Theme Issue: Exercise and Sports

Exercise and Sport for Persons With Spinal Cord Injury Kathleen A. Martin Ginis, PhD, Sophie Jörgensen, MD, Jessica Stapleton, MSc Abstract: This review article provides an overview of the evidence that links exercise and sports participation to physical and psychological well-being among people with spinal cord injury. Two aspects of physical well-being are examined, including the prevention of chronic disease and the promotion of physical fitness. Multiple aspects of psychosocial well-being are discussed, including mental health, social participation, and life satisfaction. The review concludes with future research recommendations and a discussion of challenges and opportunities for using exercise and sports to promote health and well-being among people living with spinal cord injury. PM R 2012;4:894-900

INTRODUCTION People living with a spinal cord injury (SCI) face many challenges and barriers to physical activity participation [1,2]. Consequently, this population is considered to be the most physically inactive segment of society [3] and is especially vulnerable to diseases that have been linked with a sedentary lifestyle (eg, cardiovascular disease [CVD], diabetes mellitus). Physical inactivity can also exacerbate the risk for many secondary health problems that are common among people with SCI, such as pressure sores and chronic pain [4], and may compromise aspects of psychological well-being, social participation, and overall quality of life [5-7]. Systematic efforts to increase exercise and sports participation could have substantial benefits on the physical well-being and psychosocial well-being (PSWB) of people with SCI [8,9]. Exercise is planned, structured, and repetitive physical activity intended to improve or maintain fitness [10], whereas sport is typically a competitive form of physical activity governed by rules [7]. The purpose of the present article is to provide an overview of the evidence regarding the benefits of these 2 types of activity. We begin by examining the role of exercise and sports in 2 aspects of physical well-being, the prevention of chronic disease and the promotion of physical fitness, followed by their role in promoting aspects of PSWB. The article concludes with a discussion of opportunities and challenges for using exercise and sports to promote the health and well-being of people living with SCI.

THE ROLE OF EXERCISE AND SPORTS IN PREVENTING CHRONIC DISEASE After an SCI, the body undergoes changes in composition and metabolism [11], and physical activity and daily energy expenditure often decline dramatically (compare [12]). These sequelae increase the risk for obesity and obesity-related conditions such as CVD and diabetes [4]. The prevalence of overweight and obesity in the SCI population is conservatively estimated at 66% [13]. Furthermore, circulatory diseases (including CVD) are the most common causes of death in people with chronic SCI [14], and CVD is the leading cause of death in individuals with SCI age ⬎60 or ⬎30 years after injury [15]. People with SCI may have increased risk for the early development of CVD due to an increased prevalence of hypertension [16], adverse lipid profile changes [17], and impaired glucose tolerance and/or diabetes mellitus [18]. Indeed, diabetes mellitus and impaired glucose tolerance tend to be more prevalent in the SCI population than in the general population, and those with the greatest neurologic impairment may be the most susceptible [11]. Of further concern, people with SCI who are overweight or obese, or who have PM&R

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K.A.M.G. Department of Kinesiology, McMaster University, Hamilton, Ontario L8S 4K1, Canada. Disclosures related to this publication: grant (paid to institution), Community-University Research Alliance Grant from the Social Sciences and Humanities Research Council of Canada. Disclosures outside this publication: none S.J. Department of Rehabilitation Medicine, Skåne University Hospital, Lund, Sweden; Department of Health Sciences, Lund University, Lund, Sweden. Disclosure: nothing to disclose J.S. Department of Kinesiology, McMaster University, Hamilton, Ontario, Canada. Disclosures related to this publication: grant (paid to institution), Community-University Research Alliance Grant from the Social Sciences and Humanities Research Council of Canada. Disclosures outside this publication: none

© 2012 by the American Academy of Physical Medicine and Rehabilitation Vol. 4, 894-900, November 2012 http://dx.doi.org/10.1016/j.pmrj.2012.08.006

