Accepted Manuscript Impact of Wheelchair Rugby on Body Composition of Tetraplegic Subjects: A Pilot Study José I. Gorla, PhD, Anselmo de A. Costa e Silva, PhD, Mariane Borges, Msc, Ricardo A. Tanhoffer, PhD, Priscila S. Godoy, Msc, Décio R. Calegari, PhD, Allan de O. Santos, PhD, Celso D. Ramos, PhD, Wilson Nadruz, Junior, PhD, Alberto Cliquet, Junior, PhD PII:
S0003-9993(15)01197-1
DOI:
10.1016/j.apmr.2015.09.007
Reference:
YAPMR 56319
To appear in:
ARCHIVES OF PHYSICAL MEDICINE AND REHABILITATION
Received Date: 2 June 2015 Revised Date:
2 September 2015
Accepted Date: 16 September 2015
Please cite this article as: Gorla JI, Costa e Silva AdA, Borges M, Tanhoffer RA, Godoy PS, Calegari DR, Santos AdO, Ramos CD, Nadruz Junior W, Cliquet Junior A, Impact of Wheelchair Rugby on Body Composition of Tetraplegic Subjects: A Pilot Study, ARCHIVES OF PHYSICAL MEDICINE AND REHABILITATION (2015), doi: 10.1016/j.apmr.2015.09.007. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
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Title page Running head: Body composition of quad rugby players
TETRAPLEGIC SUBJECTS: A PILOT STUDY José I. Gorla1 (PhD) Anselmo de A. Costa e Silva1,2 (PhD)
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Mariane Borges1 (Msc)
Décio R. Calegari3 (PhD) Allan de O. Santos4 (PhD) Celso D. Ramos4 (PhD)
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Wilson Nadruz Junior5 (PhD)
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Ricardo A. Tanhoffer1 (PhD) Priscila S. Godoy1 (Msc)
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TITLE: IMPACT OF WHEELCHAIR RUGBY ON BODY COMPOSTION OF
Alberto Cliquet Junior6 (PhD)
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School of Physical Education; University of Campinas, Campinas, SP, Brazil
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Faculty of Physical Education; Federal University of Pará, Castanhal, PA,
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Brazil
School of Physical Education; University of Maringá, Maringá, Pr, Brazil
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Service of Nuclear Medicine, School of Medical Sciences, University of
Campinas, Campinas, SP, Brazil 5
Department of Internal Medicine, School of Medical Sciences,University of
Campinas, Campinas, SP, Brazil
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Department of Orthopaedics, School of Medical Sciences, University of
Campinas, Campinas, SP, Brazil, Department of Electrical Engineering University of São Paulo (USP), São Carlos, SP, Brazil
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CORRESPONDING AUTHOR: José Irineu Gorla PhD, Address: School of Physical Education, University of Campinas; Érico Veríssimo Avenue, number 701, Unicamp. Postal Code: 13.083-851. Campinas, São Paulo State, Brazil. E-
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mail:
[email protected]. Phone: (55)1935216616. Fax number: 55 (19) 3521-6750
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Financial Disclosure: We certify that no party having a direct interest in the results of the research supporting this article has or will confer a benefit on us or on any organization with which we are associated AND, if applicable, we certify that all financial and material support for this research (eg, NIH or NHS grants)
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and work are clearly identified in the title page of the manuscript.
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KEY WORDS: Spinal Cord Injury, Physical Fitness, Tetraplegia.
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TITLE IMPACT OF WHEELCHAIR RUGBY ON BODY COMPOSITION OF TETRAPLEGIC SUBJECTS: A PILOT STUDY
3 4 ABSTRACT
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OBJECTIVE: To investigate the longitudinal effects of Wheelchair Rugby (WR)
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training on body composition of tetraplegic subjects. DESIGN: Subjects were
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evaluated at baseline (T1) and after WR training (T2). SETTING: Faculty of Physical
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Education Settings. PARTICIPANTS: Thirteen tetraplegic individuals (26.6±6.0
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years). INTERVENTIONS: Four sessions per week of WR training composed by
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aerobic and anaerobic activities, and technical and tactical aspects of WR. The
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average time of intervention was 8.1 ± 2.5 months. MAIN OUTCOME MEASURES:
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body composition assessed by Dual-energy W-ray Absorptiometry. RESULTS: After
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training, fat mass was significantly reduced in the whole body (15,191±4,603 vs.
