are often subnormal for given levels of V02. 36AlA 2 Peripheral vascular insufficiency and inactivity of the skeletal muscle venous pump may induce excessive venous pooling in the legs and abdomen, reduce the circulating blood voi.ume and diminish venous return, thereby limiting SV, Q and blood flow to exercising arm muscles. Additionally, blood flow to metabolically less active areas would not be redistributed toward the active musculature. Quadriplegics are frequently hypotensive during upright arm exercise, due to vasodilation in exercising muscles for which peripheral vasoconstriction in the legs and viscera does not adequately compensate.42. 43
This dysfunctional syndrome of inadequate acute hemodynamic responses to increased metabolic demands has been named "circulatory hyp~kines~s" by several investigators.6•14·15·44-46 Values of VD2, Q, SV and HR during peak arm-crank exercise performed in the supine posture have been found to be significantl.(; higher than those in the upright sitting posture. 7
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Therefore, hypokinetic circulatory response may be partially attributable to the upright posture in which the exercise is performed. If upright posture induces pre-exercise central hypovolemia, then cardiac volumeloading becomes an even less likely effect of arm exercise in quadriplegia, further reducing the likelihood of central cardiovascular training effects. During voluntary arm exercise in quadriplegia, it may be impossible to accurately evaluate central cardiovascular fitness due to the inability of small muscles to maximally stress the heart. 18 Thus, the end point during maximal-effort arm exercise stress tests in otherwise healthy quadriplegics probably does not reflect the maximal capacity of the central cardiovascular system (i.e., pumping capacity of the heart, or ability of the heart to deliver blood and to exercising muscles). These tests do measure peak exercise capacity, as limited by the integration of all physiologic support systems under the specific conditions of the test (i.e., exercise mode, posture, etc.). The fatigue end point of these tests may reflect the following peripheral metabolic and/ or circulatory limitations: 13 1) the limited metabolic capacity of small muscles in the presence of a normal Q and muscle blood flow (i.e., where 02 supply exceeds the demand) 2) the inability of the peripheral vasculature to maintain sufficient arterial pressure in the presence of acutely vasodilated muscles and reduced total peripheral resistance, and/ or 3) subnormal venous return, relative to the desired level of 6 (due to impaired muscle pump and excessive venous compliance/venous pooling), resulting in red\}ced circulating blood volume, and inadequate Q and muscle blood flow.
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en
Training The primary stimulus for central circulatory (cardiac) improvement is an inc~ased volume-load on the heart (i.e., elevated SV and Q), which in able-bodied persons is proportional to the size of the muscle mass active during exercise training. 48 Central cardiovascular !"daptations are manifested by 1) higher peak SV and Q (reflecting an increased capacity to circulate blood) and/ or 2) lower HR and contractility at rest and during submaximal exercise (reflecting an increased cardiovascular reserve and decreased relative exercise intensity). If quadriplegics are unable to recruit a sufficient muscle mass during arm exercise to induce an adequate cardiac volume-load and stress the cardiovascular system, then we should not expect central cardiovascular training adaptations. Training studies have shown that exerci~ tolerance muscular endurance, peak PO, and peak can be improved in quadriplegia, but no evidence is available to support the presence of central cardiovascular training effects from upright voluntary
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arm exercise in quadriplegics. 42•49 Peripheral adaptations would nevertheless be valuable in assisting in performance of those activities of daily living, such as wheelchair propulsion, requiring muscular endurance.50 Given the difficulty of assessing maximal cardiovascular responses to arm exercise in quadriplegia without cardiac disease, it is equally difficult to determine changes in these parameters conseq';lent to training. For example, if a true maximal Q cannot be determined during arm exercise, then central cardiovascular reserve and, indeed, the relative degree of stress of any exercise, cannot be determined. If the previously mentioned peripheral limitations are reduced or removed (i.e., through the use of a horizontal posture, lower-body compression, recruitment of additional muscle mass through electrical stimulation, sympathomimetic agents, etc.), then exercise may be more likely to stress and train the heart. 