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diabetes report more comorbidities and a poorer quality of life than those who have not developed these conditions [19,20]. In the general population, the association between physical activity and risk for obesity, CVD, and diabetes is well established [12,21]. In the SCI population, relatively little is known about the role that physical activity plays in reducing these risks. Nevertheless, physical activity has been suggested as possibly playing an important role [12,22-24] in maintaining wellness. To address this possibility, one cross-sectional study compared obesity, CVD, and diabetes risk factors among physically inactive and active men and women with paraplegia or tetraplegia [25]. Active participants were classified as those reporting ⱖ25 min/d of leisure time physical activity (eg, sports, exercise), whereas inactive participants reported 0 min/d of these activities. Body mass index, fat mass, and the proportion of people with insulin insensitivity were significantly greater in the inactive group. Inactive people also had significantly greater levels of another risk factor linked to CVD, the inflammatory marker C-reactive protein. There, however, were no between-groups differences in high-density lipoprotein cholesterol or any other lipid measure. Notwithstanding the limitations of the crosssectional study design, these results suggest that physical activity is linked to chronic disease risk factors. To our knowledge, no single training study has looked at changes in all of these risk factors simultaneously, but individual risk factors have been examined in individual studies of persons with SCI. With regard to changes in body fat, most interventions have failed to produce significant reductions in fat mass (for a review, see Hicks et al [26]), with the exception of some lower-quality functional electrical stimulation (FES)cycling studies [27,28]. With regard to changes in glucose metabolism, there is evidence that physical activity has a positive effect [4,23], and, more specifically, body-weight– supported treadmill training (BWSTT) has been shown to increase glucose tolerance and insulin sensitivity [29]. Furthermore, several reviews of the SCI literature conclude that exercise improves lipid profiles, mostly by increasing the level of the cardioprotective high-density lipoprotein cholesterol [4,12,22,29]. With regard to the effects of sports participation on chronic disease prevention among persons with SCI, preliminary evidence indicates potential protective benefits. For instance, there is some evidence that sports participation is associated with greater lean mass and lower fat mass. More specifically, upper limb fat mass and lean mass ratios have been shown to be better among athletes with SCI than nonathletes [30,31]. Participation in sports has also been associated with greater insulin sensitivity [32] and higher high-density lipoprotein cholesterol levels [32-34]. When taken together, research on the association between exercise and sports participation and on chronic disease prevention has yielded some encouraging findings. However,

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it is still not clear what intensities, durations, and specific types of activity are needed to reduce the risk of developing different conditions. The extant data should also be interpreted with some caution, because most studies are limited by factors such as unrepresentative samples, cross-sectional designs, and potentially imprecise measures of physical activity. Although we recognize the tremendous challenges associated with conducting exercise and sports training studies in persons with SCI [35], more training studies are needed to substantiate assertions that physical activity may decrease risk factors for chronic disease among persons with SCI.

THE ROLE OF EXERCISE AND SPORTS IN ENHANCING PHYSICAL FITNESS Physical activity guidelines for adults with SCI state that, to achieve important fitness benefits, adults should engage in at least 20 minutes of moderate to vigorous intensity aerobic activity twice a week. Adults should also perform strength training exercises twice a week, which consists of 3 sets of 8-10 repetitions of each exercise for each major muscle group [36]. These guidelines were generated after a systematic review of 82 exercise training studies, which focused on 4 aspects of physical fitness: physical capacity, muscle strength, body composition, and functional performance [26]. In the following paragraphs, that systematic review is used as a basis for summarizing what is known regarding the effects of exercise training on fitness among people with chronic SCI. For each fitness outcome, we also summarize the relatively sparse research regarding the effects of sports participation on that particular outcome.