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13,212±3,318 grams, p=0.016), trunk (7,058±2,639 vs. 5,693±1,498 grams, p=0.012)
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and legs (2,847±817 vs. 2,534±742 grams p=0.003). Conversely, increased bone
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mass content (BMC) (183±35 vs. 195±32 grams, p=0.010) and fat-free mass
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(2,991±549 vs. 3,332±602 grams, p=0.016) in the arms and reduced BMC in the
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trunk (553±82 vs. 521±86 grams, p=0.034) were observed after training.
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Furthermore, no significant correlation between the duration of training and changes
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in body composition was detected. CONCLUSIONS: Regular WR training increased
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lean mass and bone mass content in the arms and decreased total body fat mass.
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Conversely, WR training was associated with decreased BMC in the trunk. These
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results suggest that regular WR training improves body composition in tetraplegic
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subjects.
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Key words: Spinal Cord Injury, Physical Fitness, Tetraplegia.
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ABBREVIATIONS
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SCI – Spinal Cord Injury
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WH – Wheelchair Rugby
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FM – Fat Mass
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FFM – Fat-Free Mass
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BMD – Bone Mineral Density
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BMC – Bone Mineral Content
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DXA - Dual X-Ray Absorptiometry
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T1 - Baseline T2 - Post-assessment
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INTRODUCTION
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Subjects with tetraplegia usually have few sports/exercises opportunities to engage,
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mainly due to their physical impairment and lack of specialized sports venues. In this
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sense, Wheelchair Rugby (WR) was developed in the 1970’s aiming exclusively the
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participation of people with tetraplegia, and is currently a paralympic sport.1
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Tetraplegia occurs when the spinal cord, at the level of any cervical vertebrae, is
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injured or damaged, impairing motor and sensory functions at and below this
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neurological level. Tetraplegic subjects may face physiological dysfunctions such as
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bradycardia and impaired blood venous return and thermoregulation.2 In addition,
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these individuals might develop marked changes in body composition, which include
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reductions in fat-free mass (FFM) in lower and upper limbs and increases in visceral
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and subcutaneous fat deposition.3
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In able-bodied subjects, body composition is directly related to sports performance.
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There is a positive correlation between higher levels of FFM and sports performance
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such as endurance, strength, power and speed, while increased adiposity has a
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negative impact on this regard.4 In addition, higher levels of fat mass have been
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related to increased metabolic disorders such as dyslipidemias,5 insulin resistance6
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and cardiovascular diseases.7
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Subjects with spinal cord injury (SCI), especially those with tetraplegia, usually
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exhibit both higher adiposity3 and incidence of cardiovascular diseases8 in addition to
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lower levels of physical activity2 when compared to able-bodied individuals. Previous
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reports demonstrated that physical activity may promote benefits in SCI population
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by increasing aerobic power and strength9 and preventing decreases in Bone Mineral
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Density (BMD).10 Furthermore, cross-sectional studies showed that performance of
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adapted sports (WR, wheelchair basketball, handball and tennis) was associated with
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reduced carotid atherosclerosis and improved cardiac diastolic function in subjects
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with SCI.11,12 However, little is known about the impact of regular WR training on
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body composition. Therefore, the aim of this study was to examine the longitudinal
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effects of WR training on body composition in tetraplegic subjects.
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METHODS
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Thirteen men with tetraplegia, who were part of a high-level WR team (one of the
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main teams of Brazilian WR Championship – 1st division), participated in the study.
