Narrative Review

Physical Activity, Exercise, and Health-relatedMeasures of Fitness in Adults With Spina Bifida:A Review of the LiteratureTheresa M. Crytzer, DPT, Brad E. Dicianno, MD, Roohi Kapoor, MPT

T.M.C. Human Engineering Research Labo-

Spina bifida (SB) is the most common birth defect in United States that results in per-manent lifelong disability according to the Spina Bifida Association. Advancements inmedical care have led to a longer life span and an increase in the risk of secondary con-ditions, for example, obesity, with age. The need to maintain a healthy and active lifestyle iseven stronger in adults with SB than the general population. Our objective was to fill a gapin the literature by highlighting the current state of the literature on health-related measuresof fitness, exercise, and physical activity (PA) in adults with SB. PubMed and Ovid weresearched for articles by using the terms “spina bifida or myelomeningocele and exercise,”published between January 1, 1988 and May 10, 2012. Results of studies showed thatadults with SB had an inactive lifestyle, lower aerobic capacity, decreased level of daily PA,higher prevalence of obesity, and lower health-related quality of life compared withreference groups. Therapeutic interventions reduced pain, increased biomechanical effi-ciency during wheelchair propulsion, and improved PA and balance. Overall, the quality ofthe evidence on PA, exercise, and health-related measures of fitness is low in SB. Givenmisdistribution of adipose tissue, short stature, scoliosis, and joint contractures, futureresearch should be conducted to determine the most reliable and low-cost methods ofmeasuring body composition and to establish norms. Other reference standards, forexample, aerobic capacity, require further development. Studies are needed to investigatelifestyle interventions that facilitate PA and exercise, and to determine the amount of ex-ercise required to reduce secondary conditions as people with SB age.

PM R 2013;5:1051-1062

ratories, Veterans Administration PittsburghHealthcare System, Pittsburgh, PA; Rehabili- tation Science and Technology, University ofPittsburgh, Pittsburgh, PA; Center for AssistiveTechnology, University of Pittsburgh MedicalCenter, Pittsburgh, PADisclosure: nothing to disclose

B.E.D. Human Engineering Research Labora-tories, Veterans Administration PittsburghHealthcare System, Pittsburgh, PA; Rehabili-tation Science and Technology, University ofPittsburgh, Pittsburgh, PA; Center for AssistiveTechnology, University of Pittsburgh MedicalCenter, Pittsburgh, PA; Adult Outpatient SpinaBifida Clinic, University of Pittsburgh MedicalCenter, Pittsburgh, PA; Spina Bifida Clinic,Children’s Hospital of Pittsburgh, University ofPittsburgh Medical Center, Pittsburgh, PA;Department of Physical Medicine and Reha-bilitation, University of Pittsburgh MedicalCenter, Kaufmann Medical Building, Suite202, 3471 5th Avenue, Pittsburgh,PA 15213. Address correspondence to:B.E.D.; e-mail: dicianno@pitt.eduDisclosure: nothing to disclose

R.K. Indian Spinal Injuries Centre, New Delhi,IndiaDisclosure: nothing to disclose

Submitted for publication February 14, 2013;accepted June 29, 2013.

INTRODUCTION

Spina bifida (SB) is a birth defect caused by incomplete closure of the neural tube andprotrusion of spinal membranes and nerves during the early days of gestation [1]. SB is themost common birth defect today that results in permanent disability, according to theSpina Bifida Association [1]. In the United States, approximately 8 children per day areborn with SB [2]. The Spina Bifida Association reports that 7 of every 10,000 children bornin the United States have this condition and that there are more than 166,000 peoplecurrently living with SB [3]. Myelomeningocele is the most severe form and results inpartial or complete motor and sensory loss below the level of the lesion [3].

Individuals with SB have a variety of complications, including limitations in mobility,cognitive impairments, orthopedic deformities, psychosocial issues, bowel and bladderproblems, and other limitations that require extensive multidisciplinary medical care [4].As a result, people with SB are often at risk for developing an inactive lifestyle. Thus, avicious cycle is created with the hypoactive lifestyle, which leads to decreased musclestrength and endurance, an increase in body fat, and a reduction in stamina, which in turnlimits functional independence and may considerably affect quality of life [5,6]. Physicalactivity (PA) is known to lower the risk of cardiovascular disease and to promote health inpeople without disabilities by increasing high-density cholesterol levels and reducingarterial blood pressure in those with hypertension and through favorable effects on glucosetolerance and bone density [5].

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1052 Crytzer et al FITNESS IN ADULTS WITH SPINA BIFIDA

Advancements in medical and surgical care haveconsiderably increased the life expectancy of people with SB,which results in at least 75% of children surviving well intoadulthood [7]. Consequently, maintaining a healthy lifestyleto improve quality of life and prevent development of sec-ondary lifestyleerelated conditions has assumed topimportance. In addition, adulthood leads to a reduction inthe PA level and an increase in body mass. In a study byDosa et al [8], the obesity rate among adults with SB was37% (n ¼ 94), more than twice the rate for children andadolescents with SB (18% [n ¼ 34]). Extreme obesity wasprevalent in 11% of adult women and 4% of adult men withSB [8]. Obesity may lead to further deterioration in functionby causing difficulties with transfers and manual wheelchairpropulsion, a decline in ambulatory status, an increased riskof developing pressure sores, and other complications [9].Therefore, regular exercise and daily PA is particularlycrucial for adults. However, for some individuals, having aphysical disability is a barrier to exercise when compoundedby personal and environmental deterrents. The PhysicalActivity for People with a Disability model developed by vander Ploeg et al [10] heightens awareness of the role thatenvironmental and personal factors play in achieving regularPA involvement for individuals who have conditions thathave multisystem involvement, for example, SB.

By understanding the daily PA levels of adults with SB,factors that affect PA behavior, their cardiovascular fitnesslevel, their therapeutic programs, and the use of technologyin exercise, we can guide the establishment of exercise in-terventions and improve PA levels in adults with SB. In thisarticle, we will discuss the current state of the literature onthe PA level and therapeutic exercise interventions of adultswith SB and suggest areas of future research.