Physical Capacity Physical capacity reflects the amount of physical work a person can do and is captured by measures of aerobic capacity and power output. Greater aerobic capacity is associated with better cardiovascular health and fatigue resistance. In addition, a person’s power output can positively impact his or her functional independence by enhancing the ability to perform multiple activities of daily living (ADL) such as propelling one’s wheelchair and performing transfers [26]. By drawing on the results of 46 training studies, the systematic review by Hicks et al [26] concluded that there was strong evidence of (a) the effects of FES-assisted exercise, arm ergometry, and wheelchair exercise on aerobic capacity; and (b) the effects of FES-assisted exercise and combined aerobic and strength-training on power output. When turning to the sports literature, analysis of the limited evidence suggests that sports participation is associated with a variety of cardiovascular improvements. Cardiac hypertrophy, maximal work rate, maximal oxygen consumption, maximal lactate level [37], and pulmonary function [38] have all been shown to be greater in athletes with SCI

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compared with sedentary individuals with similar injuries. Regardless of their injury level, it has been repeatedly demonstrated that athletes with SCI can achieve and maintain exercise intensities sufficiently high to improve cardiorespiratory fitness [39-41] and that hours of training explain significant variance in physical capacity among wheelchair athletes [42,43]. Interestingly, analysis of preliminary data suggests that people with SCI tend to participate in sports at higher intensities and longer durations than they participate in exercise [44]. These data encompass a variety of aerobic and anaerobic sports (ie, wheelchair basketball, track, rugby, and swimming). Together, analysis of these results suggests that sports may be a particularly effective type of physical activity for maximizing cardiorespiratory fitness benefits.

Muscular Strength After an SCI, individuals experience a loss of muscle mass due to denervation and inactivity, and a concomitant decrease in strength. The importance of muscle strength cannot be overstated. It is crucial for functional independence and for reducing the risk of overuse injuries and pain in the upper extremities. Moreover, because muscle mass is metabolically active, if changes in muscle strength are accompanied by changes in muscle mass, such increases could positively affect metabolism. By drawing on the results of 22 exercise training studies, Hicks et al concluded that there is strong evidence that muscular strength can be significantly improved with a variety of exercise training modalities, including circuit resistance training, BWSTT, arm ergometry, and FES-assisted exercise [26]. We are unaware of any studies that examined strength gains associated with sports participation. However, it seems intuitive that many sports (eg, those that involve propulsion, such as wheelchair basketball, rugby, tennis) would increase upper body strength. Research is needed to quantify the magnitude of these improvements across sports.

Body Composition Increased fat mass and the loss of lean mass after SCI contribute to the development of secondary health complications and chronic disease, and can lead to problems with transfers, poorer functional outcomes, and the need for more specialized equipment and assistance [45]. In addition, bone mineral density (BMD) decreases rapidly after SCI as the result of neural, vascular, and hormonal changes, thus increasing the risk of osteoporosis and fractures [46]. In the 24 studies reviewed, there was insufficient evidence from highquality studies to draw firm conclusions about the effects of exercise on body composition [26]. Of note, most training studies failed to produce reductions in body fat, but many yielded significant increases in lean mass. FES-assisted exercise appears to be a particularly promising intervention in

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this regard. BMD was not included in the systematic review because so few studies included this outcome. However, a separate review reported that frequent FES exercise seems to increase BMD in those persons with chronic SCI [29], whereas ambulation training (eg, BWSTT) has failed to show the same beneficial effects [4,29]. In the sports literature, as previously noted, there is some evidence that sports participation is associated with higher lean mass and lower fat mass [30,31]. However, these outcomes may hinge on sports training that occurs at sufficiently high intensities and durations [30]. In addition, similar to the benefits observed for FES exercise, analysis of preliminary evidence suggests that sports training may improve BMD. In particular, 2 studies reported that athletes with SCI have greater upper body BMD than their inactive counterparts [31,47]. Interestingly, one of these studies [31] reported no differences in the total BMD of athletes with SCI when compared with able-bodied controls. The researchers attributed this finding to greater upper body BMD in the athletes, which may compensate for their reduced lower-body BMD.