47 Additional research is 33 needed in this area since the central cardiovascular trainability in quadriplegia (i.e., effect of training upon central hemodynamic function during rest or exercise) is largely unknown. Exercise Response and Paraplegia Compared with quadriplegia, complete paraplegia is characterized by less extensive sensorimotor losses and by only partial separation of the peripheral sympathetic nervous system from control by the brain. The physiologic responses to exercise in paraplegia may be more heterogeneous than in quadriplegia due to more variable innervation of the peripheral sympathetic system. Paraplegics with functional levels from T2-T4 have normal upper extremity muscle mass and partial sympathetic outflow to the heart. However, sympathetic outflow to blood vessels of the viscera, lower extremities and adrenal medullae are usually absent. The degree of sympathetic decentralization is directly dependent upon the level and completeness of SCI. The level of injury and presumed sympathetic function, however, appear to be poor predictors of upper-body exercise capability among paraplegics. For example, peak arm-crank or wheelchair exercise performance, as demonstrated in laboratory tests and wheelchair racing, vary ~atly with level of injury and medical classification. 1-53 In addition to aerobic and cardiovascular fitness, these performances may depend heavily upon proper biomechanical utilization of a large muscle mass that is highly trained for both aerobic and anaerobic work. 22 Testing In the upright sitting posture, paraplegics frequently demonstrate some circulatory hypokinesis during arm-crank exercise. 46 Although HR and arterial BP in paraplegia tend to be more normal than in quad-
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riplegia, Q _:md SV appear to be subnormal for given levels of V02. 46.54-56 Peak exercise performance is probably also limited by the same peripheral mechanisms as in quadriplegia, but to a lesser degree. Therefore, principles of ann exercise physiology and training for able-bodied individuals are likely to be more applicable to paraplegia than to quadriplegia. 15,32 Relatively little is known about cardiovascular and hemodynamic responses during wheelchair ergometry or racing. 57 However,. given similarities in active muscle mass and peak V02, acute and chronic responses to wheelchair exercise are not likely to differ markedly from responses to ann-cranking.58 Research is now in progress to evaluate wheelchair graded exercise testing as a tool to assess cardiopulmonary fitness and disease in disabled subjects using their own wheelchairs on stationary rollers.59
Training As is true for able-bodied persons, paraplegics may be able to use voluntary upright ann exercise to recruit a sufficient muscle mass to induce adequate volume and pressure loads on the heart to induce cardiac adaptations and improve cardiovascular fitness. Research has clearly show~! that arm strength, endurance, peak PO, and peak V02 can improve through arm training. 15•42. 60 To date, no specific central cardiovascular adaptations at rest or during exercise have been documented in paraplegics who have completed their acute rehabilitation. Moderate intensity wheelchair ergometer training has been shown, however, to increase high-density lipoprotein cholesterol (HDLC) concentration, as well as reduce triglycerides, low-density lipoprotein cholesterol, and the ratio of triglycerides to HDLC61 - changes that may lower the risk of eventual coronary heart disease. ELECTRICAL STIMULATION LEG CYCLE ERGOMETRY (ES·LCE)
In the quest for more effective techniques for cardiovascular testing and training of SCI individuals, the concept of using electrically induced contractions of paralyzed leg muscles has great physiologic appeal. Recruitment of the large lower extremity muscle mass and reactivation of the leg muscle pump to facilitate venous return may provide the SCI population with an aerobic exercise mode comparable to able-bodied bicycling or jogging.16 Research to evaluate the cardiovascular safety of two commercially available ergometers, the "ERGYS I" and "REGYS 1" (Therapeutic Technologies, Inc., TAMPA, FL), has elucidated several advantages and limitations of ES-LCE as currently used. These systems allow stationary leg cycle ergometry with 300 muscle contractions/min through microprocessor-controlled electrical stimulation delivered via skin surface electrodes to bilateral quad-
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riceps, hamstring, and gluteal muscle groups. The SCI user population to which ES-LCE is applicable is restricted to relatively healthy individuals with functional levels above T12, i.e., upper motor neuron SCI, with minimal residual skin sensation, and with no medical contraindication to ES-LCE.62 It should be remembered that this exercise technology is still in early development, and that any limitations or problems found regarding its use may be overcome with subsequent technological advancements.