METHODS

A review of publications was performed by using PubMedand Ovid (Ovid Technologies Inc, New York, NY). Thesearch terms used were “spina bifida or myelomeningoceleand exercise.” The limits were publication dates fromJanuary 1, 1988, to May 10, 2012, adults 19þ, and English.A total of 43 citations were retrieved from this initial search.These articles were then reviewed, wherein the followingexclusion criteria were applied. Studies that focused mainlyon children, literature reviews, validity and reliabilitystudies, and articles with no direct bearing on exercise or PAwere excluded. It, however, should be noted that manystudies included both adults and younger age groups.Therefore, to be as inclusive as possible, these were notexcluded. The majority of articles included people withmyelomeningocele; however, in cases in which an article didnot specify the type of SB, we included it if it did not meetthe exclusion criteria. Articles that included both SB andother disability types were included if they did not meet theexclusion criteria. After applying these criteria, 15 citations

were reviewed. After this, 3 additional citations were iden-tified from bibliographies of primary articles and wereincluded in the review. A total of 18 articles were included inthe review (Figure 1).

SUMMARY OF PUBLISHED LITERATURE

The studies were classified into various categories, depend-ing on their main target area, including barriers and facili-tators, health-related measures of fitness, participation,therapeutic interventions, and technologic advancements.The quality of evidence collected was weak because themajority of studies were low powered, cross-sectional studieswith a Sackett level of either 3B (11 studies) or 4 (7 studies)(Table 1). Articles rated with a Sackett level of 3B are case-control studies, and articles with a Sackett level of 4 are casestudies or poorly controlled cohort studies [11]. Higher-levelstudies or randomized clinical trials (Sackett level 1A or 1B)[11] were not identified in this search. The type of SB (eg,myelomeningocele, lipomeningocele, meningocele) wasmentioned in only 12 studies. In addition, most of thestudies excluded power-wheelchair users, thereby limitingexternal validity to this subgroup of individuals with SB.

EXERCISE BARRIERS AND FACILITATORS

There was a limited amount of published literature on theknowledge of various barriers and facilitators that affectmaintenance of an exercise routine. Only 1 article thatfocused on this topic (by Buffart et al [12]) was retrievedfrom the search. Focus group sessions were conducted toidentify personal and environmental barriers and facilitatorsin adolescents and young adults with childhood-onset dis-abilities (n ¼ 16), including SB (n ¼ 8), with the majority ofparticipants having had a history of prior involvement inchildhood sports. By using the Physical Activity for Peoplewith a Disability model as a guide for qualitative assessment[10], the following barriers were identified: the presence ofany injury and/or complication, the lack of energy and/orfatigue, and the lack of time due to work and/or school;motivational barriers, such as waking up early and/orchanging clothing, feeling embarrassed when exercising,lacking information on exercise, having bad weather, havingexpensive and inappropriate equipment; and a limitednumber of adaptive sports programs and fitness facilities forpeople with disabilities. Facilitators to PA included havingmotivation for staying healthy and keeping in shape,wanting an improved physical appearance, wanting tomaintain walking and wheelchair skills, having sufficientsocial support, having nice weather, and having attitude andmotivational facilitators such as reaching a goal and freeingthe mind. However, due to the nonquantitative nature of thestudy, factors that had the greatest impact on PA were notidentified [12].

Figure 1. Flow chart of review article search.

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HEALTH-RELATED MEASURES OF FITNESS

Health-related measures of fitness are often used to assessbaseline aerobic fitness, body composition, and risk of healthconditions, and to evaluate the progress of exercise pro-grams. The following health-related measures of fitness havebeen assessed in a limited number of cross-sectional studiesin individuals with SB.

Aerobic Fitness and Aerobic Capacity

Adults and adolescents with myelomeningocele have pooreraerobic fitness compared with peers with and withoutdisabilities [13-16]. The average peak oxygen consumption(VO2), or aerobic capacity, is a measure of how a person’sbody uses oxygen during a maximal exercise stress test. Theaverage peak VO2 in individuals with myelomeningoceleacross several studies is shown in Table 2. Similarities in themethods used for maximal exercise testing conducted bythe researchers are listed in Table 2 and included the use ofan electronically braked arm or leg ergometer to measureaerobic capacity (peak VO2) after either a standard ramp[17] or the McMaster All Out Progressive ContinuingCycling and Arm protocol [18], in which the workload wasincreased at a set time increment. Variations in the testing

protocols of these studies included the amount of rest andwarm-up time, the starting workload, the time incrementin which watts (W) were increased, and revolutions perminute that the subjects were encouraged to maintainduring the exercise test (Table 2). Muscle strength, range ofmotion, height, weight, body fat, and daily PA level wereassessed by most of the studies [13-16]. In addition, 1study measured energy expenditure during daily life activ-ities and exercise (via wheelchair propulsion at set speedsor cycling at a set watts rate) [19]. The Hoffer classification[20] was the primary means of stratifying the ambulatorystatus of participants with SB in the majority of the studiesin Table 2. In some studies, leg or arm cycle ergometry wasused for exercise testing, depending on the main mode ofmobility, to elicit the highest VO2 values [13,14,16,19],with 1 study that used arm ergometry only (Table 2) [15].Widman et al [15] explained that the specificity of usingarm ergometry to test the aerobic fitness of individualswhose mode of ambulation is wheelchair propulsion shouldnaturally result in a higher anaerobic threshold becauseanaerobic threshold quantifies how efficiently oxygen ismetabolized in the extremities that performed the workduring exercise [15].

Expected differences in peak VO2 were observed betweengenders, with male participants attaining significantly higher

Table 1. Included articles with Sackett levels

Study, y AgeSampleSize Sample Source Disability

Main OutcomeMeasures Study Design

SackettLevel

Buffart et al,2009a [12]

22.4 � 3.4 y 16 Outpatientrehabilitationcenters, theNetherlands

8 MMC, 4 CP, 2ABI, 2 RA

Barriers and facilitatorsto exercise

Qualitative 4

Buffart et al,2008a [27]

21.1 � 4.5 y 51 Hospitals andrehabilitationcenters, theNetherlands

MMC VO2, skin-fold thickness,muscle strength,intensity/time spentin sports, FIM, socialsupport, perceivedcompetence/globalself-worth, exerciseenjoyment, min/d ofdynamic activity,self-recall of physicalactivity

Cross-sectional

3B

Buffart et al,2009b [28]

21 y, 1 mo �4.5 y, 6 mo

51 Hospitals andrehabilitationcenters, theNetherlands

MMC VO2, skin fold, HRQOL,difficulty andassistance need withlife activities, min/d of dynamicexercise

Cross-sectional

4

Buffart et al,2008b [16]

21.1 � 4.5 y 51 University hospitalsandrehabilitationcenters, theNetherlands

MMC VO2, muscle strength,joint mobility, height,weight, skin fold, min/d spent in dynamicphysical activity

