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Effect of Exercise on Cardiometabolic Risk Factors in Adults With Chronic Spinal Cord Injury: A Systematic Review

      Abstract

      Objective

      To determine the effects of exercise on individual cardiometabolic syndrome (CMS) risk factors in adults with chronic spinal cord injury (SCI).

      Data Sources

      English language searches of PubMed, Web of Science, EMBASE, and Scopus (January 1, 1970, to July 31, 2019).

      Study Selection

      Articles were included if they met the following criteria: (1) original articles with statistical analysis, (2) participants were adults with a SCI sustained ≥1 year ago, (3) exercise intervention duration ≥2 weeks, and (4) included any CMS risk factor as an outcome.

      Data Extraction

      The methodological quality of articles was assessed using the Downs and Black score.

      Data Synthesis

      Sixty-five studies were included for the final analysis, including 9 studies classified as high quality (≥66.7%), 35 studies classified as fair quality (50%-66.6%), and 21 studies classified as low quality (<50%). Improvements in waist circumference (4/6 studies) and markers of hepatic insulin sensitivity (4/5 studies) were reported following upper body aerobic exercise training, but no improvements in fasting glucose (8/8 studies), lipid profile (6/8 studies), systolic blood pressure (8/9 studies), or diastolic blood pressure (9/9 studies) were observed. Improvements in markers of peripheral insulin sensitivity (5/6 studies) were observed following functional electrical stimulation (FES) cycling. Improvements in lipid profile (4/5 studies) were observed following upper body resistance training (RT) (with or without aerobic exercise). No consistent improvements in CMS risk factors were observed following assisted ambulation, FES hybrid, FES rowing, and FES RT.

      Conclusions

      Upper body aerobic exercise training (>75% maximum heart rate) appears to improve waist circumference and hepatic insulin sensitivity but appears insufficient for improving fasting glucose, lipid profile, or resting blood pressure. The addition of RT to upper body aerobic exercise may elicit favorable changes in the lipid profile. More high-quality studies are needed to confirm if FES cycling is effective at improving peripheral insulin sensitivity.

      Keywords

      List of abbreviations:

      CMS (cardiometabolic syndrome), DBP (diastolic blood pressure), ES (effect size), FES (functional electrical stimulation), HDL-C (high-density lipoprotein cholesterol), HOMA-IR (homeostasis model assessment of insulin resistance), HRR (heart rate reserve), LDL-C (low-density lipoprotein cholesterol), RT (resistance training), RCT (randomized controlled trial), SBP (systolic blood pressure), SCI (spinal cord injury), TC (total cholesterol), TG (triglyceride)
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      References

