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Exercise Guidelines to Promote Cardiometabolic Health in Spinal Cord Injured Humans: Time to Raise the Intensity?

Published:January 14, 2017DOI:https://doi.org/10.1016/j.apmr.2016.12.008

      Abstract

      Spinal cord injury (SCI) is a life-changing event that, as a result of paralysis, negatively influences habitual levels of physical activity and hence cardiometabolic health. Performing regular structured exercise therefore appears extremely important in persons with SCI. However, exercise options are mainly limited to the upper body, which involves a smaller activated muscle mass compared with the mainly leg-based activities commonly performed by nondisabled individuals. Current exercise guidelines for SCI focus predominantly on relative short durations of moderate-intensity aerobic upper-body exercise, yet contemporary evidence suggests this is not sufficient to induce meaningful improvements in risk factors for the prevention of cardiometabolic disease in this population. As such, these guidelines and their physiological basis require reappraisal. In this special communication, we propose that high-intensity interval training (HIIT) may be a viable alternative exercise strategy to promote vigorous-intensity exercise and prevent cardiometabolic disease in persons with SCI. Supplementing the limited data from SCI cohorts with consistent findings from studies in nondisabled populations, we present strong evidence to suggest that HIIT is superior to moderate-intensity aerobic exercise for improving cardiorespiratory fitness, insulin sensitivity, and vascular function. The potential application and safety of HIIT in this population is also discussed. We conclude that increasing exercise intensity could offer a simple, readily available, time-efficient solution to improve cardiometabolic health in persons with SCI. We call for high-quality randomized controlled trials to examine the efficacy and safety of HIIT in this population.

      Keywords

      List of abbreviations:

      HIIT (high-intensity interval training), MICT (moderate-intensity continuous training), PAG-SCI (Physical Activity Guidelines for Spinal Cord Injury), SCI (spinal cord injury), SIT (sprint interval training), Vo2peak (peak oxygen uptake)
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      References

        • Devivo M.J.
        • Shewchuk R.M.
        • Stover S.L.
        • Black K.J.
        • Go B.K.
        A cross-sectional study of the relationship between age and current health-status for persons with spinal-cord injuries.
        Paraplegia. 1992; 30: 820-827
        • Bauman W.A.
        • Spungen A.M.
        Disorders of carbohydrate and lipid-metabolism in veterans with paraplegia or quadriplegia: a model of premature aging.
        Metabolism. 1994; 43: 749-756
        • Garshick E.
        • Kelley A.
        • Cohen S.A.
        • et al.
        A prospective assessment of mortality in chronic spinal cord injury.
        Spinal Cord. 2005; 43: 408-416
        • Lee B.B.
        • Cripps R.A.
        • Fitzharris M.
        • Wing P.C.
        The global map for traumatic spinal cord injury epidemiology: update 2011, global incidence rate.
        Spinal Cord. 2014; 52: 110-116
        • Booth F.W.
        • Gordon S.E.
        • Carlson C.J.
        • Hamilton M.T.
        Waging war on modern chronic diseases: primary prevention through exercise biology.
        J Appl Physiol. 2000; 88: 774-787
        • Kesaniemi Y.A.
        • Danforth E.
        • Jensen M.D.
        • Kopelman P.G.
        • Lefebvre P.
        • Reeder B.A.
        Dose-response issues concerning physical activity and health: an evidence-based symposium.
        Med Sci Sports Exerc. 2001; 33: S351-S358
        • Haskell W.L.
        • Lee I.M.
        • Pate R.R.
        • et al.
        Physical activity and public health: updated recommendation for adults from the American College of Sports Medicine and the American Heart Association.
        Med Sci Sports Exerc. 2007; 39: 1423-1434
        • Washburn R.A.
        • Zhu W.M.
        • McAuley E.
        • Frogley M.
        • Figoni S.F.
        The Physical Activity Scale for Individuals With Physical Disabilities: development and evaluation.
        Arch Phys Med Rehabil. 2002; 83: 193-200
        • Ginis K.A.
        • Arbour-Nicitopoulos K.P.
        • Latimer A.E.
        • et al.
        Leisure time physical activity in a population-based sample of people with spinal cord injury part ii: activity types, intensities, and durations.
        Arch Phys Med Rehabil. 2010; 91: 729-733
        • Tanhoffer R.A.
        • Tanhoffer A.I.P.
        • Raymond J.
        • Hills A.P.
        • Davis G.M.
        Exercise, energy expenditure, and body composition in people with spinal cord injury.
        J Phys Act Health. 2014; 11: 1393-1400
        • Tanhoffer R.A.
        • Tanhoffer A.I.P.
        • Raymond J.
        • Johnson N.A.
        • Hills A.P.
        • Davis G.M.
        Energy expenditure in individuals with spinal cord injury quantified by doubly labeled water and a multi-sensor armband.
        J Phys Act Health. 2015; 12: 163-170
        • Blair S.N.
        Physical inactivity: the biggest public health problem of the 21st century.
        Br J Sports Med. 2009; 43: 1-2
        • Thyfault J.P.
        • Krogh-Madsen R.
        Metabolic disruptions induced by reduced ambulatory activity in free-living humans.