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Subjects were recruited by convenience sampling and did not regularly perform
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physical activity before entering into the WR training program. The small number of
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WR teams in Brazil as well as the relatively low number of subjects interested in
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playing this sport did not allow the performance of a randomized study and the
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inclusion of a larger group of athletes. Exclusion criteria comprised any illness that
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might affect regular training participation: pressure sores, cardiovascular diseases,
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urinary tract and upper respiratory tract infections. Injury level and severity were
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assessed according to the American Spinal Injury Association Impairment Scale.13
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The study was conducted in accordance with the Declaration of Helsinki and the
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protocol was approved by the Institutional Review Board of the University of
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Campinas. All participants read and signed informed consent.
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Evaluation of anthropometric features and analysis of body composition by Dual X-
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Ray Absorptiometry (DXA) were performed before the beginning of the training
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program (Baseline - T1) and after a period of regular training (Post-assessment –
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T2). All subjects who underwent T1 were also evaluated at T2. Due to recovery of
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infections and/or injuries, we had differences in the time between T1-T2
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measurements. Furthermore, two athletes were admitted into the team during the
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season and therefore had a smaller period (three months) between the
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measurements (see Table 1). The average time between T1 and T2 was 8.1±2.5
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months (Table 1).
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The training program (planned and conducted by team coaches) was designed to
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meet the demands required by WR matches. Previous data showed that during a
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high-level WR match, players usually cover an average distance of 4.5 km and
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achieve average speeds of 1.22 m.s-1 and 1.05 m.s-1 on the first and second half,
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respectively.14 To meet these requirements, our training program was basically
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composed by aerobic and anaerobic activities (aerobic training, aerobic circuit
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training, weight lifting, circuit training, 20-meter sprints, and technical and tactical
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aspects of WR). These activities were performed in four sessions per week and each
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session had three hours of duration. This training load is similar to that reported in
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other studies evolving elite wheelchair rugby players.15,16 All participants regularly
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participated in the training program and attended at least 3 sessions per week with
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an training average of 10.5 hours/per week.
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DXA was assessed using a Hologic Discovery® device (Hologic Inc., Bedford,
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Massachusetts, USA). Bone Mass Content (BMC, grams), Bone Mass Density (BMD,
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g/cm2), Fat-Free Mass (FFM, grams) and Fat Mass (FM, grams) were measured in
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the whole body and in selected regions (trunk, legs and arms). Bone area was
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calculated as the ratio between BMC and BMD. The measurements were performed
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in T1 and T2 by the same investigator and the volunteers were fasting. Body mass
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(Kg) was measured using a floor digital scale (Lider®; Araçatuba, Brazil). First the
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athletes were measured in a wheelchair and then the wheelchair weight was
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measured separately. Body mass of each athlete was calculated as the difference
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between these measurements. Stature of the individuals was measured in supine
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position. Body mass index was calculated as body mass divided by squared height
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(kg/m2).
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Data were analyzed using SPSS® (Windows Version 18.0, Chicago, IL, USA). The
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Shapiro-Wilk test was used to assess normal distribution. BMC and BMD in the legs
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did not have normal distribution and the values are presented as median
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(interquartile range). All other variables had normal distribution and are presented as
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mean ± standard deviation. Differences between pre and post assessments in
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continuous normal and non-normal variables were evaluated by paired t-test and
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Mann–Whitney test, respectively. Spearman’s method was used to assess bivariate
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correlations between variables that presented significant changes after training and
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the time between T1 and T2 measurements (in months). A p-value ≤ 0.05 was
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considered significant.
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7 RESULTS
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Background characteristics of all participants are presented in Table 1. The mean
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age and stature were 26.6±6.0 years and 1.77±0.10 m, respectively. Data regarding
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body mass index and body composition assessed by DXA in T1 and T2 are
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presented in Table 2. There was no difference in body mass index between T1 and
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T2. After the training period, adiposity was significantly reduced in the trunk, legs and
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in the whole body, but not in the arms. In contrast, FFM only increased in the arms
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and did not change in the other studied segments or in the whole body. BMC and
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bone area significantly increased in the arms but showed a significant reduction in
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the trunk after the training period. Furthermore, no changes in BMD were detected in
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the arms, trunk, legs or in the whole body.