Cross-sectional

3B

Van den Berg-Emons et al,2003 [14]

14-26 y 14 Rehabilitation andmedical centers,the Netherlands

MMC VO2, skin-fold thickness,height, weight, % ofday in spent indynamic physicalactivity

Cross-sectional

3B

Widman et al,2007 [15]

11-21 y 115 Outpatient andinpatient,California

SB, SCI, overweightunimpaired,unimpaired

VO2, height, weight,body composition,self- assessment ofstage of puberty,muscle strength

Cross-sectional

3B

Buffart et al,2008 [13]

21.2 y � 4.5 y 50 University hospitalsandrehabilitationcenters, theNetherlands

MMC VO2, height, weight,skin fold, musclestrength, joint rangeof motion, number ofrestricted joints

Cross-sectional

3B

Buffart et al,2008 [21]

21.4 � 4.4 y 31 University hospitalsandrehabilitationcenters, theNetherlands

MMC VO2, lipid/lipoproteinprofile, bloodpressure, skin fold,min/d of dailydynamic PA, no.cardiovasculardisease risk factors,smoking

Cross-sectional

3B

Bruinings et al,2007 [19]

21 y, 4 mo � 4y, 8 mo

36 University hospitalsandrehabilitationcenter;nondisabledgroup schoolsand university,the Netherlands

18 MMC, 18unimpaired

VO2, height, weight,energy cost andphysical strain ofvarious activities inhome and/orcommunity

Cross-sectional

3B

1054 Crytzer et al FITNESS IN ADULTS WITH SPINA BIFIDA

Table 1. Continued

Study, y AgeSampleSize Sample Source Disability

Main OutcomeMeasures Study Design

SackettLevel

Bandini et al,1991 [23]

CP: 18.5 � 1.2y (females);17.2 � 2.3 y(males);MDP: 16.8 �2.7 y(females);17.8 � 1.1 y(males)

29 School andhospital,Massachusetts

13 CP, 16myelodysplasia

Height, weight, skin-fold bodycomposition, totalenergy expenditure,resting metabolicrate, fat-free mass,total body water,extracellular water

Cross-sectional

3B

Shepherd et al,1991 [26]

0.3-29 y 59 Hospital and clinic,Australia

MMC Height, body weight(extracellular water,body fat), total bodywater, total bodypotassium, body cellmass

Cross-sectional

3B

Nawoczenski et al,2006 [31]

Intervention,47.1 � 11.7y; control,38.1 � 7.6

41 PT department,local clinics,support groups,New York andMinnesota

Manual-wheelchair userwith SB, SCI

Self- reported survey forshoulder pain, visualanalog scale ofshoulder pain withactivities, patientsatisfaction

Clinical trial 3B

Buffart et al,2010 [32]

n1 ¼ 17 y;n2 ¼ 23 y

2 Outpatient, theNetherlands

MMC, CP VO2, fitness (6-min walkor wheel chair pushtest, or armergometry exercisetest), patientsatisfaction

Case study 4

Karmel-Ross et al,1992 [29]

n1, n3 ¼ 5 y; n2,n4 ¼ 12 y;n5 ¼ 21 y

5 Outpatient,location notspecified

SB Daily written journal oftime and/or activityduring NMES,maximal kneeextension torque,walking on level, upstairs, down stairs

Case study 4

Rodgers et al,2001 [30]

44 � 11 y 19 Location notspecified

15 SCI, 1 SB, 2multitrauma and1 B/L tarsaltunnel syndrome

VO2, heart rate,cardiac strokevolume

Pretest-Posttest

4

Davis et al,1991 [33]

24 Outpatient,Canada

Paraplegia VO2, handgrip,kinematic data, andjoint kinetics, handrim kinetics,propulsion temporalcharacteristicsduring wheelchairergometer, trunk andshoulder range ofmotion

Pretest-Posttestwith control

3B

Betker et al,2007 [34]

n1 ¼ 26 y; n2 ¼52 y; n3¼ 41 y

3 1 person, inpatientrehabilitation; 1,paralympicsport; 1,outpatient,location notspecified

MMC, TBI,paraplegia

Satisfactionquestionnaire,dynamic balanceassessment, centerof pressure measure

Pretest-Posttest

4

PM&R Vol. 5, Iss. 12, 2013 1055

Table 1. Continued

Study, y AgeSampleSize Sample Source Disability

Main OutcomeMeasures Study Design

SackettLevel

Van den Berg-Emons et al,2001 [6]

14-26 y 14 Rehabilitationcenters, theNetherlands

MMC FIM, heart rate duringdaily activities, typeand time/wk spent insports activities

Cross-sectional

4

MMC ¼ myelomeningocele; CP ¼ cerebral palsy; ABI ¼ acquired brain injury; RA ¼ rheumatoid arthritis; VO2 ¼ aerobic capacity; FIM ¼ Functional IndependenceMeasure; HRQOL ¼ health-related quality of life; SB ¼ spina bifida; SCI ¼ spinal cord injury; PA ¼ physical activity; NMES ¼ neuromuscular electrical stimulation;MDP ¼ myelodysplasia; PT ¼ physical therapy; B/L ¼ bilateral; TBI ¼ traumatic brain injury; n1 ¼ sample size of one group of subjects; n2 ¼ sample size of asecond group of subjects.

1056 Crytzer et al FITNESS IN ADULTS WITH SPINA BIFIDA

peak VO2 than female participants (Table 2) [13,16,21].Aerobic fitness was also significantly higher in individualswith SB who had lower level lesions [13]. As a whole,ambulatory and nonambulatory subjects with myelome-ningocele who were tested on either arm or leg cycleergometry had 42% lower aerobic fitness capacity comparedwith reference values of unimpaired Dutch individuals [16].It is important to note that the primary mode of ambulationwas used not only as a means to stratify subjects for analysisbut also as a means to determine the exercise stress testmode (ie, leg cycle ergometer or arm ergometer) for eachindividual who participated in the study [13,14,16,21]. Insome studies, community ambulatory subjects with SB werefound to have significantly higher average peak VO2 thansubjects with SB who were ambulatory in the home or whowere wheelchair users (Table 2) [13,16]. In contrast, 1 studythat used the Hoffer classification for ambulatory status butcondensed the stratification for analysis into ambulatory andnonambulatory categories showed no significant differencein peak VO2 levels among groups (Table 2) [14]. Morespecifically, ambulatory subjects with myelomeningocelewho were tested on cycle ergometry had 32% lower aerobiccapacity compared with reference values of unimpairedambulatory individuals from the general population [13].Furthermore, nonambulatory male subjects with myelome-ningocele who were tested on arm ergometry had 22%lower aerobic peak VO2 in comparison with reference valuesfor male subjects with spinal cord injuries (SCI) below T10[13,16]. Even when the researchers considered that peakVO2 for arm crank ergometry was 70% that of leg ergo-metry, van den Berg-Emons et al [14] still found 20% lowerpeak VO2 in nonambulatory persons with SB comparedwith the Dutch reference values. However, the researcherspoint out that some discrepancy exists in this comparisonbecause wheelchair users are more accustomed to armwork than are those in an unimpaired ambulatory referencepopulation [14].