        J Appl Physiol. 2011; 111: 1218-1224
        • Ginis K.A.
        • Hicks A.L.
        • Latimer A.E.
        • et al.
        The development of evidence-informed physical activity guidelines for adults with spinal cord injury.
        Spinal Cord. 2011; 49: 1088-1096
        • Evans N.
        • Wingo B.
        • Sasso E.
        • Hicks A.
        • Gorgey A.S.
        • Harness E.
        Exercise recommendations and considerations for persons with spinal cord injury.
        Arch Phys Med Rehabil. 2015; 96: 1749-1750
      1. Tweedy SM, Beckman EM, Geraghty TJ, et al. Exercise and Sports Science Australia (ESSA) position statement on exercise and spinal cord injury. J Sci Med Sport. 2016 Mar 9. [Epub ahead of print].

        • Theisen D.
        Cardiovascular determinants of exercise capacity in the Paralympic athlete with spinal cord injury.
        Exp Physiol. 2012; 97: 319-324
        • Jehl J.L.
        • Gandmontagne M.
        • Pastene G.
        • Eyssette M.
        • Flandrois R.
        • Coudert J.
        Cardiac output during exercise in paraplegic subjects.
        Eur J Appl Physiol Occup Physiol. 1991; 62: 256-260
        • Jacobs K.A.
        • Burns P.
        • Kressler J.
        • Nash M.S.
        Heavy reliance on carbohydrate across a wide range of exercise intensities during voluntary arm ergometry in persons with paraplegia.
        J Spinal Cord Med. 2013; 36: 427-435
        • de Zepetnek J.O.
        • 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
        • Carlson K.F.
        • Wilt T.J.
        • Taylor B.C.
        • et al.
        Effect of exercise on disorders of carbohydrate and lipid metabolism in adults with traumatic spinal cord injury: systematic review of the evidence.
        J Spinal Cord Med. 2009; 32: 361-378
        • Rimmer J.H.
        • Riley B.
        • Wang E.
        • Rauworth A.
        • Jurkowski J.
        Physical activity participation among persons with disabilities: barriers and facilitators.
        Am J Prev Med. 2004; 26: 419-425
        • Kehn M.
        • Kroll T.
        Staying physically active after spinal cord injury: a qualitative exploration of barriers and facilitators to exercise participation.
        BMC Public Health. 2009; 9: 168
        • Craig A.
        • Tran Y.
        • Wijesuriya N.
        • Middleton J.
        Fatigue and tiredness in people with spinal cord injury.
        J Psychosom Res. 2012; 73: 205-210
        • Gorgey A.S.
        Exercise awareness and barriers after spinal cord injury.
        World J Orthop. 2014; 5: 158-162
        • Myers J.
        • Lee M.
        • Kiratli J.
        Cardiovascular disease in spinal cord injury.
        Am J Phys Med Rehabil. 2007; 86: 142-152
        • Nash M.S.
        Exercise as a health-promoting activity following spinal cord injury.
        J Neurol Phys Ther. 2005; 29: 87-106
        • 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
        • 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
        • 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
        • 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
        • 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
        • Moholdt T.
        • Wisløff U.
        • Nilsen T.I.
        • Slørdahl S.A.
        Physical activity and mortality in men and women with coronary heart disease: a prospective population-based cohort study in Norway (the HUNT study).
        Eur J Cardiovasc Prev Rehabil. 2008; 15: 639-645
        • Wisløff U.
        • Nilsen T.I.
        • Drøyvold W.B.
        • Mørkved S.
        • Slørdahl S.A.
        • Vatten L.J.
        A single weekly bout of exercise may reduce cardiovascular mortality: how little pain for cardiac gain? 'The HUNT study, Norway'.
        Eur J Cardiovasc Prev Rehabil. 2006; 13: 798-804
        • Wen C.P.
        • Wai J.P.
        • Tsai M.K.
        • et al.
        Minimum amount of physical activity for reduced mortality and extended life expectancy: a prospective cohort study.
        Lancet. 2011; 378: 1244-1253
        • Gebel K.
        • Ding D.
        • Chey T.
        • Stamatakis E.
        • Brown W.J.
        • Bauman A.E.
        Effect of moderate to vigorous physical activity on all-cause mortality in middle-aged and older Australians.
        JAMA Intern Med. 2015; 175: 970-977
        • Samitz G.
        • Egger M.
        • Zwahlen M.
        Domains of physical activity and all-cause mortality: systematic review and dose-response meta-analysis of cohort studies.
        Int J Epidemiol. 2011; 40: 1382-1400
      2. MacInnis MJ, Zacharewicz E, Martin BJ, et al. Superior mitochondrial adaptations in human skeletal muscle after interval compared to continuous single-leg cycling matched for total work. J Physiol. 2016 Jul 11. [Epub ahead of print].

        • Weston K.S.
        • Wisløff U.
        • Coombes J.S.
        High-intensity interval training in patients with lifestyle-induced cardiometabolic disease: a systematic review and meta-analysis.
        Br J Sports Med. 2014; 48: 1227-1234
        • Ramos J.S.
        • Dalleck L.C.
        • Tjonna A.E.
        • Beetham K.S.
        • Coombes J.S.