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We then performed bivariate correlation analysis in order to assess whether variation
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in body composition was related to duration of training (in months). However, no
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significant correlation was found between training duration and variation in arm BMC
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(rho=0.28; p=0.35), arm bone area (rho=-0.42; p=0.14), arm FFM (rho=0.10; p=0.73),
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trunk BMC (rho=0.06; p=0.85), trunk bone area (rho=-0.17; p=0.58), trunk FM (rho=-
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0.04; p=0.88), leg FM (rho=0.06; p=0.84) and whole body FM (rho=0.02; p=0.73).
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DISCUSSION
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Chronic SCI leads to reductions in physical activity and are associated with changes
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in body composition, such as increases in FM and dramatic reductions in FFM.3
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Physical activity may improve body composition in subjects with SCI, and cross-
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sectional data have suggested that even upper-body exercises are associated with
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reduced body adiposity and higher lean tissue mass in this population.17 The results
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of the present report showed that regular WR training improved body composition of
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tetraplegic subjects, by increasing lean mass and BMC in the arms and by
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decreasing FM in the trunk and the legs. Furthermore, we observed a significant
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decrease in BMC in the trunk of the studied individuals after the training period. As
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far as we know, this is the first longitudinal study to demonstrate that WR training
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sessions may affect the body composition in subjects with SCI.
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After the training protocol, the participants of this study had a significant increase in
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arm FFM. This difference was somewhat expected, as all individuals exclusively use
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the arms for pushing their wheelchair. These long-term effects on lean tissue might
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underscore the quite high intensity characteristics of WR, which has also been
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acknowledged by another research group.14 Conversely, FFM in the trunk and legs
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did not show any changes, as these segments were not subject to voluntary motion
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control due to SCI. In addition, whole body FFM did not change in our sample after
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the training protocol, which is in contrast with data reported by Kim et al, who showed
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a slight increase in total body FFM following chronic upper-body physical activity.18
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However, that aforementioned study was conducted in a SCI sample comprising 83%
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of paraplegic individuals, who had a lower injury level in comparison with our sample
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and therefore had a higher muscle area that could be affected by the trophic effects
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of upper-body exercise.
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We found a 13% reduction in total body FM after the training protocol, which may be
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explained by the respective reduction observed in the trunk and legs. The reduction
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in FM in a remote region, such as the legs, indicates that the effects of physical
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activity on adiposity might be systemic. Similar findings have been also reported by
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Kim et al.,18 who demonstrated 14% of reduction in body fat in SCI individuals who
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performed training sessions on a motor-driven rowing machine, 5 days a week, for 6
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weeks. A possible explanation for the systemic effects of exercise might involve the
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elevation of adiponectin levels.19 A previous study showed that exercise promotes
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rises in plasmatic adiponectin levels and demonstrated that such increase is
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associated with weight loss in humans.20 On the other hand, regular exercise is
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related to increases in resting metabolic rate, which may promote decreases in body
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fat.21 In the arms, however, there was no reduction in FM, probably due to the smaller
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baseline FM in these limbs.