        • Cragg J.J.
        • Noonan V.K.
        • Dvorak M.
        • Krassioukov A.
        • Mancini G.B.
        • Borisoff J.F.
        Spinal cord injury and type 2 diabetes: results from a population health survey.
        Neurology. 2013; 81: 1864-1868
        • Cragg J.J.
        • Noonan V.K.
        • Krassioukov A.
        • Borisoff J.
        Cardiovascular disease and spinal cord injury: results from a national population health survey.
        Neurology. 2013; 81: 723-728
        • Wannamethee S.G.
        • Shaper A.G.
        • Lennon L.
        • Morris R.W.
        Metabolic syndrome vs Framingham Risk Score for prediction of coronary heart disease, stroke, and type 2 diabetes mellitus.
        Arch Intern Med. 2005; 165: 2644-2650
        • Alberti K.
        • Zimmet P.
        • Shaw J.
        Metabolic syndrome - a new world-wide definition. A consensus statement from the International Diabetes Federation.
        Diabet Med. 2006; 23: 469-480
        • Ravensbergen H.J.C.
        • Lear S.A.
        • Claydon V.E.
        Waist circumference is the best index for obesity-related cardiovascular disease risk in individuals with spinal cord injury.
        J Neurotrauma. 2014; 31: 292-300
        • Laughton G.E.
        Lowering body mass index cutoffs better identifies obese persons with spinal cord injury.
        Spinal Cord. 2009; 47: 757-763
        • Gater D.R.
        • Farkas G.J.
        • Berg A.S.
        • Castillo C.
        Prevalence of metabolic syndrome in veterans with spinal cord injury.
        J Spinal Cord Med. 2019; 42: 86-93
        • Booth F.W.
        • Roberts C.K.
        • Laye M.J.
        Lack of exercise is a major cause of chronic diseases.
        Compr Physiol. 2012; 2: 1143-1211
        • Piercy K.
        • Troiano R.
        • Ballard R.M.
        • et al.
        The physical activity guidelines for Americans.
        J Am Med Assoc. 2018; 320: 2020-2028
        • World Health Organization
        Global recommendations on physical activity for health.
        World Health Organization, Geneva, Switzerland2010
        • van der Scheer J.W.
        • Ginis K.A.M.
        • Ditor D.S.
        • et al.
        Effects of exercise on fitness and health of adults with spinal cord injury: a systematic review.
        Neurology. 2017; 89: 736-745
        • Ginis K.A.M.
        • van der Scheer J.W.
        • Latimer-Cheung A.E.
        • et al.
        Evidence-based scientific exercise guidelines for adults with spinal cord injury: an update and a new guideline.
        Spinal Cord. 2018; 56: 308-321
        • Neefkes-Zonneveld C.R.
        • Bakkum A.J.
        • Bishop N.C.
        • van Tulder M.W.
        • Janssen T.W.
        Effect of long-term physical activity and acute exercise on markers of systemic inflammation in persons with chronic spinal cord injury: a systematic review.
        Arch Phys Med Rehabil. 2015; 96: 30-42
        • Shojaei M.H.
        • Alavinia S.M.
        • Craven B.C.
        Management of obesity after spinal cord injury: a systematic review.
        J Spinal Cord Med. 2017; 40: 783-794
        • Liberati A.
        • Altman D.G.
        • Tetzlaff J.
        • et al.
        The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration.
        BMJ. 2009; 339: b2700
        • El-Sayed M.S.
        • Younesian A.
        Lipid profiles are influenced by arm cranking exercise and training in individuals with spinal cord injury.
        Spinal Cord. 2005; 43: 299-305
        • Petrofsky J.S.
        • Stacy R.
        The effect of training on endurance and the cardiovascular responses of individuals with paraplegia during dynamic exercise induced by functional electrical stimulation.
        Eur J Appl Physiol Occup Physiol. 1992; 64: 487-492
        • Downs S.H.
        • Black N.
        The feasibility of creating a checklist for the assessment of the methodological quality both of randomised and non-randomised studies of health care interventions.