        The impact of high-intensity interval training versus moderate-intensity continuous training on vascular function: a systematic review and meta-analysis.
        Sports Med. 2015; 45: 679-692
        • Jelleyman C.
        • Yates T.
        • O'Donovan G.
        • et al.
        The effects of high-intensity interval training on glucose regulation and insulin resistance: a meta-analysis.
        Obes Rev. 2015; 16: 942-961
        • Duran F.S.
        • Lugo L.
        • Ramirez L.
        • Eusse E.
        Effects of an exercise program on the rehabilitation of patients with spinal cord injury.
        Arch Phys Med Rehabil. 2001; 82: 1349-1354
        • Hooker S.P.
        • Wells C.L.
        Effects of low-intensity and moderate-intensity training in spinal cord-injured persons.
        Med Sci Sports Exerc. 1989; 21: 18-22
        • 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
        • 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
        • Swain D.P.
        • Leutholtz B.C.
        Heart rate reserve is equivalent to %VO2 reserve, not to %VO2max.
        Med Sci Sports Exerc. 1997; 29: 410-414
        • Gibala M.J.
        • Gillen J.B.
        • Percival M.E.
        Physiological and health-related adaptations to low-volume interval training: influences of nutrition and sex.
        Sports Med. 2014; 44: S127-S137
        • Gibala M.J.
        • Little J.P.
        • van Essen M.
        • et al.
        Short-term sprint interval versus traditional endurance training: similar initial adaptations in human skeletal muscle and exercise performance.
        J Physiol. 2006; 575: 901-911
        • Cocks M.
        • Shaw C.S.
        • Shepherd S.O.
        • et al.
        Sprint interval and endurance training are equally effective in increasing muscle microvascular density and eNOS content in sedentary males.
        J Physiol. 2013; 591: 641-656
        • Shepherd S.O.
        • Cocks M.
        • Tipton K.D.
        • et al.
        Sprint interval and traditional endurance training increase net intramuscular triglyceride breakdown and expression of perilipin 2 and 5.
        J Physiol. 2013; 591: 657-675
        • Gillen J.B.
        • Martin B.J.
        • MacInnis M.J.
        • Skelly L.E.
        • Tarnopolsky M.A.
        • Gibala M.J.
        Twelve weeks of sprint interval training improves indices of cardiometabolic health similar to traditional endurance training despite a five-fold lower exercise volume and time commitment.
        PLoS One. 2016; 11: e0154075
        • Rakobowchuk M.
        • Tanguay S.
        • Burgomaster K.A.
        • Howarth K.R.
        • Gibala M.J.
        • MacDonald M.J.
        Sprint interval and traditional endurance training induce similar improvements in peripheral arterial stiffness and flow-mediated dilation in healthy humans.
        Am J Physiol Regul Integr Comp Physiol. 2008; 295: R236-R242
        • Little J.P.
        • Gillen J.B.
        • Percival M.E.
        • et al.
        Low-volume high-intensity interval training reduces hyperglycemia and increases muscle mitochondrial capacity in patients with type 2 diabetes.
        J Appl Physiol. 2011; 111: 1554-1560
      3. Harnish CR, Daniels JA, Caruso D. Training response to high-intensity interval training in a 42-year-old man with chronic spinal cord injury. J Spinal Cord Med. 2016 Jan 18. [Epub ahead of print].

        • Tjønna A.E.
        • Lee S.J.
        • Rognmo Ø.
        • et al.
        Aerobic interval training versus continuous moderate exercise as a treatment for the metabolic syndrome: a pilot study.
        Circulation. 2008; 118: 346-354
        • Ross A.
        • Leveritt M.
        Long-term metabolic and skeletal muscle adaptations to short-sprint training: implications for sprint training and tapering.
        Sports Med. 2001; 31: 1063-1082
        • Gibala M.J.
        • Little J.P.
        • Macdonald M.J.
        • Hawley J.A.
        Physiological adaptations to low-volume, high-intensity interval training in health and disease.
        J Physiol. 2012; 590: 1077-1084
        • Janssen T.W.
        • Dallmeijer A.J.
        • Veeger D.
        • van der Woude L.H.
        Normative values and determinants of physical capacity in individuals with spinal cord injury.
        J Rehabil Res Dev. 2002; 39: 29-39
        • Haisma J.A.
        • van der Woude L.H.
        • Stam H.J.
        • Bergen M.P.
        • Sluis T.A.
        • Bussmann J.B.
        Physical capacity in wheelchair-dependent persons with a spinal cord injury: a critical review of the literature.
        Spinal Cord. 2006; 44: 642-652
        • 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
        • Nightingale T.E.
        • Walhin J.P.
        • Thompson D.
        • Bilzon J.L.
        Impact of moderate-intensity exercise on metabolic health and aerobic capacity in persons with chronic paraplegia.
        Med Sci Sports Exerc. 2016; 48: 430
        • De Groot P.C.
        • Hjeltnes N.
        • Heijboer A.C.
        • Stal W.
        • Birkeland K.
        Effect of training intensity on physical capacity, lipid profile and insulin sensitivity in early rehabilitation of spinal cord injured individuals.
        Spinal Cord. 2003; 41: 673-679
        • Helgerud J.