Thus, in general, individuals with SB demonstratedlow aerobic fitness than existing population referencevalues for various unimpaired and impaired groups.One study, however, showed that, when weight wasconsidered, the subjects with SCI and SB, and unimpairedsubjects who were overweight had significantly loweraerobic fitness compared with unimpaired normal-weight

controls. Furthermore, the SCI and SB groups attainedexhaustion at significantly lower watts rates than boththe unimpaired controls and unimpaired overweightsubjects [15]. One study also showed that subjects withSB achieved anaerobic threshold at lower levels of VO2

maximum [15]. Interestingly, Widman et al [15] observedthat wheelchair users with SB and SCI attained anaerobicthreshold at a higher percentage of their oxygen uptakereserve compared with unimpaired controls, a findingthat would indicate greater metabolic efficiency in thepresence of lower aerobic fitness in those with SB andSCI [15].

Determinants of Health-related Fitness

Overall, compared with reference values for other pop-ulations of individuals with and without disabilities, aerobicfitness levels were abnormally low in adolescents and youngadults with myelomeningocele. A variety of factors weresignificantly related to aerobic fitness in people with mye-lomeningocele. For instance, 1 study showed that the levelof everyday PA was significantly related to aerobic capacityin nonambulatory individuals with myelomeningocele [16].Another study found that being ambulatory and malegender explained 50% of the variance in peak VO2, andmuscle strength explained an additional 5% of the variancein peak VO2 in individuals with myelomeningocele [13].Furthermore, peak VO2 was significantly correlated (r2 ¼0.65; P ¼ .01) with the amount of time consumed in dailydynamic activities (eg, walking, wheelchair propulsion,cycling) in a cohort of ambulatory and nonambulatory in-dividuals with myelomeningocele (n ¼ 14) [14]. In thesame study, peak VO2 of individuals with myelomeningo-cele who were tested by using arm ergometry (primarywheelchair users) was significantly correlated (rs ¼ 0.83;P ¼ .011) with daily dynamic activities, whereas no cor-relation was observed in these factors for subjects withmyelomeningocele who completed the exercise test on acycle ergometer [14]. Thus, those who spent more timebeing physically active during the day had better aerobicfitness than those who were less involved in daily dynamicactivities, which suggests that lifestyle interventions thatincrease daily PA may have a positive effect on aerobicfitness.

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Cardiovascular Disease Risk

Cardiovascular disease risk was found to be higher inadolescent and adult subjects with myelomeningocele incomparison with unimpaired reference population values[21]. A clustering, or the presence of more than 2 risk factorsfor cardiovascular disease (per the Framingham study [22]),was observed in 42% of ambulatory subjects with myelo-meningocele and, notably, a significantly larger proportionof nonambulatory subjects with myelomeningocele [21].Hypertension was present in 24% of men with myelome-ningocele in comparison with 13% seen in reference valuesfor unimpaired Dutch male subjects. Total cholesterol washigh in 29% of participants (n ¼ 31) and low-density li-poprotein was high in 38% of participants. High-densitylipoprotein was low in 19% of participants with myelome-ningocele [21]. Smoking behavior was present in 19% of thesubjects (n ¼ 31).

Aerobic fitness was the only risk factor that was negativelyassociated with the clustering of �2 cardiovascular diseaserisk factors in individuals with myelomeningocele [21].Indeed, those with higher aerobic fitness were more likely tohave no risk of cardiovascular disease. Higher aerobic fitnesswas positively associated with higher systolic blood pressure.However, no significant association was found between theclustering of cardiovascular disease risk factors and body fator daily PA participation. The researchers noted that PA maybe a fleeting behavior, whereas aerobic fitness is a physio-logical attribute achievable primarily through lifespaninvolvement in PA [21].

Body Composition and Body Fat

Obesity is a risk factor for cardiovascular disease, butstandards for measurement have not yet been establishedfor this population [21]. Individuals with SB tend to be ofshorter stature and may have scoliosis or lower extremityjoint contractures for which traditional measures of height,such as a tape measure, may not reflect true height.Ambulatory individuals with myelomeningocele were foundto be 12 cm shorter than the controls, and nonambulatoryindividuals with myelomeningocele were 25.3 cm shorterthan controls when height was measured with the subjectsin supine and by using a flexible tape, with the presence ofjoint contractures addressed by joint-to-joint measurement[19]. Methods used to measure body composition (ie,height, weight, body fat) differed among studies. Mea-surement of body fat, for example, varied from use of aflexible tape measure to obtain waist and extremity cir-cumferences [23] to use of Harpenden skin-fold calipers[13,14,16,23] or to more costly but precise measures suchas dual energy x-ray absorptiometry. To calculate bodymass index in the presence of joint contractures, somestudies measured from joint to joint [13,16,19], used armspan as a proxy measure for height [14], or used a supine

stadiometer [15]. Thus, a number of tools and measure-ment techniques have been used to determine bodycomposition in individuals with SB. and norms have notbeen established.

Obesity is a known risk factor for cardiovascular disease inadults in the general population [24] and is prevalent inadults with SB [25]. The prevalence of obesity in those withSB varied from 29%-50% across various studies [14,16,23].A lack of PA in nonambulatory persons with SB [16],decreased energy expenditure [23], and lower resting meta-bolic rate [26] were found to play a significant role in the highrate of obesity. Furthermore, age-related changes to bodycomposition appear to have roots in the early childhood ofindividuals with myelomeningocele [26]. Age-relatedchanges in body composition occurred in children ages 4years and older due to a relative depletion of body cell massand lean mass tissue [26]. Body cell mass is a compilation ofmuscle, bone, organ tissues, and intra- and extracellularwater. Muscle is the most abundant component of lean masstissue. The reduction in lean muscle mass resulted in an in-crease in adipose tissue [26]. Furthermore, Bandini et al [23]reported that, in people with SB, there was misdistribution offat, with greater fat distribution over lower extremitiescompared with the upper limbs. Because of the difference inupper and lower body fat, triceps skin-fold thickness mightnot be a good indicator of body fat in people with SB [23].