        J Epidemiol Community Health. 1998; 52: 377-384
        • Batacan R.B.
        • Duncan M.J.
        • Dalbo V.J.
        • Tucker P.S.
        • Fenning A.S.
        Effects of high- intensity interval training on cardiometabolic health: a systematic review and meta-analysis of intervention studies.
        Br J Sports Med. 2017; 51: 494-503
        • Hooker S.P.
        • Wells C.L.
        Effects of low- and moderate-intensity training in spinal cord-injured persons.
        Med Sci Sports Exerc. 1989; 21: 18-22
        • Bakkum A.J.
        • Paulson T.A.
        • Bishop N.C.
        • et al.
        Effects of hybrid cycle and handcycle exercise on cardiovascular disease risk factors in people with spinal cord injury: a randomized controlled trial.
        J Rehabil Med. 2015; 47: 523-530
        • Nightingale T.E.
        • Walhin J.P.
        • Thompson D.
        • Bilzon J.L.J.
        Impact of exercise on cardiometabolic component risks in spinal cord-injured humans.
        Med Sci Sports Exerc. 2017; 49: 2469-2477
        • Rosety-Rodriguez M.
        • Camacho A.
        • Rosety I.
        • et al.
        Low-grade systemic inflammation and leptin levels were improved by arm cranking exercise in adults with chronic spinal cord injury.
        Arch Phys Med Rehabil. 2014; 95: 297-302
        • Bresnahan J.J.
        • Farkas G.J.
        • Clasey J.L.
        • Yates J.W.
        • Gater D.R.
        Arm crank ergometry improves cardiovascular disease risk factors and community mobility independent of body composition in high motor complete spinal cord injury.
        J Spinal Cord Med. 2018; 42: 272-280
        • Han D.S.
        • Hsiao M.Y.
        • Wang T.G.
        • Chen S.Y.
        • Yang W.S.
        Association of serum myokines and aerobic exercise training in patients with spinal cord injury: an observational study.
        BMC Neurol. 2016; 16: 142
        • McLean K.P.
        • Skinner J.S.
        Effect of body training position on outcomes of an aerobic training study on individuals with quadriplegia.
        Arch Phys Med Rehabil. 1995; 76: 139-150
        • Gorgey A.S.
        • Graham Z.A.
        • Bauman W.A.
        • Cardozo C.
        • Gater D.R.
        Abundance in proteins expressed after functional electrical stimulation cycling or arm cycling ergometry training in persons with chronic spinal cord injury.
        J Spinal Cord Med. 2017; 40: 439-448
        • Akkurt H.
        • Karapolat H.U.
        • Kirazli Y.
        • Kose T.
        The effects of upper extremity aerobic exercise in patients with spinal cord injury: a randomized controlled study.
        Eur J Phys Rehabil Med. 2017; 53: 219-227
        • Kim D.I.
        • Lee H.
        • Lee B.S.
        • Kim J.
        • Jeon J.Y.
        Effects of a 6-week indoor hand-bike exercise program on health and fitness levels in people with spinal cord injury: a randomized controlled trial study.
        Arch Phys Med Rehabil. 2015; 96: 2033-2040
        • Horiuchi M.
        • Okita K.
        Arm-cranking exercise training reduces plasminogen activator inhibitor 1 in people with spinal cord injury.
        Arch Phys Med Rehabil. 2017; 98: 2174-2180
        • Midha M.
        • Schmitt J.K.
        • Sclater M.
        Exercise effect with the wheelchair aerobic fitness trainer on conditioning and metabolic function in disabled persons: a pilot study.
        Arch Phys Med Rehabil. 1999; 80: 258-261
        • Mukherjee G.
        • Bhowmik P.
        • Samanta A.
        Physical fitness training for wheelchair ambulation by the arm crank propulsion technique.
        Clin Rehabil. 2001; 15: 125-132
        • Gass G.C.
        • Watson J.
        • Camp E.M.
        • Court H.J.
        • McPherson L.M.
        • Redhead P.
        The effects of physical training on high level spinal lesion patients.
        Scand J Rehabil Med. 1980; 12: 61
        • Yim S.Y.
        • Cho K.J.
        • Park C.I.