        • Høydal K.
        • Wang E.
        • et al.
        Aerobic high-intensity intervals improve VO2max more than moderate training.
        Med Sci Sports Exerc. 2007; 39: 665-671
        • Nybo L.
        • Sundstrup E.
        • Jakobsen M.D.
        • et al.
        High-intensity training versus traditional exercise interventions for promoting health.
        Med Sci Sports Exerc. 2010; 42: 1951-1958
        • Schjerve I.E.
        • Tyldum G.A.
        • Tjønna A.E.
        • et al.
        Both aerobic endurance and strength training programmes improve cardiovascular health in obese adults.
        Clin Sci (Lond). 2008; 115: 283-293
        • Karstoft K.
        • Winding K.
        • Knudsen S.H.
        • et al.
        The effects of free-living interval-walking training on glycemic control, body composition, and physical fitness in type 2 diabetic patients: a randomized, controlled trial.
        Diabetes Care. 2013; 36: 228-236
        • Lee D.C.
        • Sui X.M.
        • Artero E.G.
        • et al.
        Long-term effects of changes in cardiorespiratory fitness and body mass index on all-cause and cardiovascular disease mortality in men: the Aerobics Center Longitudinal Study.
        Circulation. 2011; 124: 2483-2490
        • Kodama S.
        • Saito K.
        • Tanaka S.
        • et al.
        Cardiorespiratory fitness as a quantitative predictor of all-cause mortality and cardiovascular events in healthy men and women: a meta-analysis.
        JAMA. 2009; 301: 2024-2035
        • Blair S.N.
        • Kampert J.B.
        • Kohl III, H.W.
        • et al.
        Influences of cardiorespiratory fitness and other precursors on cardiovascular disease and all-cause mortality in men and women.
        JAMA. 1996; 276: 205-210
        • Blair S.N.
        • Kohl III, H.W.
        • Paffenbarger Jr., R.S.
        • Clark D.G.
        • Cooper K.H.
        • Gibbons L.W.
        Physical fitness and all-cause mortality. A prospective study of healthy men and women.
        JAMA. 1989; 262: 2395-2401
        • Blair S.N.
        • Kohl III, H.W.
        • Barlow C.E.
        • Paffenbarger Jr., R.S.
        • Gibbons L.W.
        • Macera C.A.
        Changes in physical fitness and all-cause mortality. A prospective study of healthy and unhealthy men.
        JAMA. 1995; 273: 1093-1098
        • Myers J.
        • Prakash M.
        • Froelicher V.
        • Do D.
        • Partington S.
        • Atwood J.E.
        Exercise capacity and mortality among men referred for exercise testing.
        N Engl J Med. 2002; 346: 793-801
        • Bassett D.R.
        • Howley E.T.
        Limiting factors for maximum oxygen uptake and determinants of endurance performance.
        Med Sci Sports Exerc. 2000; 32: 70-84
        • Lundby C.
        • Montero D.
        CrossTalk opposing view: diffusion limitation of O2 from microvessels into muscle does not contribute to the limitation of Vo2 max.
        J Physiol. 2015; 593: 3759-3761
        • Wagner P.D.
        CrossTalk proposal: diffusion limitation of O2 from microvessels into muscle does contribute to the limitation of Vo2 max.
        J Physiol. 2015; 593: 3757-3758
        • van der Zwaard S.
        • de Ruiter J.C.
        • Noordhof D.A.
        • et al.
        Maximal oxygen uptake is proportional to muscle fiber oxidative capacity: from chronic heart failure patients to professional cyclists.
        J Appl Physiol (1985). 2016; 121: 636-645
        • Gifford J.R.
        • Garten R.S.
        • Nelson A.D.
        • et al.
        Symmorphosis and skeletal muscle VO2 max: in vivo and in vitro measures reveal differing constraints in the exercise-trained and untrained human.
        J Physiol. 2016; 594: 1741-1751
        • Devillard X.
        • Rimaud D.
        • Roche F.
        • Calmels P.
        Effects of training programs for spinal cord injury.
        Ann Readapt Med Phys. 2007; 50 (490-498, 480-489)
        • Hoeks J.
        • Schrauwen P.
        Muscle mitochondria and insulin resistance: a human perspective.
        Trends Endocrinol Metab. 2012; 23: 444-450
        • Lee D.E.
        • Kehlenbrink S.
        • Lee H.N.
        • Hawkins M.
        • Yudkin J.S.
        Getting the message across: mechanisms of physiological cross talk by adipose tissue.
        Am J Physiol Endocrinol Metab. 2009; 296: E1210-E1229
        • Campbell P.J.
        • Mandarino L.J.
        • Gerich J.E.
        Quantification of the relative impairment in actions of insulin on hepatic glucose-production and peripheral glucose-uptake in non-insulin-dependent diabetes-mellitus.
        Metabolism. 1988; 37: 15-21
        • Bauman W.A.
        • Kahn N.N.
        • Grimm D.R.
        • Spungen A.M.
        Risk factors for atherogenesis and cardiovascular autonomic function in persons with spinal cord injury.
        Spinal Cord. 1999; 37: 601-616
        • Nuhlicek D.N.
        • Spurr G.B.