Testing Metabolic studies using available ES-LCE instrumentation (i.e., ERGYS 1 and REGYS 1 ergometers) have revealed that this exercise mode is mechanically inefficient comgared with able-bodied cycling at equivalent PO's. 2.63 This energy wastefulness helps account for the low PO's used by SCI individuals even after several months of training. Physiologic responses, however, are high relative to the PO's, which is advantageous in terms of stimula!ing hem~dynarnic responses. ES-LCE typically elevates V02 and Q to approximately 1 1/min and 9 1/min, respectively, at a PO of about 10 W (i.e., 0.25 Kp load @ 42 RPM cadence).56·63-67 These responses correspond to disabled individuals performing wheelchair ergometry at 35 W or arm-cranking at 70 WP or to able-bodied persons walking at 3 MPH (4 METS, 300 kcal/hr). Aerobic exercise at this absolute intensity generally provides mild central cardiovascular conditioning with potential for significant caloric expenditure if performed regularly for sufficient periods of time (e.g., 60 min/session, 3-4 sessions/week). Compared with paraplegics, quadriplegics generally perform ES-LCE at slightly lower PO's which elicit proportionally lower levels of physiologic responses.54•676? However, mean peak hemodynamic responses (SV and Q) of quadriplegics during ES-LCE are significantly higher than those elicited during sub-peak and peak arm-crank exercise at equivalent V02levels, especially for quadriplegics with functional levels above C7.68•70 Therefore, ES-LCE appears to be more effective than arm-crank exercise for cardiac volume-loading quadriplegics. For paraplegics, sympathetically mediated responses such as HR and BP increase moderately during ES-LCE, suggesting that sympathetic nervous system activity is stimulated either by the peripherally applied (FNS-induced) muscular contractions and/ or through intact central command pathways.40.66·69 Whereas voluntary arm-cranking generates a higher peak HR in paraplegics, ES-LCE appears hemodynamically superior in terms of cardiac volume-loading. For both quadriplegics and paraplegics, this may be due to activation of the leg muscle venous pump, facilitation of venous return, and enhancement of cardiac preload and SV through the Frank-Starling mechanism56,69-71
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Training . Signific;ant training-induced increases in peak PO, V02 and VE have been reported by several inve.stigators, with little or no change in peak HR, SV, Q, MAP, and TPR after several weeks or months of ES-LCE training. 67·71 -74 Therefore, improved exercise performance following ES-LCE training appears to be due to peripheral adaptations that enhance muscular strength and endurance. ES-LCE training has also been reported to have minimal effects upon resting physiology. For example, some investigators have reported small increases in supine resting hemodynamic respon~s after an ESLCE training program (i.e., increased Q, HR and SBP by 0.33 1/min, 3-4 bpm, and 7 mmHG, respectively)?5·76 Others have found no changes in resting HR, BP, metabolic and respiratory parameters. 72 In summary, some individuals may benefit from ES-LCE training that utilizes the currently available technology. However, scientific research has yet to generalize the efficacy of ES-LCE as a central cardiovascular training tool for the SCI population. Although not the primary focus of this paper, several possible peripheral physiolo~c effects have been hypothesized by ES-LCE users. Most of these effects on skin, muscles, bones and joints await scientific documentation. However, they deserve attention due to their potential for preventing or treating specific SCI medical complications and improving the health of ES-LCE users. Peripheral effects which merit scientific investigation include the following: 1) Skin: skin blood flow, altered sitting pressure distribution, incidence of pressure sores, e.ffect on
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wound healing. 2) Muscle: muscular hypertrophy and its sequelae, ef-
fect on metabolic rate, utility as a measure for weight control/ obesity management and cosmesis, effect on paretic muscle strength for lower-extremity ADL, effect on spasticity. 3) Bone: rate of bone resorption or density; incidence of pathological fractures, hypercalciuria, renal calculi, and heterotropic ossification. 4) Joints: long-term effect on joint integrity, range of motion and incidence of contracture. 5) Lower extremity circulation: effect on lymphatic and venous circulation, on normalization of fluid content and distribution on reduced venous pooling/ stasis and on decreased blood coagulation; incidence of deep venous thrombosis, pulmonary embolism, orthostatic hypotension, edema and acrocyanosis; effect on cosmesis. COMBINED ARM+LEG (HYBRID) EXERCISE