        • et al.
        Effect of wheelchair ergometer training on spinal cord-injured paraplegics.
        Yonsei Med J. 1993; 34: 278-286
        • Davis G.M.
        • Shephard R.J.
        • Leenen F.H.
        Cardiac effects of short term arm crank training in paraplegics: echocardiographic evidence.
        Eur J Appl Physiol Occup Physiol. 1987; 56: 90-96
        • Giangregorio L.
        • Craven C.
        • Richards K.
        • et al.
        A randomized trial of functional electrical stimulation for walking in incomplete spinal cord injury: effects on body composition.
        J Spinal Cord Med. 2012; 35: 351-360
        • de Zepetnek JOT
        • Pelletier C.A.
        • Hicks A.L.
        • MacDonald M.J.
        Following the physical activity guidelines for adults with spinal cord injury for 16 weeks does not improve vascular health: a randomized controlled trial.
        Arch Phys Med Rehabil. 2015; 96: 1566-1575
        • Mogharnasi M.
        • TaheriChadorneshin H.
        • Papoli-Baravati S.A.
        • Teymuri A.
        Effects of upper-body resistance exercise training on serum nesfatin-1 level, insulin resistance, and body composition in obese paraplegic men.
        Disabil Health J. 2019; 12: 29-34
        • Kim D.I.
        • Taylor J.A.
        • Tan C.O.
        • et al.
        A pilot randomized controlled trial of 6-week combined exercise program on fasting insulin and fitness levels in individuals with spinal cord injury.
        Eur Spine J. 2019; 28: 1082-1091
        • Cugusi L.
        • Solla P.
        • Serpe R.
        • et al.
        Effects of an adapted physical training on functional status, body composition and quality of life in persons with spinal cord injury paraplegia: a pilot study.
        Med Sport (Roma). 2015; 68: 473-485
        • Hicks A.L.
        • Adams M.M.
        • Martin Ginis K.
        • et al.
        Long-term body-weight-supported treadmill training and subsequent follow-up in persons with chronic SCI: effects on functional walking ability and measures of subjective well-being.
        Spinal Cord. 2005; 43: 291-298
        • Nash M.S.
        • Jacobs P.L.
        • Mendez A.J.
        • Goldberg R.B.
        Circuit resistance training improves the atherogenic lipid profiles of persons with chronic paraplegia.
        J Spinal Cord Med. 2001; 24: 2-9
        • Allison D.J.
        • Chapman B.
        • Wolfe D.
        • Sequeira K.
        • Hayes K.
        • Ditor D.S.
        Effects of a functional electrical stimulation-assisted cycling program on immune and cardiovascular health in persons with spinal cord injury.
        Top Spinal Cord Inj Rehabil. 2016; 22: 71-78
        • Sadowsky C.L.
        • Hammond E.R.
        • Strohl A.B.
        • et al.
        Lower extremity functional electrical stimulation cycling promotes physical and functional recovery in chronic spinal cord injury.
        J Spinal Cord Med. 2013; 36: 623-631
        • Jeon J.Y.
        • Weiss C.B.
        • Steadward R.D.
        • et al.
        Improved glucose tolerance and insulin sensitivity after electrical stimulation-assisted cycling in people with spinal cord injury.
        Spinal Cord. 2002; 40: 110-117
        • Gerrits H.L.
        Peripheral vascular changes after electrically stimulated cycle training in people with spinal cord injury.
        Arch Phys Med Rehabil. 2001; 82: 832-840
        • Liu C.W.
        • Chen S.C.
        • Chen C.H.
        • et al.
        Effects of functional electrical stimulation on peak torque and body composition in patients with incomplete spinal cord injury.
        Kaohsiung J Med Sci. 2007; 23: 232-240
        • Faghri P.D.
        • Glaser R.M.
        • Figoni S.F.
        Functional electrical stimulation leg cycle ergometer exercise: training effects on cardiorespiratory responses of spinal cord injured subjects at rest and during submaximal exercise.
        Arch Phys Med Rehabil. 1992; 73: 1085-1093