        • Barboriak J.J.
        • Rooney C.B.
        • Elghatit A.Z.
        • Bongard R.D.
        Body-composition of patients with spinal-cord injury.
        Eur J Clin Nutr. 1988; 42: 765-773
        • Kocina P.
        Body composition of spinal cord injured adults.
        Sports Med. 1997; 23: 48-60
        • Dionyssiotis Y.
        • Petropoulou K.
        • Rapidi C.A.
        • et al.
        Body composition in paraplegic men.
        J Clin Densitom. 2008; 11: 437-443
        • Biering-Sorensen B.
        • Kristensen I.B.
        • Kjaer M.
        • Biering-Sorensen F.
        Muscle after spinal cord injury.
        Muscle Nerve. 2009; 40: 499-519
        • Capaldo B.
        • Gastaldelli A.
        • Antoniello S.
        • et al.
        Splanchnic and leg substrate exchange after ingestion of a natural mixed meal in humans.
        Diabetes. 1999; 48: 958-966
        • DeFronzo R.A.
        The triumvirate: β-cell, muscle, liver: a collusion responsible for NIDDM.
        Diabetes. 1988; 37: 667-687
        • Gorgey A.S.
        • Dudley G.A.
        Skeletal muscle atrophy and increased intramuscular fat after incomplete spinal cord injury.
        Spinal Cord. 2007; 45: 304-309
        • Shah P.K.
        • Gregory C.M.
        • Stevens J.E.
        • et al.
        Non-invasive assessment of lower extremity muscle composition after incomplete spinal cord injury.
        Spinal Cord. 2008; 46: 565-570
        • 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
        • 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.e1
        • Matsuda M.
        • DeFronzo R.A.
        Insulin sensitivity indices obtained from oral glucose tolerance testing: comparison with the euglycemic insulin clamp.
        Diabetes Care. 1999; 22: 1462-1470
        • Radziuk J.
        Homeostastic model assessment and insulin sensitivity/resistance.
        Diabetes. 2014; 63: 1850-1854
        • Mitranun W.
        • Deerochanawong C.
        • Tanaka H.
        • Suksom D.
        Continuous vs interval training on glycemic control and macro- and microvascular reactivity in type 2 diabetic patients.
        Scand J Med Sci Sports. 2014; 24: e69-e76
        • Iellamo F.
        • Manzi V.
        • Caminiti G.
        • et al.
        Matched dose interval and continuous exercise training induce similar cardiorespiratory and metabolic adaptations in patients with heart failure.
        Int J Cardiol. 2013; 167: 2561-2565
        • Iellamo F.
        • Caminiti G.
        • Sposato B.
        • et al.
        Effect of high-intensity interval training versus moderate continuous training on 24-h blood pressure profile and insulin resistance in patients with chronic heart failure.
        Intern Emerg Med. 2014; 9: 547-552
        • Earnest C.P.
        • Lupo M.
        • Thibodaux J.
        • et al.
        Interval training in men at risk for insulin resistance.
        Int J Sports Med. 2013; 34: 355-363
        • Little J.P.
        • Jung M.E.
        • Wright A.E.
        • Wright W.
        • Manders R.J.
        Effects of high-intensity interval exercise versus continuous moderate-intensity exercise on postprandial glycemic control assessed by continuous glucose monitoring in obese adults.
        Appl Physiol Nutr Metab. 2014; 39: 835-841
        • Karstoft K.
        • Christensen C.S.
        • Pedersen B.K.
        • Solomon T.P.
        The acute effects of interval- vs continuous-walking exercise on glycemic control in subjects with type 2 diabetes: a crossover, controlled study.
        J Clin Endocrinol Metab. 2014; 99: 3334-3342
        • van Loon L.J.
        • Greenhaff P.L.
        • Constantin-Teodosiu D.
        • Saris W.H.
        • Wagenmakers A.J.
        The effects of increasing exercise intensity on muscle fuel utilisation in humans.
        J Physiol. 2001; 536: 295-304
        • Bogardus C.
        • Thuillez P.
        • Ravussin E.
        • Vasquez B.
        • Narimiga M.
        • Azhar S.
        Effect of muscle glycogen depletion on in vivo insulin action in man.
        J Clin Invest. 1983; 72: 1605-1610
        • Newsom S.A.
        • Schenk S.
        • Thomas K.M.
        • et al.
        Energy deficit after exercise augments lipid mobilization but does not contribute to the exercise-induced increase in insulin sensitivity.
        J Appl Physiol. 2010; 108: 554-560
        • Holtz K.A.
        • Stephens B.R.
        • Sharoff C.G.
        • Chipkin S.R.
        • Braun B.
        The effect of carbohydrate availability following exercise on whole-body insulin action.
        Appl Physiol Nutr Metab. 2008; 33: 946-956
        • Shokawa T.
        • Imazu M.
        • Yamamoto H.
        • et al.
        Pulse wave velocity predicts cardiovascular mortality: findings from the Hawaii-Los Angeles-Hiroshima study.
        Circ J. 2005; 69: 259-264
        • Inaba Y.
        • Chen J.A.
        • Bergmann S.R.
        Prediction of future cardiovascular outcomes by flow-mediated vasodilatation of brachial artery: a meta-analysis.