Muscle Strength

Weakness of the upper or lower extremities may be present inthose with SB and has been measured in studies to determineits association with aerobic capacity. By using a hand-helddynamometer to perform a break test, Buffart et al [13]measured hip flexion and knee extension in ambulatory in-dividuals, and shoulder abductors and elbow extensors innonambulatory individuals. Decreased muscle strength wasfound in 61% of all participants, with a greater percentage ofambulatory persons having lower muscle strength (79%) thannonambulatory individuals (54%) [13]. It was believed thatconstant use of upper extremities for wheelchair propulsion innonambulatory persons might have led to this preservation ofmuscle strength. Widman et al [15] measured peak dynamicstrength by using an isokinetic dynamometer to measureshoulder flexion and extension. Themain differences betweenthe strength of people without disabilities and people with SBexisted in shoulder flexors and extensors. Unimpaired controlsubjects had higher shoulder extensor strength than subjectswith SB, SCI, and unimpaired subjects who were overweight[15]. Unimpaired male controls demonstrated significantlyhigher strength in the shoulder flexors than male subjectswith SB, SCI, and unimpaired overweight subjects. On thecontrary, no difference was found between female controlsand female subjects with SB and SCI, although unimpairedfemales were significantly stronger than the unimpairedfemale subjects who were overweight [15].

Table 2. Average peak VO2 reported in studies that conducted exercise stress testing in individuals with MMC

Study Population Metabolic Cart/Ergo Exercise Test Protocol*

Buffart et al, 2009 [13];Buffart et al, 2008 [16]

Adolescents and young adults withMMC, power-wheelchair users wereexcluded

Jaeger arm or legergox, K4b2 portablemetabolic cart{

Warm-up: 5 W/3 min; McMastersprotocol: 60 rpm/2 min

Widman et al, 2007 [15] Adolescents and young Adults with SB,the majority were wheelchair users

Lode arm ergo;Medgraphicsmetabolic cart

Warm-up: 3 min rest, 0 W/2 min;ramp protocol: 70 rpm/10 W/1 min

Bruinings et al, 2007 [19] Adolescents and young adults withMMC, power-wheelchair users wereexcluded

Jaeger arm or leg ergox Warm-up: 5 W/3 min arm 20 W/3 minleg; ramp protocol 60 rpm/2 min

Van den Berg-Emonset al, 2003 [14]

Adolescents and young adults withMMC, power-wheelchair users wereexcluded

Jaeger arm or leg ergox,K4b2 portablemetabolic cart{

Warm-up: 3 min/5 W; McMastersprotocol: 60 rpm � 2 min

VO2 ¼ aerobic capacity; MMC ¼ myelomeningocele; ergo ¼ ergometer; SD ¼ standard deviation; SB ¼ spina bifida.*Warm-up time/watts (W)/name of exercise testing protocol/revolutions per minute (rpm)/ramp up resistance by(x)(W)/min. If no W listed, then variable load.yThe subjects who were classified as community ambulatory and household ambulatory were combined by Bruinings [19] and van den Berg-Emons [14].zNonfunctional ambulatory category includes those who walk in physical therapy only.xJaeger ER800SH arm and ER800 leg ergometer, Jaeger Toennies, Breda, The Netherlands.{COSMED, Rome, Italy.

1058 Crytzer et al FITNESS IN ADULTS WITH SPINA BIFIDA

Energy Cost

Energy cost, determined by the measurement of oxygenuptake during a standard activity protocol, is measured inmetabolic equivalents. Only 1 study in our search (Bruiningset al [19]) classified mobility and a limited number of ac-tivities of daily living skills in terms of metabolic equivalents.It was discovered that energy cost was lower in wheelchairusers with myelomeningocele compared with age- andgender-matched ambulatory counterparts [19]. Although thepreferred gait speed of ambulatory individuals with SB was14% slower than the preferred speed of controls, no signif-icant difference in energy cost was observed. The peak VO2

was significantly lower (P < .001) in the nonambulatorygroup (23.5 mL/kg/min) compared with unimpaired con-trols (51.0 mL/kg/min); however, the energy cost of wheel-chair propulsion in nonambulatory subjects was lower thanthe energy cost of walking in the controls at preferred and setspeeds. Physical strain of daily activities for ambulatory andnonambulatory individuals with myelomeningocele were allsignificantly higher than that in controls, with the exceptionof cycling at 80 W and 100 W; therefore, people withmyelomeningocele use a greater percentage of their aerobiccapacity to carry out their daily activities with the exceptionof leg or arm ergometry [19].

SPORTS PARTICIPATION

Although participation in sports by adolescents and youngadults with SB was equal to that of other individuals withdisabilities, lower scores on the Physical Activity Scalefor Individuals with Disabilities indicated that adolescents

and young adults with myelomeningocele participate at asignificantly lower intensity and with lower energy expen-diture than their peers [27]. Individuals with SB who weresports participants engaged in 39 more minutes per day ofPA and 56 more minutes per day of nonexercise walkingor wheelchair propulsion than those with SB who did notplay sports. Significant factors that explain sports participa-tion included family participation, rewarding family experi-ence, athletic competence, and desire to attain a betterphysical appearance. Furthermore, participants who enjoyedeveryday PA (measured by the Groningen EnjoymentQuestionnaire) were more likely to participate in exercise[27]. Another Dutch study found that individuals withmyelomeningocele reported significantly lower health-related quality of life than their able-bodied counterparts.More than half of the subjects with myelomeningoceleexperienced difficulties with participation in activities ofdaily living, notably mobility and personal care as well aswith social roles, employment, and housing. Further, thosewho used wheelchairs and had low educational levelsexperienced the lowest levels of participation in activitiesof daily living, in addition to reporting a lower physicalhealtherelated quality of life [28]. Importantly, bothinvolvement in PA and higher levels of aerobic fitness werepositively correlated with physical healtherelated quality oflife, modifiable factors that could be addressed with lifestyleinterventions.