In an attempt to further stress the cardiovascular system, initial a·ttempts have been made to combine volunta7a arm exercise with electrical stimulation leg exercise. S..SJ The combined arm+leg (hybrid) exercise may have the potential advantages of a) utilization of larger muscle mass, which may promote higher physiologic responses and improve fitness training capability, and b) the voluntary arm-crank component may elicit higher cardiovascular sympathetic activity and facilitate leg exercise performance. 82 Figure 1 illustrates a research hybrid exercise system consisting of a Monark Rehab Trainer TM arm-crank ergometer mounted on a specially built table to allow arm-crank-
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ing while pedaling the "ERGYS 1" ergometer. 17 Other arm+leg ergometers for disabled individuals are also commercially available with the paralyzed leg muscles driven actively by electrical stimulation ("Power Trainer," Sinties Scientific Corp., Tulsa, OK) or passively by mechanical linkage to the arm cranks ("Pedal-InPlace," Thoele Mfg., Montrose, IL). At present, physiologic responses to use of these devices have yet to be clinically or scientifically evaluated.
with possible dizziness, nausea, and extreme fatigue. In summary, while hybrid exercise can induce higher peak physiologic responses acutely in some individuals, the two exercise modes may interact with each other and may not be tolerated by some quadriplegics. As with therapeutic exercise, the optimal combinations of arm and leg exercise may need to be individualized according to the tolerance and needs of each person.
Testing
Training
Recent research findings are redefining the upper limits of peak exercise performance for SCI individuals, especially for quadriplegics. For example, in a group of untrained quadriplegics who performed a maximal-effort graded arm-cran}< exercise test during "0" -W ESLCE, peak values of VCh Q, SV and JR were increased significantly by 35, 46, 26 and 18%, respectively, above levels observed during peak arm-cranking witl}out ESLCE.81 Therefore, the ability to increase peak Q above that for arm-cranking alone strongly suggests that peak vo2 is limited more by peripheral factors such as active muscle mass and venous insufficiency rather than by central cardiac factors. The increments of the peak arm+leg physiologic responses above resting levels appeared to be an additive function of the arm and leg exercises performed separately. On the other hand, untrained paraplegics responded to combined peak arm-crank exercise and 0-W ES-LCE with an increased peak VOl but with little or no increment in peak Q, suggesting a central circulatory limitation during peak hybrid exercise (unpublished observations). It may be possible to drive peak physiologic responses during arm+leg exercise to even higher levels with a more effective form of electrical stimulation involving additional muscle groups, use of "gravity-eliminated" posture or environment, or hybrid exercise training. Systemic sympathetic impairment may ultimately limit exercise performance with relatively large muscle groups, especially in quadriplegics. Combining peak voluntary arm-cranking with increasing amounts of voluntary and/ or electrically induced leg cycling has been shown to induce increasing degrees of exercise hypotension. 83 The arterial pressure gradient (represented by the mean arterial pressure, MAP) and total peripheral resistance (TPR) are the basic hemodynamic determinants of cardiac output (Q =MAP I TPR). Extensive vasodilation of a large proportion of the muscle mass (i.e., decreased total peripheral resistance, TPR), combined with impaired compensatory ability to vasoconstrict other arterial vessels and increases HR and myocardial contractility (i.e., increase mean arterial presspre, MAP), will preclude maintenance of BP.84 Hence, Q and perfusion of vital organs such as the brain will decrease, resulting in exercise hypotension
Training studies with hybrid exercise are currently in progress at the VA Medical Center and Wright State University School of Medicine in Dayton, OH. 85 While an earlier studyll2 found that voluntary arm exercise facilitated electrically induced knee extension resistance exercise, more recent research indicates that simultaneous voluntary arm and ES-LCE may interfere with each other when performed in the upright sitting posture. That is, when moderate-intensity arm-cranking is added to a bout of relatively high-level ES-LCE, some SCI individuals respond with a decrease in ESLCE performance. At the present time, it is speculative if the nature of the limitation is mechanical (upperbody exercise interfering with lower-body exercise), circulatory (legs not competing successfully with the arms for their limited share of blood flow, especially in the presence of orthostatic hypotension or excessive venous pooling), humoral (increased metabolic acidosis from the arms interfering with the legs), or a combination of the above or other unknown factors. Some evidence from able-bodied subjects supports the circulatory hypothesis. 