        Int J Cardiovasc Imaging. 2010; 26: 631-640
        • Celermajer D.S.
        • Sorensen K.E.
        • Bull C.
        • Robinson J.
        • Deanfield J.E.
        Endothelium-dependent dilation in the systemic arteries of asymptomatic subjects relates to coronary risk factors and their interaction.
        J Am Coll Cardiol. 1994; 24: 1468-1474
        • West C.R.
        • AlYahya A.
        • Laher I.
        • Krassioukov A.
        Peripheral vascular function in spinal cord injury: a systematic review.
        Spinal Cord. 2013; 51: 10-19
        • Totosy de Zepetnek J.O.
        • Ditor D.S.
        • Au J.S.
        • MacDonald M.J.
        Impact of shear rate pattern on upper and lower limb conduit artery endothelial function in both spinal cord-injured and able-bodied men.
        Exp Physiol. 2015; 100: 1107-1117
        • Molmen-Hansen H.E.
        • Stolen T.
        • Tjonna A.E.
        • et al.
        Aerobic interval training reduces blood pressure and improves myocardial function in hypertensive patients.
        Eur J Prev Cardiol. 2012; 19: 151-160
        • Wisløff U.
        • Støylen A.
        • Loennechen J.P.
        • et al.
        Superior cardiovascular effect of aerobic interval training versus moderate continuous training in heart failure patients: a randomized study.
        Circulation. 2007; 115: 3086-3094
        • Bristow S.
        • Dalal K.
        • Santos J.O.
        • Martinez-Arizala A.
        • Banavac K.
        Prevalence of hypertension, dyslipidemia, and diabetes mellitus after spinal cord injury.
        Fed Pract. 2013; 30: 15-18
        • Wecht J.M.
        • Weir J.P.
        • Galea M.
        • Martinez S.
        • Bauman W.A.
        Prevalence of abnormal systemic hemodynamics in veterans with and without spinal cord injury.
        Arch Phys Med Rehabil. 2015; 96: 1071-1079
        • Ciolac E.G.
        • Bocchi E.A.
        • Bortolotto L.A.
        • Carvalho V.O.
        • Greve J.M.
        • Guimarães G.V.
        Effects of high-intensity aerobic interval training vs. moderate exercise on hemodynamic, metabolic and neuro-humoral abnormalities of young normotensive women at high familial risk for hypertension.
        Hypertens Res. 2010; 33: 836-843
        • Gater D.R.
        Obesity after spinal cord injury.
        Phys Med Rehabil Clin N Am. 2007; 18: 333-351
        • Gorgey A.
        • Gater D.
        Prevalence of obesity after spinal cord injury.
        Top Spinal Cord Inj Rehabil. 2007; 12: 1-7
        • Edwards L.A.
        • Bugaresti J.M.
        • Buchholz A.C.
        Visceral adipose tissue and the ratio of visceral to subcutaneous adipose tissue are greater in adults with than in those without spinal cord injury, despite matching waist circumferences.
        Am J Clin Nutr. 2008; 87: 600-607
        • Nakamura T.
        • Tokunaga K.
        • Shimomura I.
        • et al.
        Contribution of visceral fat accumulation to the development of coronary-artery disease in nonobese men.
        Atherosclerosis. 1994; 107: 239-246
        • Boyko E.J.
        • Fujimoto W.Y.
        • Leonetti D.L.
        • Newell-Morris L.
        Visceral adiposity and risk of type 2 diabetes: a prospective study among Japanese Americans.
        Diabetes Care. 2000; 23: 465-471
        • Shah R.V.
        • Murthy V.L.
        • Abbasi S.A.
        • et al.
        Visceral adiposity and the risk of metabolic syndrome across body mass index: the MESA Study.
        JACC Cardiovasc Imaging. 2014; 7: 1222-1235
        • Gorgey A.S.
        • Mather K.J.
        • Gater D.R.
        Central adiposity associations to carbohydrate and lipid metabolism in individuals with complete motor spinal cord injury.
        Metabolism. 2011; 60: 843-851
        • Thompson D.
        • Karpe F.
        • Lafontan M.
        • Frayn K.
        Physical activity and exercise in the regulation of human adipose tissue physiology.
        Physiol Rev. 2012; 92: 157-191
        • Donnelly J.E.
        • Blair S.N.
        • Jakicic J.M.
        • Manore M.M.
        • Rankin J.W.
        • Smith B.K.
        Appropriate physical activity intervention strategies for weight loss and prevention of weight regain for adults.
        Med Sci Sports Exerc. 2009; 41: 459-471
        • Warburton D.E.
        • McKenzie D.C.
        • Haykowsky M.J.
        • et al.
        Effectiveness of high-intensity interval training for the rehabilitation of patients with coronary artery disease.
        Am J Cardiol. 2005; 95: 1080-1084
        • Heydari M.
        • Freund J.
        • Boutcher S.H.
        The effect of high-intensity intermittent exercise on body composition of overweight young males.
        J Obes. 2012; 2012: 480467
        • Shepherd S.O.
        • Wilson O.J.
        • Taylor A.S.
        • et al.
        Low-volume high-intensity interval training in a gym setting improves cardio-metabolic and psychological health.