THERAPEUTIC INTERVENTIONS

A total of 5 studies within the search included therapeuticinterventions. One of these studies (Karmel-Ross et al [29])

Table 2. Continued

Average Peak VO2, mL/kg min

Total sample,mean (SD),± mL/kg min

Male Subjects,± mL/kg min

Female Subjects,± mL/kg min

CommunityAmbulatory,± mL/kg miny

HouseholdAmbulatory,± mL/kg miny

NonfunctionalAmbulatory,± mL/kg minz

22.6 � 8.2 [13,16](n ¼ 50)

28.1 � 7.0 [13](n ¼ 25)

17.0 � 4.7 [13](n ¼ 25)

29.0 � 7.7 [13,16](n ¼ 15)

22.3 � 6.6 [13,16](n ¼ 7)

19.2 � 6.8(n ¼ 28) [13,16]

20.6 � 7.6(n ¼ 18)

14.2 � 4.2(n ¼ 19)

31.4 � 8.3(n ¼ 8)y

23.5 � 5.3(n ¼ 10)

27.3 � 7.4(n ¼ 14)

30.1 � 6.2(n ¼ 9)

y 22.5 � 7.5(n ¼ 5)

PM&R Vol. 5, Iss. 12, 2013 1059

aimed at improving muscle strength. Although this studyincluded only 5 people with SB (1 adult, 2 adolescents, and2 children), it offered insight into a therapeutic modalityrarely studied in those with SB. Neuromuscular electricalstimulation was applied over the belly of the vastus lateralisand rectus femoris muscles proximally, and to the rectusfemoris and vastus medialis muscles distally in all subjectsfor 8 weeks [29]. The neuromuscular electrical stimulationcurrent was adjusted every day according to each subject’stolerance rather than as a percentage of maximum voluntarycontraction. Although the sample size is small, the resultsdemonstrated a reduction in the time required to completefunctional tasks with 4 participants and an increase in themaximum torque production of the stimulated limbs of 2older participants. The 21-year-old participant showedinitially lower strength in the stimulated limb compared withthe control limb, but, after 8 weeks of neuromuscular elec-trical stimulation, the stimulated limb was stronger andshowed gains in function [29].

Two studies focused on the problems associated withwheelchair propulsion in SB, including improper scapularkinematics and resulting shoulder pain. Rodgers et al [30]provided a 6-week intervention composed of strengthening,stretching, and endurance exercises to manual-wheelchairusers with SB and found significant improvement in thebiomechanics of wheelchair propulsion with an increase inshoulder flexion and extension range of motion, maximumelbow extension, trunk flexion, and propulsive moment.Nawoczenski et al [31] developed a rehabilitation protocolthat focused on the concept of selective stretching andstrengthening of muscles that contribute to abnormal kine-matic deviation and resultant shoulder impingement in 41

long-term wheelchair users, primarily with SCI, and in 1person with SB. Biofeedback was used as a training tool toimprove activation, contraction, and relaxation of the scap-ular muscles, and as a means to prescribe only the exercisesthat the subject could do with optimal biomechanical formwithout pain. Shoulder pain significantly decreased with aconcomitant significant increase in function in the inter-vention group after the 8-week rehabilitation protocol [31].A limiting factor of this study is that the outcomes of theintervention group were compared with an asymptomaticcontrol group who received no intervention. However,biofeedback appears to be a promising tool for reinforcingthe proper activation of the scapular muscles during a homeexercise program in manual-wheelchair users.

Improvements in PA and exercise capacity were targetedby 2 studies [32,33]. In an effort to promote PA and aerobicfitness in people with disabilities, Buffart et al [32] used anactive lifestyle and sports participation intervention that wastailored for an individual with cerebral palsy and an indi-vidual with myelomeningocele. After the 12-week interven-tion, self-reported PA improved by 51% and 76% for thesubjects with myelomeningocele and cerebral palsy,respectively. Submaximal exercise capacity, as measured by a6-minute walk or wheel distance, improved by 16% and 9%for myelomeningocele and cerebral palsy, respectively. Aer-obic fitness, as determined by peak VO2, improved only forthe subject with myelomeningocele by 39%. The researchersexplain that, because they were unable to monitor the home-based session, it might not have been of sufficient intensityto improve aerobic fitness. They thus stress the need of ex-ercise logs or heart rate monitors to keep track of the exercisesessions as well as to ensure correct performance of the

1060 Crytzer et al FITNESS IN ADULTS WITH SPINA BIFIDA

exercises. It should be emphasized that the personalizednature of the intervention enabled PA barriers specific to theparticipants to be addressed separately, which might haveserved as an important factor in improving patient compli-ance to the intervention program. Davis et al [33] studied theeffect of arm crank training on cardiorespiratory fitness andused 4 different types of training regimens classified on thebasis of either duration or intensity of exercise. The re-searchers reported a significant increase in peak oxygenuptake and cardiac stroke volume in all subjects with SBexcept in those who performed short-duration arm-crankexercise (20 minutes) at low intensity (50% peak oxygenuptake) and in control subjects [33]. Peak VO2 was one ofthe outcome measures in both the studies.

ADVANCES IN TECHNOLOGY TO FACILITATEEXERCISE

Betker et al [34] designed a rehabilitation protocol by usingan interactive video game system that required the player toweight shift to activate a computer game while sitting on aball or a mat table under various conditions (ie, eyes open,eyes closed, arms raised). Force sensitive applications soft-ware and a pressure mat with piezoelectric-resistive sensorswere used to determine the subject’s center of pressure whilehe or she was seated on a mat table or a softer surface, suchas an underinflated ball. Adjustability was built into thesoftware of the games so that individuals could progress atcustom speeds and increase competition throughout thegame. All participants demonstrated an improvement inbalance and a decrease in the number of falls after theintervention program. In addition, an increase in motivationlevel of the participants to practice dynamic movement taskswas reported [34].

The activity monitor (AM) has been used in some studies[6,14,16] as a purportedly valid and reliable means ofobjectively assessing daily PA participation in individualswith myelomeningocele who are both ambulatory andnonambulatory and is reportedly useful in making com-parisons across groups. Van den Berg Emons et al [6]attached piezo-resistive accelerometers to various parts of thebody, such as the sternum and extremities, and a bag thatheld the AM was worn at the waist. Wheelchair users alsowore accelerometers on one or both wrists, depending onwhether the person was a full-time or part-time user of awheelchair. Computer software was used to download thedata from the AM for analysis. Only 2 days of activitymonitoring were obtained with the AM due to “practicalconsiderations,” as noted by the researchers. There was nosignificant difference between the 2 randomly selected daysof monitoring and the average of the 2 days was used foranalysis. Seven days of monitoring is the preferred standardfor accuracy; consequently, the correlation between PAand aerobic fitness may have been underestimated. Theresearchers found that adolescents and adults with

myelomeningocele are considerably more hypoactivecompared with unimpaired controls [6]. Ambulatory andnonambulatory individuals with myelomeningocele spent asignificantly lower percentage of the day in dynamic PA incomparison with unimpaired controls. In addition, thenumber of periods of wheeling or walking during the daywas significantly lower in those with myelomeningocele thanin controls [6].