        • Griffin L.
        • Decker M.J.
        • Hwang J.Y.
        • et al.
        Functional electrical stimulation cycling improves body composition, metabolic and neural factors in persons with spinal cord injury.
        J Electromyogr Kinesiol. 2009; 19: 614-622
        • Robergs R.A.
        • Appenzeller O.
        • Qualls C.
        • et al.
        Increased endothelin and creatine kinase after electrical stimulation of paraplegic muscle.
        J Appl Physiol. 1993; 75: 2400-2405
        • Hjeltnes N.
        • Aksnes A.K.
        • Birkeland K.I.
        • Johansen J.
        • Lannem A.
        • WallbergHenriksson H.
        Improved body composition after 8 wk of electrically stimulated leg cycling in tetraplegic patients.
        Am J Physiol Regul Integr Comp Physiol. 1997; 273: R1072-R1079
        • Kahn N.N.
        • Feldman S.P.
        • Bauman W.A.
        Lower-extremity functional electrical stimulation decreases platelet aggregation and blood coagulation in persons with chronic spinal cord injury: a pilot study.
        J Spinal Cord Med. 2010; 33: 150-158
        • Hjeltnes N.
        • Galuska D.
        • Bjornholm M.
        • et al.
        Exercise-induced overexpression of key regulatory proteins involved in glucose uptake and metabolism in tetraplegic persons: molecular mechanism for improved glucose homeostasis.
        FASEB J. 1998; 12: 1701-1712
        • Lammers G.
        • Van Duijnhoven N.T.L.
        • Hoenderop J.G.
        • et al.
        The identification of genetic pathways involved in vascular adaptations after physical deconditioning versus exercise training in humans.
        Exp Physiol. 2013; 98: 710-721
        • Mohr T.
        • Dela F.
        • Handberg A.
        • Biering-Sorensen F.
        • Galbo H.
        • Kjaer M.
        Insulin action and long-term electrically induced training in individuals with spinal cord injuries.
        Med Sci Sports Exerc. 2001; 33: 1247-1252
        • Sköld C.
        • Lönn L.
        • Harms-Ringdahl K.
        • et al.
        Effects of functional electrical stimulation training for six months on body composition and spasticity in motor complete tetraplegic spinal cord-injured individuals.
        J Rehabil Med. 2002; 34: 25-32
        • Chilibeck P.D.
        • Bell G.
        • Jeon J.
        • et al.
        Functional electrical stimulation exercise increases GLUT-1 and GLUT-4 in paralyzed skeletal muscle.
        Metabolism. 1999; 48: 1409-1413
        • Gorgey A.S.
        • Khalil R.
        • Gill R.S.
        • et al.
        Low-dose testosterone and evoked resistance exercise after spinal cord injury on cardio-metabolic risk factors: an open-label randomized clinical trial.
        J Neurotrauma. 2019; 36: 2631-2645
        • Gorgey A.S.
        • Mather K.J.
        • Cupp H.R.
        • Gater D.R.
        Effects of resistance training on adiposity and metabolism after spinal cord injury.
        Med Sci Sports Exerc. 2012; 44: 165-174
        • Rodgers M.M.
        • Glaser R.M.
        • Figoni S.F.
        • et al.
        Musculoskeletal responses of spinal cord injured individuals to functional neuromuscular stimulation-induced knee extension exercise training.
        J Rehabil Res Dev. 1991; 28: 19-26
        • Ryan T.E.
        • Brizendine J.T.
        • Backus D.
        • McCully K.K.
        Electrically induced resistance training in individuals with motor complete spinal cord injury.
        Arch Phys Med Rehabil. 2013; 94: 2166-2173
        • Stoner L.
        • Sabatier M.J.
        • Mahoney E.T.
        • Dudley G.A.
        • McCully K.K.
        Electrical stimulation-evoked resistance exercise therapy improves arterial health after chronic spinal cord injury.
        Spinal Cord. 2007; 45: 49-56
        • Ragnarsson K.T.
        • Pollack S.
        • O'Daniel Jr., W.
        • Edgar R.
        • Petrofsky J.
        • Nash M.S.
        Clinical evaluation of computerized functional electrical stimulation after spinal cord injury: a multicenter pilot study.