Functional Performance Given the declines in physical capacity and strength that occur after an SCI, it is not uncommon for people to have insufficient residual function to independently perform functional ADL. Indeed, it is estimated that only 25% of healthy young persons with paraplegia have the bare minimum level of fitness needed to maintain independent living [48]. Hicks et al [26] reviewed 24 training studies that measured functional performance outcomes of walking, standing, and wheelchair propulsion. The evidence was insufficient to draw conclusions regarding the overall effects of exercise on these outcomes. On the one hand, the researchers noted mixed lower- and higher-quality evidence regarding the effects of step training (eg, BWSTT, FES-assisted overground walking training) on overground walking. On the other hand, they found consistent low-quality evidence that arm, wheelchair, and rowing ergometry can improve wheelchair skills and propulsion. A separate, small review of 6 studies reported on the effects of exercise interventions on additional types of functional outcomes, such as performing transfers, self-care, and other ADLs [2]. These studies involved a mix of acute and chronic SCI samples. The highest-quality study reviewed reported significant improvements in motor Functional Independence Measure scores (Uniform Data System for Medical Rehabilitation, Amherst, NY), body care, and transfers after 4 months of swimming, 2 days a week [49]. The results of the lower-quality studies were generally similar. It is noteworthy that these studies incorporated different modes of exercise (eg, FES-assisted exercise, arm ergometry, BWSTT) and typically showed increased overall Functional Independence Measure scores and/or improved performance of select ADLs.

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Very little research has been published regarding the effects of sports on functional performance. However, one study reported that as little as an hour per week of sports participation improved wheeling, transfers, and the ability to open and close a sliding door [50]. This study also showed that sports improved physical capacity, which may have contributed to the functional improvements. In addition, paralympic athletes with SCI have reported that sports was one of the avenues by which they acquired their most essential wheelchair mobility skills [51]. Together, analysis of these data suggests that sports could improve functional performance through a continuum of mechanisms, which range from basic improvements in physical capacity to the development of advanced mobility skills. In summary, when looking across the fitness research, there is good evidence that physical capacity and strength are improved through exercise and seemingly through sports participation as well. Effects on body composition are unclear; it is possible that certain outcomes (eg, changes in BMD) are linked to certain types (eg, FES, sports) and amounts of activity. The effects of physical activity on functional performance have been understudied, but sports may be a particularly potent training ground for developing mobility skills.

THE ROLE OF EXERCISE AND SPORTS IN ENHANCING PSWB PSWB refers to a broad category of phenomena that includes mental health, community integration, social participation, and overall life satisfaction. A considerable body of research in the able-bodied and some clinical populations (eg, cardiac rehabilitation patients, cancer patients) indicates that physical activity is associated with improvements in a wide range of psychosocial outcomes [52]. However, there is relatively little research of this issue among people living with SCI. This is unfortunate; people with SCI often score lower than ablebodied people on indices of PSWB [5,53] and are in particular need of PSWB-enhancing interventions. Analysis of emerging data suggests that exercise and sports could be effective. For example, Martin Ginis et al [44] conducted a metaanalysis of 21 studies that examined the association between exercise and sport participation and indices of PSWB. Indices included measures of affect (eg, stress, anger), mental health (eg, depressive symptoms, self-concept), satisfaction with important domains (eg, satisfaction with appearance, functioning), and overall life satisfaction. Despite a broad range of measures used in these studies, as well as a mix of study designs, the investigators found a significant association between physical activity and PSWB overall, with an average effect of r ⫽ .25. Similar-sized effects were found for separate meta-analyses of depressive symptoms (r ⫽ .22) and life satisfaction (r ⫽ .23). However, the effect sizes were larger