86 When arm exercise was added to leg exercise, Q increased but leg blood flow decreased. Apparently the heart could not supply both the legs and the arms with blood because the combined demands exceeded the pumping capacity of the heart. 87 It is not known if this interaction will be a function of training status, level of injury, sympathetic impairment, medications or other specific characteristics of SCI individuals. Individuals who can tolerate activation of a very large muscle mass will be able to take advantage of the greater metabolic and circulatory loads that hybrid exercise can generate. FUTURE RESEARCH In the future, researchers need to investigate several major questions in SCI/ cardiovascular exercises physiology. First, what exercise mode will enable high-level, yet safe, cardiac volume-loading in SCI individuals? Can the sympathetic nervous system be stimulated to provide appropriate support of highlevel aerobic metabolism? A challenge for future research is to develop techniques to maintain arterial pressure and increase peripheral resistance in inactive areas of the body, so that Q can be maintained during
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large muscle group exercise in SCI subjects with profound sympathetic impairment. Secondly, a major thrust of future research should address the central versus peripheral trainability in quadriplegics and paraplegics for various modes of voluntary and/or electrically induced exercise training. We need to define the relationships between physiologic training effects and specific parameters of health and functional independence. What level of exercise metabolism and central circulation must be achieved to develop and maintain general physical fitness and wellness? Is the arm muscle mass large enough to provide sufficient training stimulus to improve resting peripheral and central circulatory function? Thirdly, what are the clinical benefits of increased cardiovascular fitness? Can it help control orthostatic hypotension, increase skin blood flow and pressure tolerance of skin, prevent excessive venous pooling and lymphedema, and reduce the incidence of deep venous thrombosis and other circulatory disorders? Can exercise training play the same role in preventative health care as in the able-bodied population88primary and secondary prevention of heart disease through modification of coronary risk factors such as obesity, hypertension and hyperlipidemia; and prevention of osteoporosis? Does exercise enhance mental health, improve affect, and increase self-esteem? Given the pathophysiologic diversity within the SCI population, the use of single-subject experimental research designs should be considered along with traditional group research designs to better evaluate the effects of training upon specific medical conditions/ dysfunctions and patient-treatment interactions. 89 This approach can generate clinically relevant information for immediate use by practitioners. Scientific documentation of medical indications may facilitate acceptance or rejection of these exercise modalities for more widespread clinical use.
SUMMARY SCI often impairs the ability of individuals to perform large-muscle-group aerobic exercise. The exercise modes currently being studied include voluntary armcranking and wheelchair exercise, electrical stimulation leg cycle ergometry, and combined voluntary arm and electrical stimulation leg (hybrid) exercise. When paralyzed muscle can be activated electrically and added to the residual voluntary muscle mass, the intensity and duration of exercise may be limited by sympathetic nervous system impairment, which is more severe in individuals with higher-level and more complete SCI. However, hybrid exercise shows promise in terms of volume-loading the heart and inducing central cardiovascular training effects in SCI individuals. Ongoing research aims to develop hybrid exercise instrumentation that maximizes appropriate physiologic
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responses, that is tolerated by and available to more SCI individuals, and that provides beneficial general cardiovascular conditioning as well as a therapeutic modality for selected medical conditions. More research is needed to establish the medical efficacy of electrical stimulation in the treatment of specific pathologies and dysfunctions.
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