CONCLUSION

The review is limited by the number (n ¼ 18) and quality ofstudies (Sackett level 3B or 4). The studies had small samplesizes, with low power, which resulted in a low quality ofevidence. Knowledge gaps were found in all areas. Analysisof the available evidence suggests that people with SB havepoorer health-related fitness compared with able-bodiedindividuals; however, no reference values with respect tothese measures are yet available. As a result, most of thestudies compared these values with age- and gender-matched reference values of people without disabilities. Re-sults of studies also reported that people with SB have lowermuscle strength and higher body fat compared with peoplewithout disabilities. Conventional measures of determiningtriceps skin-fold thickness and body mass index that wereused in these studies may not reflect the true height andbody mass for the SB population due to shorter stature,lower lean tissue, scoliosis, and joint contractures. Theseresults support findings that, to fill the gaps in knowledgethat still persist and to eliminate disparities in measuringobesity and other health-related measures of fitness, refer-ence standards with respect to people with SB and otherphysical disabilities need to be developed [35].

Exercise testing was used in 6 of the 8 of articles whoseprimary purpose was to investigate factors associated withhealth-related physical fitness in individuals with SB, butnone of the articles applied the information directly todeveloping exercise interventions. Furthermore, althoughuniform within each site, exercise testing protocols variedacross sites. In addition, although norms for VO2 based onage and gender are available for able-bodied individuals, nonorms have been established for individuals with SB.

More than half of the studies reviewed were conducted inlaboratories in the Netherlands by using Dutch referencevalues for comparison; therefore, the results may havelimited generalizability to individuals with SB worldwide.One of the strengths of the exercise testing studies overall isthat the laboratories were accessible for wheelchair userswho required the use of arm ergometry to undergo maximalexercise testing. However, power-wheelchair users wereexcluded in the majority of the studies. Power-wheelchairusers may be at an even higher risk than ambulatory in-dividuals and wheelchair users with SB for secondary con-ditions, such as cardiovascular disease and metabolicsyndrome, due to potentially lower levels of PA.

PM&R Vol. 5, Iss. 12, 2013 1061

DIRECTIONS FOR FUTURE RESEARCH

Given misdistribution of adipose tissue, short stature,scoliosis, and joint contractures, further research is neededto determine the most reliable and low-cost methods ofmeasuring body composition and to establish norms. Futurestudies should establish standardized protocols by usingboth leg and arm ergometry for exercise testing and toevaluate larger cohorts of individuals with myelomeningo-cele to establish age- and gender-matched reference valuesworldwide. Consideration should be given to comparingresults between genders and among ambulatory groups.

Further investigation is needed on the effects of home-based video game systems on trunk balance in wheelchairusers. An easy to use, low-cost activity monitoring systemmade available to consumers who are wheelchair users couldpromote self-monitoring of exercise programs. Furtherinvestigation into the effectiveness of low-cost training pro-grams designed to elicit efficient propulsion to reducerepetitive strain in addition to determining the amount ofeducation and training required to develop a consistentlybiomechanically efficient stroke pattern is needed [36].Investigation into cross-training by using interactive video-gaming technology to strengthen the trunk and musclesthat support the shoulder girdle and reduce muscle imbal-ance from daily wheelchair propulsion is an importantconsideration.

Higher-level intervention studies are needed to determinethe dose-response relationship of exercise because lowerlevels of fitness are prevalent, and cardiovascular disease andobesity risk is high in those with SB, especially non-ambulatory individuals. Consideration should be given todiscovering behavioral methods to improve exercise partic-ipation in adults with SB to combat age-related changes suchas reduced mobility and obesity. The barriers and facilitatorsnoted by Buffart et al [12] could be addressed in future in-terventions through inclusion of low-cost methods of exer-cise, provision of education and supervision to decrease therisk of injury, promotion of proper biomechanics of exerciseand inclusion of neuromuscular electrical stimulation inexercise programs, and in discovering ways to increase self-efficacy and independence with exercise. Investigation intotactics that engage individuals with SB in community groupfitness at low cost should be considered as well as lifestyleinterventions that increase day-to-day PA and can becompleted at home. Further insight could be gleaned by alongitudinal study to evaluate daily dynamic activityparticipation and what role it plays in reducing cardiovas-cular disease risk in individuals with SB as they age.

REFERENCES1. Liptak, G. What is Spina Bifida? Available at http://www.spinabif

idaassociation.org/site/c.evKRI7OXIoJ8H/b.8277225/k.5A79/What_is_Spina_Bifida.htm. Accessed July 23, 2013.

2. Liptak, G., Spotlight on Spina Bifida. Available at http://www.spinabifidaassociation.org/site/c.liKWL7PLLrF/b.2642343/k.8D2D/Fact_Sheets.Accessed July 18, 2012.

3. Spina Bifida Association of America. How Often Does Spina BifidaOccur. Available at: http://www.kintera.org/site/c.liKWL7PLLrF/b.2700313/k.28B2/How_Often_Does_Spina_Bifida_Occur.htm. AccessedAugust 9, 2013.

4. Dicianno BE, Kurowski BG, Yang JM, et al. Rehabilitation and medicalmanagement of the adult with spina bifida. Am J Phys Med Rehabil2008;87:1027-1050.

5. HeathGW, Fentem PH. Physical activity among personswith disabilities:A public health perspective. Exerc Sport Sci Rev 1997;25:195-234.

6. van den Berg-Emons HJ, Bussmann JB, Brobbel AS, Roebroeck ME, vanMeeteren J, Stam HJ. Everyday physical activity in adolescents andyoung adults with meningomyelocele as measured with a novel activitymonitor. J Pediatr 2001;139:880-886.

7. Bowman RM, McLone DG, Grant JA, Tomita T, Ito JA. Spina bifidaoutcome: A 25-year prospective. Pediatr Neurosurg 2001;34:114-120.