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(range, .27-.45) when the meta-analyses included only those studies that implemented some type of sports or exercise intervention (and excluded cross-sectional studies), which suggests that medium- to large-sized effects might be expected when physical activity is applied as a treatment modality. A separate review examined the role of exercise and sports in facilitating community integration and social participation after SCI [7]. Research on these topics is especially difficult to interpret given the variety of operational definitions and measures that have been applied. Nevertheless, the reviewers cited preliminary evidence that athletes score higher on measures of community integration than nonathletes [54]. They also cited several examples of community-based exercise and sports initiatives that provided opportunities for enhanced social participation and integration. One of the most compelling examples was a study that describes how 6 athletes with SCI used an FES-assisted indoor rowing system to train and successfully compete with able-bodied rowers in major indoor rowing events [55], thus highlighting the potential for sports to provide opportunities for full integration. Taken together, the exercise and sports literature consistently reports positive associations between physical activity participation and PSWB. However, most of these studies have been cross-sectional, with little consistency in the PSWB constructs and measures used. Although the evidence is promising, it is premature to draw firm conclusions regarding the effectiveness of physical activity for improving specific aspects of PSWB in persons with SCI.

RESEARCH CONCLUSIONS AND FUTURE DIRECTIONS The purpose of this article was to review evidence regarding the benefits of exercise and sports participation on physical well-being and PSWB among people with SCI. With regard to physical well-being, the evidence is strongest regarding the benefits of physical activity on physical fitness, particularly physical capacity and muscular strength. The evidence is weakest regarding the effects of physical activity on reducing risk for chronic disease, because the exercise studies have yielded inconsistent results that are difficult to interpret and synthesize given methodologic limitations and inconsistencies. Studies of sports participation and disease risk are virtually nonexistent. It is noteworthy that SCI researchers have typically focused on risk reduction for just 3 diseases: obesity, diabetes, and CVD. In the general population, physical activity has been linked to more than 25 chronic conditions, including cancer, stroke, and osteoporosis [56]. Although some might argue that these linkages should be assumed to hold among people with SCI, there is still a need to study the extent to which activity mitigates risk in this population. It is also necessary to determine the types, amounts, and intensities of activity that are linked to risk

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Table 1. Barriers to physical activity for persons with SCI* Type

Barrier

Description

Intrapersonal

Physical health factors

Autonomic dysreflexia, thermal dysregulation, circulatory dysregulation, musculoskeletal injury, recurring infections Depression, lack of motivation, lack of energy, lack of time, lack of activity skill, lack of interest, lack of self-confidence, fear of pain and injury, fear of failure, fear of embarrassment, fear of conspicuous or unfriendly exercise environments, worry concerning physical limitations, perceive exercise as boring or too difficult, dislike of exercise Equipment (eg, inadequate transfer space, difficulty operating equipment independently), facilities (eg, small space, heavy doors), outdoor environment (eg, steep or uneven terrain, lack of sidewalks, poorly maintained sidewalks, lack of curb cuts, inclement weather, neighborhood crime rate), limited accessible transportation High cost of transportation, programs, equipment, and membership Development of an exercise program to meet guidelines about types of activities that are appropriate, execution of exercises, play of adapted sport Exercise program availability, adapted sport availability Failure of physicians to discuss PA, fitness professionals lack of SCI-specific PA knowledge

Psychological factors

Systemic

Accessibility

Informational

Financial cost Lack of knowledge

Lack of awareness Experts SCI ⫽ spinal cord injury; PA ⫽ physical activity. *Table information is compiled from Refs 1,8,59-61.

reduction so that physical guidelines and prescriptions can be developed to prevent these conditions. With regard to PSWB, there are consistent findings that exercise and sports participation are associated with better PSWB. Although PSWB encompasses a wide range of constructs, depressive symptoms and life satisfaction have received the most research attention in the SCI literature [44]. In contrast, results of research in the general population have shown that exercise and sports interventions can improve a wide range of psychosocial outcomes, such as mood, pain, stress, body image, and self-esteem [52]. Presumably, people with SCI also derive these benefits from physical activity, but research is needed to determine what exercise prescriptions are most effective. Researchers should also focus on the unique benefits of physical activity to people with SCI. For instance, sports may be a powerful catalyst for enhancing social participation and community integration. Research that addresses these issues could inform the development of interventions to improve PSWB in persons with SCI.