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BMC was found to be higher in the arms after the training protocol. WR is a sport
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with high physical requirement,14 where athletes need to make rapid movements
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during the game and are required to perform abrupt stops to block the opponent or to
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change the direction of movement. Therefore, it can be assumed that the increased
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mechanical stress to which the arms of WR players are subjected22 might explain the
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gain of BMC in these limbs. Conversely, no difference in leg BMC was detected after
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training. Given that the average time since injury was approximately 7 years in our
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sample and that WR does not require lower limb activity, our findings are in
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accordance with previous data which showed that bone loss in the legs of SCI
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individuals usually reaches a steady state up to 7 years after injury.23
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An interesting finding of our study was that BMC in the trunk was significantly lower
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after training. This unexpected result seems to be in agreement with data from a
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former cross-sectional study, which showed a higher lumbar spine bone mass
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density (Z score) in sedentary rather than in physically-active SCI tetraplegic
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individuals.24 The reason for this finding is not clear. It has been suggested that
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sedentary SCI individuals are more susceptible to extraneous calcification on that
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region24. In this context, we may hypothesize that WR training would help preventing
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this situation. On the other hand, it can be also speculated that trunk BMC changes
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were due to the natural history of SCI-induced bone mass loss. Nevertheless,
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previous data have suggested that lumbar spine BMC does not significantly change
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even after several years of injury25, thus making this hypothesis less probable.
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It was noteworthy that training-induced changes in arms and trunk BMC were not
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paralleled by variation in corresponding BMD. BMD is obtained by dividing BMC by
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bone area, which could lead to the assumption that BMC and BMD should be tightly
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correlated. However, it has been shown that not only BMC but also bone area can
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change over time.26,27 In this regard, we found that exercise-induced changes in arms
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and trunk BMC were followed by parallel variations in bone area, which seems to
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explain the absence of variation in BMD after the training program.
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The present data indicate that WR may modify body composition of tetraplegic
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individuals, which could potentially lead to a more favorable cardiovascular and
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metabolic profile. So, further longitudinal studies in larger populations are necessary
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to evaluate the impact of body composition changes induced by the WR on metabolic
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characteristics, such as lipid and glycemic profiles and cardiovascular features, such
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as atherosclerosis and cardiac structure and function. In addition, it is necessary to
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evaluate whether the trend toward decreased trunk bone mass may be also
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reproduced in other SCI populations subjected to adapted sports activities.
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Some potential limitations of this study should be acknowledged. First, there were
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differences in the time between the measurements among the studied subjects.
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However, we did not find a significant correlation between the duration of training and
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measures that significant modified after training, indicating that the participants of
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study achieved significant results even after little intervention time. Second, the
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participants were recruited by convenience and thus were not randomized. In
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addition, we did not assess body composition changes in a control group of SCI
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individuals who did not perform physical activity. This approach would be valuable to
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confirm that variation in body composition in the intervention group was due to the
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training program. However, it has been consistently shown that chronic SCI is
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associated with progressively worse body composition profile28 and decreases in
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bone mass,29 which support the notion that our results showing changes in body
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composition and bone mass were due to the WR training program.
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CONCLUSION
2 In summary, we present the first longitudinal study assessing the impact of WR on
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the body composition of tetraplegic individuals. Our results showed that regular
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training increased lean mass and BMC in the arms and decreased FM mass in the
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whole body, thus supporting the notion that WR is a useful approach in order to
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promote a more favorable metabolic profile in SCI individuals. Conversely, we
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provided novel evidence that regular WR training seems to be associated with
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decreased bone mass in the trunk. Whether this latter finding has clinical significance
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or is related to a higher risk of local fractures remains to be established.
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PRACTICAL IMPLICATION
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o Wheelchair rugby training improves body composition profile, by
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increasing lean mass (muscle) in the arms and by decreasing fat mass
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in the whole body.
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o Wheelchair Rugby training may be a useful approach in order to
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promote a more favorable metabolic profile in spinal cord injured
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subjects.
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Acknowledgments:
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Conflict of Interest: The authors declare no conflict of interests.
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28 - Dionyssiotis Y, Petropoulou K, Rapidi CA, et al. Body Composition in Paraplegic
5
Men. J Clin Densitom 2008;11:437- 443.
6
29 – Clasey JL, Janowiak AL, Gater DV. Relationship Between Regional Bone
7
Density Measurements and the Time Since Injury in Adults With Spinal Cord Injuries.