        Arch Phys Med Rehabil. 1988; 69: 672-677
        • Pollack S.F.
        • Axen K.
        • Spielholz N.
        • Levin N.
        • Haas F.
        • Ragnarsson K.T.
        Aerobic training effects of electrically induced lower extremity exercises in spinal cord injured people.
        Arch Phys Med Rehabil. 1989; 70: 214-219
        • Mahoney E.T.
        • Bickel C.S.
        • Elder C.
        • Black C.
        • Slade J.M.
        • Apple D.
        • et al.
        Changes in skeletal muscle size and glucose tolerance with electrically stimulated resistance training in subjects with chronic spinal cord injury.
        Arch Phys Med Rehabil. 2005; 86: 1502-1504
        • Pacy P.J.
        • Hesp R.
        • Halliday D.A.
        • Katz D.
        • Cameron G.
        • Reeve J.
        Muscle and bone in paraplegic patients, and the effect of functional electrical stimulation.
        Clin Sci (Lond). 1988; 75: 481-487
        • Thijssen D.H.
        • Ellenkamp R.
        • Smits P.
        • Hopman M.T.
        Rapid vascular adaptations to training and detraining in persons with spinal cord injury.
        Arch Phys Med Rehabil. 2006; 87: 474-481
        • Kim D.I.
        • Park D.S.
        • Lee B.S.
        • Jeon J.Y.
        A six-week motor-driven functional electronic stimulation rowing program improves muscle strength and body composition in people with spinal cord injury: a pilot study.
        Spinal Cord. 2014; 52: 621-624
        • Qiu S.
        • Alzhab S.
        • Picard G.
        • Taylor J.A.
        Ventilation limits aerobic capacity after functional electrical stimulation row training in high spinal cord injury.
        Med Sci Sports Exerc. 2016; 48: 1111-1119
        • Thijssen D.H.
        • Heesterbeek P.
        • van Kuppevelt D.J.
        • Duysens J.
        • Hopman M.T.
        Local vascular adaptations after hybrid training in spinal cord-injured subjects.
        Med Sci Sports Exerc. 2005; 37: 1112-1118
        • Wilbanks S.R.
        • Rogers R.
        • Pool S.
        • Bickel C.S.
        Effects of functional electrical stimulation assisted rowing on aerobic fitness and shoulder pain in manual wheelchair users with spinal cord injury.
        J Spinal Cord Med. 2016; 39: 645-654
        • Jeon J.Y.
        • Hettinga D.
        • Steadward R.D.
        • Wheeler G.D.
        • Bell G.
        • Harber V.
        Reduced plasma glucose and leptin after 12 weeks of functional electrical stimulation-rowing exercise training in spinal cord injury patients.
        Arch Phys Med Rehabil. 2010; 91: 1957-1959
        • Hasnan N.
        • Engkasan J.P.
        • Husain R.
        • Davis G.M.
        High-intensity virtual-reality arm plus FES-leg interval training in individuals with spinal cord injury.
        Biomed Tech (Berl). 2013; 58
        • Gorman P.H.
        • Scott W.
        • York H.
        • et al.
        Robotically assisted treadmill exercise training for improving peak fitness in chronic motor incomplete spinal cord injury: a randomized controlled trial.
        J Spinal Cord Med. 2016; 39: 32-44
        • Ditor D.S.
        • MacDonald M.J.
        • Kamath M.V.
        • et al.
        The effects of body-weight supported treadmill training on cardiovascular regulation in individuals with motor-complete SCI.
        Spinal Cord. 2005; 43: 664-673
        • Ditor D.S.
        • Kamath M.V.
        • MacDonald M.J.
        • Bugaresti J.
        • McCartney N.
        • Hicks A.L.
        Effects of body weight-supported treadmill training on heart rate variability and blood pressure variability in individuals with spinal cord injury.
        J Appl Physiol. 2005; 98: 1519-1525
        • Turiel M.
        • Sitia S.
        • Cicala S.
        • et al.
        Robotic treadmill training improves cardiovascular function in spinal cord injury patients.
        Int J Cardiol. 2011; 149: 323-329