        PLoS One. 2015; 10: e0139056
        • Gillen J.B.
        • Percival M.E.
        • Ludzki A.
        • Tarnopolsky M.A.
        • Gibala M.J.
        Interval training in the fed or fasted state improves body composition and muscle oxidative capacity in overweight women.
        Obesity. 2013; 21: 2249-2255
        • Almenning I.
        • Rieber-Mohn A.
        • Lundgren K.M.
        • Shetelig Løvvik T.
        • Garnæs K.K.
        • Moholdt T.
        Effects of high intensity interval training and strength training on metabolic, cardiovascular and hormonal outcomes in women with polycystic ovary syndrome: a pilot study.
        PLoS One. 2015; 10: e0138793
        • Rognmo Ø.
        • Moholdt T.
        • Bakken H.
        • et al.
        Cardiovascular risk of high- versus moderate-intensity aerobic exercise in coronary heart disease patients.
        Circulation. 2012; 126: 1436-1440
        • Skelly L.E.
        • Andrews P.C.
        • Gillen J.B.
        • Martin B.J.
        • Percival M.E.
        • Gibala M.J.
        High-intensity interval exercise induces 24-h energy expenditure similar to traditional endurance exercise despite reduced time commitment.
        Appl Physiol Nutr Metab. 2014; 39: 845-848
        • Hazell T.J.
        • Olver T.D.
        • Hamilton C.D.
        • Lemon P.W.
        Two minutes of sprint-interval exercise elicits 24-hr oxygen consumption similar to that of 30 min of continuous endurance exercise.
        Int J Sport Nutr Exerc Metab. 2012; 22: 276-283
        • Whyte L.J.
        • Gill J.M.
        • Cathcart A.J.
        Effect of 2 weeks of sprint interval training on health-related outcomes in sedentary overweight/obese men.
        Metabolism. 2010; 59: 1421-1428
        • 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
        • Fisher G.
        • Brown A.W.
        • Bohan Brown M.M.
        • et al.
        High intensity interval- vs moderate intensity- training for improving cardiometabolic health in overweight or obese males: a randomized controlled trial.
        PLoS One. 2015; 10: e0138853
        • Kessler H.S.
        • Sisson S.B.
        • Short K.R.
        The potential for high-intensity interval training to reduce cardiometabolic disease risk.
        Sports Med. 2012; 42: 489-509
        • O'Donovan G.
        • Owen A.
        • Bird S.R.
        • et al.
        Changes in cardiorespiratory fitness and coronary heart disease risk factors following 24 wk of moderate- or high-intensity exercise of equal energy cost.
        J Appl Physiol. 2005; 98: 1619-1625
        • Austin M.A.
        • Hokanson J.E.
        • Edwards K.L.
        Hypertriglyceridemia as a cardiovascular risk factor.
        Am J Cardiol. 1998; 81: 7B-12B
        • Sarwar N.
        • Danesh J.
        • Eiriksdottir G.
        • et al.
        Triglycerides and the risk of coronary heart disease: 10,158 incident cases among 262,525 participants in 29 Western prospective studies.
        Circulation. 2007; 115: 450-458
        • Nash M.S.
        • deGroot J.
        • Martinez-Arizala A.
        • Mendez A.J.
        Evidence for an exaggerated postprandial lipemia in chronic paraplegia.
        J Spinal Cord Med. 2005; 28: 320-325
        • Emmons R.R.
        • Cirnigliaro C.M.
        • Moyer J.M.
        • et al.
        Exaggerated postprandial triglyceride response identified in individuals with spinal cord injury with cardiac risk factors.
        Med Sci Sports Exerc. 2009; 41: 404-405
        • Zilversmit D.B.
        Atherogenesis: postprandial phenomenon.
        Circulation. 1979; 60: 473-485
        • Bansal S.
        • Buring J.E.
        • Rifai N.
        • Mora S.
        • Sacks F.M.
        • Ridker P.M.
        Fasting compared with nonfasting triglycerides and risk of cardiovascular events in women.
        JAMA. 2007; 298: 309-316
        • Cowan R.E.
        • Nash M.S.
        Cardiovascular disease, SCI and exercise: unique risks and focused countermeasures.
        Disabil Rehabil. 2010; 32: 2228-2236
        • Burns S.F.
        • Miyashita M.
        • Stensel D.J.
        High-intensity interval exercise and postprandial triacylglycerol.
        Sports Med. 2015; 45: 957-968
        • Haykowsky M.J.
        • Timmons M.P.
        • Kruger C.
        • McNeely M.
        • Taylor D.A.
        • Clark A.M.
        Meta-analysis of aerobic interval training on exercise capacity and systolic function in patients with heart failure and reduced ejection fractions.
        Am J Cardiol. 2013; 111: 1466-1469
        • Hollekim-Strand S.M.
        • Bjørgaas M.R.
        • Albrektsen G.
        • Tjønna A.E.
        • Wisløff U.
        • Ingul C.B.
        High-intensity interval exercise effectively improves cardiac function in patients with type 2 diabetes mellitus and diastolic dysfunction: a randomized controlled trial.
        J Am Coll Cardiol. 2014; 64: 1758-1760
        • Madssen E.