8
Arch Phys Med Rehabil 2004;85:59-64.
AC C
EP
TE D
M AN U
SC
RI PT
1
1
ACCEPTED MANUSCRIPT TSI (years)
AIS
Heigth (m)
Mass T1 (kg)
Mass T2 (Kg)
22
10
5.3
A
1.72
65.7
66.7
2
24
9
2.8
C
1.57
57.0
56.3
3
27
8
6.2
B
1.70
55.8
57.2
4
33
8
15.0
A
1.85
75.5
72.6
5
30
10
4.0
A
1.71
62.1
61.3
6
33
10
5.6
A
1.76
62.6
63.6
7
23
9
6.0
A
1.75
62.5
61.7
8
22
3
2.0
A
1.78
58.1
56.7
9
24
3
10
26
11
11
21
8
12
20
8
13
41
8
Mean
26.62
SD (±)
6.02
M AN U
RI PT
1
SC
Table 1. Participants information Age at TBM Sub. baseline (months) (years)
1.0
A
1.98
64.5
63.6
13.0
A
1.70
62.1
64.3
4.4
A
1.83
76.2
67.1
3.4
A
1.86
64.6
62.9
7.6
B
1.79
67.8
68.7
TE D
1
8.08
7.03
1.77
64.2
63.3
2.47
4.23
0.10
6.2
4.8
Legend. TBM – time between measurements; TSI – Time since injury; AIS –
3
American Spinal Injury Association Impairment Scale.
AC C
4
EP
2
1
ACCEPTED MANUSCRIPT 1
Table 2. Comparative findings on body composition between pre-and post
2
assessments. T2 20.3 ± 1.9
214 ± 31 183 ± 35 0.851 ± 0.060 721 ± 311 2,991 ± 549
230 ± 30 195 ± 32 0.855 ± 0.069 716 ± 295 3,332 ± 602
632 ± 75 553 ± 82 0.896 ± 0.094 7,058 ± 2,639 23,326 ± 2,407
599 ± 74 521 ± 86 0.882 ± 0.093 5,693 ± 1,498 23,238 ± 1,601
5.3 5.8 1.6 19.3 0.4
0.027* 0.034* 0.272 0.012 0.858
310 ± 38 315.9 (81.5) 0.977 (0.143) 2,847 ± 817 6,793 ± 1,019
304 ± 36 304.7 (35.5) 0.967 (0.104) 2,534 ± 742 6,889 ± 823
1.5 3.5 1.0 11.0 1.4
0.704 0.946 0.706 0.003* 0.513
1.947 ± 163 2,200 ± 299 1.129 ± 0.114 15,191 ± 4,603 46,749 ± 4,831
1.951 ± 166 2,191 ± 295 1.129 ± 0.121 13,212 ± 3,318 47,661 ± 3,451
0.2 0.4 0.0 13.0 2.0
0.951 0.944 0.965 0.016* 0.308
RI PT
∆% 1.2
7.9 6.6 0.5 0.7 11.4
SC
M AN U
TE D
AC C
p-value 0.731
T1 20.6 ± 1.9
EP
Body mass index, k/m Body composition Arms Bone area, cm2 BMC, g BMD, g/cm2 FM, g FFM, g Trunk Bone area, cm2 BMC, g BMD, g/cm2 FM, g FFM, g Legs Bone area, cm2 BMC, g BMD, g/cm2 FM, g FFM, g Total body Bone area, cm2 BMC, g BMD, g/cm2 FM, g FFM, g
2
0.009* 0.010* 0.493 0.944 0.016
3
Legend. BMC - bone mass content; BMD - bone mineral density; FM - fat mass; FFT
4
– fat-free mass; T1 – pre-assessment; T2 - post–assessment. BMC and BMD of legs
5
are presented as median (interquartile range), while all other data are presented as
6
mean ± standard deviation. * denotes statistical significance with p ≤ 0.05. ∆% -
7
Percentual difference between pre-and post assessments.
8