        • Giangregorio L.M.
        • Webber C.E.
        • Phillips S.M.
        • et al.
        Can body weight supported treadmill training increase bone mass and reverse muscle atrophy in individuals with chronic incomplete spinal cord injury?.
        Appl Physiol Nutr Metab. 2006; 31: 283-291
        • Karelis A.D.
        • Carvalho L.P.
        • Castillo M.J.
        • Gagnon D.H.
        • Aubertin-Leheudre M.
        Effect on body composition and bone mineral density of walking with a robotic exoskeleton in adults with chronic spinal cord injury.
        J Rehabil Med. 2017; 49: 84-87
        • Stewart B.G.
        • Tarnopolsky M.A.
        • Hicks A.L.
        • et al.
        Treadmill training-induced adaptations in muscle phenotype in persons with incomplete spinal cord injury.
        Muscle Nerve. 2004; 30: 61-68
        • Phillips S.M.
        • Stewart B.G.
        • Mahoney D.J.
        • et al.
        Body-weight-support treadmill training improves blood glucose regulation in persons with incomplete spinal cord injury.
        J Appl Physiol. 2004; 97: 716-724
        • Klose K.J.
        • Jacobs P.L.
        • Broton J.G.
        • et al.
        Evaluation of a training program for persons with SCI paraplegia using the Parastep(R)1 ambulation system: part 1. Ambulation performance and anthropometric measures.
        Arch Phys Med Rehabil. 1997; 78: 789-793
        • Jones M.L.
        • Evans N.
        • Tefertiller C.
        • et al.
        Activity-based therapy for recovery of walking in individuals with chronic spinal cord injury: results from a randomized clinical trial.
        Arch Phys Med Rehabil. 2014; 95: 2239-2246
        • Li J.
        • Polston K.F.L.
        • Eraslan M.
        • et al.
        A high-protein diet or combination exercise training to improve metabolic health in individuals with long-standing spinal cord injury: a pilot randomized study.
        Physiol Rep. 2018; 6e13813
        • Ordonez F.J.
        • Rosety M.A.
        • Camacho A.
        • et al.
        Arm-cranking exercise reduced oxidative damage in adults with chronic spinal cord injury.
        Arch Phys Med Rehabil. 2013; 94: 2336-2341
        • Rosety-Rodriguez M.
        • Rosety I.
        • Fornieles G.
        • et al.
        A short-term arm-crank exercise program improved testosterone deficiency in adults with chronic spinal cord injury.
        Int Braz J Urol. 2014; 40: 367-372
        • Sim J.
        The Kappa statistic in reliability studies: use, interpretation, and sample size requirements.
        Phys Ther. 2005; 85: 257-269
        • Thompson J.D.
        • Peacock A.O.
        • Betts A.J.
        Substitution and compensation erode the energy deficit from exercise interventions.
        Med Sci Sports Exerc. 2014; 46: 423
        • Nightingale T.E.
        • Williams S.
        • Thompson D.
        • Bilzon J.L.J.
        Energy balance components in persons with paraplegia: daily variation and appropriate measurement duration.
        Int J Behav Nutr Phys Act. 2017; 14: 132
        • Radziuk J.
        Homeostastic model assessment and insulin sensitivity/resistance.
        Diabetes. 2014; 63: 1850
        • Matsuda M.
        • Defronzo R.
        Insulin sensitivity indices obtained from oral glucose tolerance test: comparison with the euglycemic insulin clamp.
        Diabetes Care. 1999; 22: 1462-1470
        • Mann S.
        • Beedie C.
        • Jimenez A.
        Differential effects of aerobic exercise, resistance training and combined exercise modalities on cholesterol and the lipid profile: review, synthesis and recommendations.
        Sports Med. 2014; 44: 211-221
        • Gilbert O.
        • Croffoot J.R.
        • Taylor A.J.
        • Nash M.
        • Schomer K.
        • Groah S.
        Serum lipid concentrations among persons with spinal cord injury - a systematic review and meta-analysis of the literature.
        Atherosclerosis. 2014; 232: 305-312