CLINICAL IMPLICATIONS Based on the extant evidence, SCI clinicians should promote sports and exercise as means to improve physical fitness. Because “physical fitness” can be a nebulous term for many patients, clinicians must explain the importance of strength and endurance for performing ADL, maintaining independence, and ultimately affecting quality of life. In addition, patients with acute SCI need to know that their bodies will change after injury and that some of these changes (eg, decreased strength and conditioning) can be mitigated by physical activity. The expectation of such physical benefits

and the opportunity to regain some control over one’s body can be motivating. Patients may also be motivated by the potential psychosocial outcomes of activity, such as reduced pain and stress, or enhanced mood and self-esteem. Although there may be some risks associated with physical activity participation (eg, overuse injuries, increased risk for autonomic dysreflexia), the benefits far outweigh the risks [26]. Clinicians need to be aware of these benefits so that they can help their patients find personally meaningful reasons to be active. Such reasons are integral to sustained physical activity motivation and participation. Motivation is just one piece of the physical activity promotion puzzle. People with SCI must also learn to identify, manage, and overcome numerous intrapersonal, systemic, and informational barriers to sports and exercise participation. An evidence-based summary of these barriers is provided in Table 1. An evidence-informed list of potential facilitators is provided in Table 2. Although only a few studies have tested strategies to target these barriers and facilitators in persons with SCI, positive effects have been observed for interventions that incorporate elements such as action planning, goal setting, and self-monitoring [2]. Videos, manuals, and other tools are available to facilitate clinicians’ use of these strategies with their patients (eg, www.ncpad.org; www.sciactioncanada.ca).

SUMMARY Emerging evidence indicates that exercise and sports can have significant physical and psychosocial health benefits for people with SCI. Although there are many challenges to physical activity participation in this population, the

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Table 2. Evidence-informed examples of facilitators to physical activity for persons with SCI* Type Intrapersonal

Facilitator Action planning Coping planning Goal setting Seeking social support

Systemic

Informational

Advocacy and support organizations

Physical activity counseling services Building codes Subsidized fitness memberships Evidence-based resources Awareness of local resources Experts

Description and/or Examples Specifying where, when, and how to engage in PA Planning ways to manage anticipated barriers to PA to achieve goals Using SMART goals: specific, measurable, accomplishment oriented, realistic, time bound Sources: physicians, health and fitness professionals, rehabilitation staff, teammates, family, friends, caregivers Canadian Paraplegic Association, SCI Action Canada, Swedish Sports Organization for the Disabled, Canadian Paralympic Committee, Swedish Paralympic Committee, NCPAD, Canadian Wheelchair Sports Association, Christopher and Dana Reeve Foundation NCPAD, Get in Motion Establish and enforce policies to reduce accessibility issues Adjust costs for individuals with disabilities based upon limited access to certain facilities Manuals, videos, guides, Web sites (http://ncpad.org/; http://sciactioncanada.ca/) Alternatives to gyms or health clubs: shopping malls or outdoor tracks Clinicians talk to patients about physical activity; health and fitness professionals trained to provide exercise assistance and resources to people with SCI

SCI ⫽ spinal cord injury; NCPAD ⫽ The National Center on Physical Activity and Disability; PA ⫽ physical activity. *Table information has been drawn from Refs 1,8,59-61.

potential benefits of enhanced participation can be tremendous. Given that people with SCI consider health care professionals to be an important source of physical activity information [57,58], we urge clinicians to talk with their patients about the importance of being physically active. The promotion and facilitation of physical activity are key to improving physical well-being and PSWB in persons living with SCI.

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