8. Dosa NP, Foley JT, Eckrich M, Woodall-Ruff D, Liptak GS. Obesityacross the lifespan among persons with spina bifida. Disabil Rehabil2009;31:914-920.

9. Ausili E, Focarelli B, Tabacco F, et al. Bone mineral density and bodycomposition in a myelomeningocele children population: Effects ofwalking ability and sport activity. Eur Rev Med Pharmacol Sci 2008;12:349-354.

10. van der Ploeg HP, van der Beek AJ, van der Woude LH, vanMechelen W. Physical activity for people with a disability: A conceptualmodel. Sports Med 2004;34:639-649.

11. Rich NC. Research forum: Levels of evidence. J Womens Health PhysTherap 2005;29:19-20.

12. Buffart LM, Westendorp T, van den Berg-Emons RJ, Stam HJ,Roebroeck ME. Perceived barriers to and facilitators of physical activityin young adults with childhood-onset physical disabilities. J RehabilMed 2009;41:881-885.

13. Buffart LM, van den Berg-Emons RJ, van Wijlen-Hempel MS, Stam HJ,Roebroeck ME. Health-related physical fitness of adolescents andyoung adults with myelomeningocele. Eur J Appl Physiol 2008;103:181-188.

14. van den Berg-Emons HJ, Bussmann JB, Meyerink HJ, Roebroeck ME,Stam HJ. Body fat, fitness and level of everyday physical activity inadolescents and young adults with meningomyelocele. J Rehabil Med2003;35:271-275.

15. Widman LM, Abresch RT, Styne DM, McDonald CM. Aerobic fitnessand upper extremity strength in patients aged 11 to 21 years withspinal cord dysfunction as compared to ideal weight and overweightcontrols. J Spinal Cord Med 2007;30(Suppl 1):S88-S96.

16. Buffart LM, Roebroeck ME, Rol M, et al. Triad of physical activity,aerobic fitness and obesity in adolescents and young adults withmyelomeningocele. J Rehabil Med 2008;40:70-75.

17. Wasserman K, Hansen JE, Sue DY, et al. Principles of Exercise Testingand Interpretation: Including Pathophysiology and Clinical Implica-tions, 3rd ed. Baltimore, MD: Lippincott Williams and Wilkins; 1999.

18. Bar-Or O. Pediatric Sports Medicine for the Practicioner: From Physi-ologic Principles to Clinical Applications. New York, NY: Springer;1983.

19. Bruinings AL, van den Berg-Emons HJ, Buffart LM, van der Heijden-Maessen HC, Roebroeck ME, Stam HJ. Energy cost and physical strainof daily activities in adolescents and young adults with myelome-ningocele. Dev Med Child Neurol 2007;49:672-677.

20. Hoffer MM, Feiwell E, Perry R, Perry J, Bonnett C. Functional ambu-lation in patients with myelomeningocele. J Bone Joint Surg Am 1973;55:137-148.

21. Buffart LM, van den Berg-Emons RJ, Burdorf A, Janssen WG, Stam HJ,Roebroeck ME. Cardiovascular disease risk factors and the relationshipswith physical activity, aerobic fitness, and body fat in adolescents and

1062 Crytzer et al FITNESS IN ADULTS WITH SPINA BIFIDA

young adults with myelomeningocele. Arch Phys Med Rehabil 2008;89:2167-2173.

22. Kannel WB. Contributions of the Framingham Study to the conquest ofcoronary artery disease. Am J Cardiol 1988;62:1109-1112.

23. Bandini LG, Schoeller DA, Fukagawa NK, Wykes LJ, Dietz WH. Bodycomposition and energy expenditure in adolescents with cerebral palsyor myelodysplasia. Pediatr Res 1991;29:70-77.

24. Hubert HB, Feinleib M, McNamara PM, Castelli WP. Obesity as anindependent risk factor for cardiovascular disease: A 26-year follow-upof participants in the Framingham Heart Study. Circulation 1983;67:968-977.

25. Dosa NP, Eckrich M, Katz DA, Turk M, Liptak GS. Incidence, preva-lence, and characteristics of fractures in children, adolescents, andadults with spina bifida. J Spinal Cord Med 2007;30(Suppl 1):S5-S9.

26. Shepherd K, Roberts D, Golding S. Body composition in myelome-ningocele. Am J Clin Nutr 1991;53:1-6.

27. Buffart LM, van der Ploeg HP, Bauman AE, et al. Sports participation inadolescents and young adults with myelomeningocele and its role intotal physical activity behaviour and fitness. J Rehabil Med 2008;40:702-708.

28. Buffart LM, van den Berg-Emons RJ, van Meeteren J, Stam HJ,Roebroeck M. Lifestyle, participation, and health-related quality of lifein adolescents and young adults with myelomeningocele. Dev MedChild Neurol 2009;51:886-894.

29. Karmel-Ross K, Cooperman DR, Van Doren CL. The effect of electricalstimulation on quadriceps femoris muscle torque in children with spinabifida. Phys Ther 1992;72:723-730.

30. Rodgers MM, Keyser RE, Rasch EK, Gorman PH, Russell PJ. Influenceof training on biomechanics of wheelchair propulsion. J Rehabil ResDev 2001;38:505-511.

31. Nawoczenski DA, Ritter-Soronen JM, Wilson CM, Howe BA,Ludewig PM. Clinical trial of exercise for shoulder pain in chronicspinal injury. Phys Ther 2006;86:1604-1618.

32. Buffart LM, van den Berg-Emons RJ, van Mechelen W, et al. Promotingphysical activity in an adolescent and a young adult with physicaldisabilities. Disabil Health J 2010;3:86-92.

33. Davis G, Plyley MJ, Shephard RJ. Gains of cardiorespiratory fitness witharm-crank training in spinally disabled men. Can J Sport Sci 1991;16:64-72.

34. Betker AL, Desai A, Nett C, Kapadia N, Szturm T. Game-based exer-cises for dynamic short-sitting balance rehabilitation of people withchronic spinal cord and traumatic brain injuries. Phys Ther 2007;87:1389-1398.

35. Rimmer JH, Wang E, Yamaki K, Davis B. Documenting disparities inobesity and disability. Focus (NCDDR) 2010;24:1-16.

36. Boninger ML, Koontz AM, Sisto SA, et al. Pushrim biomechanics andinjury prevention in spinal cord injury: Recommendations based onCULP-SCI investigations. J Rehabil Res Dev 2005;42(Suppl 1):9-19.