        • Moholdt T.
        • Videm V.
        • Wisløff U.
        • Hegbom K.
        • Wiseth R.
        Coronary atheroma regression and plaque characteristics assessed by grayscale and radiofrequency intravascular ultrasound after aerobic exercise.
        Am J Cardiol. 2014; 114: 1504-1511
        • Malmo V.
        • Nes B.M.
        • Amundsen B.H.
        • et al.
        Aerobic interval training reduces the burden of atrial fibrillation in the short term: a randomized trial.
        Circulation. 2016; 133: 466-473
        • Warms C.A.
        • Backus D.
        • Rajan S.
        • Bombardier C.H.
        • Schomer K.G.
        • Burns S.P.
        Adverse events in cardiovascular-related training programs in people with spinal cord injury: a systematic review.
        J Spinal Cord Med. 2014; 37: 672-692
        • Jacobs P.L.
        • Nash M.S.
        Exercise recommendations for individuals with spinal cord injury.
        Sports Med. 2004; 34: 727-751
        • Furlan J.C.
        • Fehlings M.G.
        Cardiovascular complications after acute spinal cord injury: pathophysiology, diagnosis, and management.
        Neurosurg Focus. 2008; 25: E13
        • Steinberg L.L.
        • Lauro F.A.
        • Sposito M.M.
        • et al.
        Catecholamine response to exercise in individuals with different levels of paraplegia.
        Braz J Med Biol Res. 2000; 33: 913-918
        • Goosey-Tolfrey V.
        • Lenton J.
        • Goddard J.
        • Oldfield V.
        • Tolfrey K.
        • Eston R.
        Regulating intensity using perceived exertion in spinal cord-injured participants.
        Med Sci Sports Exerc. 2010; 42: 608-613
        • Cowan R.E.
        • Ginnity K.L.
        • Kressler J.
        • Nash M.S.
        • Nash M.S.
        Assessment of the talk test and rating of perceived exertion for exercise intensity prescription in persons with paraplegia.
        Top Spinal Cord Inj Rehabil. 2012; 18: 212-219
        • Sandler C.X.
        • Lloyd A.R.
        • Barry B.K.
        Fatigue exacerbation by interval or continuous exercise in chronic fatigue syndrome.
        Med Sci Sports Exerc. 2016; 48: 1875-1885
        • Petrofsky J.S.
        Thermoregulatory stress during rest and exercise in heat in patients with a spinal-cord injury.
        Eur J Appl Physiol Occup Physiol. 1992; 64: 503-507
        • Price M.J.
        • Campbell I.G.
        Effects of spinal cord lesion level upon thermoregulation during exercise in the heat.
        Med Sci Sports Exerc. 2003; 35: 1100-1107
        • Griggs K.E.
        • Price M.J.
        • Goosey-Tolfrey V.L.
        Cooling athletes with a spinal cord injury.
        Sports Med. 2015; 45: 9-21
        • Dyson-Hudson T.A.
        • Kirshblum S.C.
        Shoulder pain in chronic spinal cord injury, part I: epidemiology, etiology, and pathomechanics.
        J Spinal Cord Med. 2004; 27: 4-17
        • Samuelsson K.A.
        • Tropp H.
        • Gerdle B.
        Shoulder pain and its consequences in paraplegic spinal cord-injured, wheelchair users.
        Spinal Cord. 2004; 42: 41-46
        • Cratsenberg K.A.
        • Deitrick C.E.
        • Harrington T.K.
        • et al.
        Effectiveness of exercise programs for management of shoulder pain in manual wheelchair users with spinal cord injury.
        J Neurol Phys Ther. 2015; 39: 197-203
        • Jung M.E.
        • Bourne J.E.
        • Beauchamp M.R.
        • Robinson E.
        • Little J.P.
        High-intensity interval training as an efficacious alternative to moderate-intensity continuous training for adults with prediabetes.
        J Diabetes Res. 2015; 2015: 9
        • Lunt H.
        • Draper N.
        • Marshall H.C.
        • et al.
        High intensity interval training in a real world setting: a randomized controlled feasibility study in overweight inactive adults, measuring change in maximal oxygen uptake.
        PLoS One. 2014; 9: e83256
        • Saanijoki T.
        • Nummenmaa L.
        • Eskelinen J.J.
        • et al.
        Affective responses to repeated sessions of high-intensity interval training.
        Med Sci Sports Exerc. 2015; 47: 2604-2611
        • Jung M.E.
        • Bourne J.E.
        • Little J.P.
        Where does HIT fit? An examination of the affective response to high-intensity intervals in comparison to continuous moderate- and continuous vigorous-intensity exercise in the exercise intensity-affect continuum.
        PLoS One. 2014; 9: e114541
        • Astorino T.A.
        • Thum J.S.
        Interval training elicits higher enjoyment versus moderate exercise in persons with spinal cord injury.
        J Spinal Cord Med. 2016 Nov 3; ([Epub ahead of print])
      4. Hasnan N, Engkasan JP, Husain R, Davis GM. High-intensity virtual-reality arm plus FES-leg interval training in individuals with spinal cord injury. Biomed Tech (Berlin). 2013 Sep 7. [Epub ahead of print].