Original research| Volume 101, ISSUE 1, P121-129, January 2020

Download started.


Differences in Acute Metabolic Responses to Bionic and Nonbionic Ambulation in Spinal Cord Injured Humans and Controls

Published:August 26, 2019DOI:



      To (1) compare energy expenditure during seated rest, standing, and prolonged bionic ambulation or bipedal ambulation in participants with spinal cord injury (SCI) and noninjured controls, respectively, and (2) test effects on postbionic ambulation glycemia in SCI.


      Two independent group comparison of SCI and controls.


      Academic Medical Center.


      Ten participants with chronic SCI (C7-T1, American Spinal Injury Association Impairment Scale A-C) and 10 controls (N=20).


      A commercial bionic exoskeleton.

      Main Outcome Measures

      Absolute and relative (to peak) oxygen consumption, perceived exertion, carbohydrate/fat oxidation, energy expenditure, and postbionic ambulation plasma glucose/insulin.


      Average work intensity accompanying 45 minutes of outdoor bionic ambulation was <40% peak oxygen consumption, with negligible drift after reaching steady state. Rating of perceived exertion (RPE) did not differ between groups and reflected low exertion. Absolute energy costs for bionic ambulation and nonbionic ambulation were not different between groups despite a 565% higher ambulation velocity in controls and 3.3× higher kilocalorie per meter in SCI. Fuel partitioning was similar between groups and the same within groups for carbohydrate and fat oxidation. Nonsignificant (9%) lowering of the area under a glucose tolerance curve following bionic ambulation required 20% less insulin than at rest.


      Work intensity during prolonged bionic ambulation for this bionic exoskeleton is below a threshold for cardiorespiratory conditioning but above seated rest and passive standing. Bionic ambulation metabolism is consistent with low RPE and unchanged fuel partitioning from seated rest. Bionic ambulation did not promote beneficial effects on glycemia in well-conditioned, euglycemic participants. These findings may differ in less fit individuals with SCI or those with impaired glucose tolerance. Observed trends favoring this benefit suggest they are worthy of testing.


      List of abbreviations:

      ACSM (American College of Sports Medicine), AUC (area under the curve), CHO (carbohydrate), EE (energy expenditure), HOMA2-IR (Homeostatic Model-2 Assessment of Insulin Resistance), OGTT (oral glucose tolerance test), RER (respiratory exchange ratio), RPE (rating of perceived exertion), SCI (spinal cord injury), TEE (total energy expenditure)
      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'


      Subscribe to Archives of Physical Medicine and Rehabilitation
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect


        • Oja P.
        • Kelly P.
        • Murtagh E.M.
        • Murphy M.H.
        • Foster C.
        • Titze S.
        Effects of frequency, intensity, duration and volume of walking interventions on CVD risk factors: a systematic review and meta-regression analysis of randomised controlled trials among inactive healthy adults.
        Br J Sports Med. 2018; 52: 769-775
        • Knowler W.C.
        • Barrett-Connor E.
        • Fowler S.E.
        • et al.
        Reduction in the incidence of type 2 diabetes with lifestyle intervention or metformin.
        N Engl J Med. 2002; 346: 393-403
        • Hanson S.
        • Jones A.
        Is there evidence that walking groups have health benefits? A systematic review and meta-analysis.
        Br J Sports Med. 2015; 49: 710-715
        • Murtagh E.M.
        • Nichols L.
        • Mohammed M.A.
        • Holder R.
        • Nevill A.M.
        • Murphy M.H.
        The effect of walking on risk factors for cardiovascular disease: an updated systematic review and meta-analysis of randomised control trials.
        Prev Med. 2015; 72: 34-43
        • Maher J.L.
        • McMillan D.W.
        • Nash M.S.
        Exercise and health-related risks of physical deconditioning after spinal cord injury.
        Top Spinal Cord Inj Rehabil. 2017; 23: 175-187
        • Rimmer J.H.
        • Schiller W.
        • Chen M.D.
        Effects of disability-associated low energy expenditure deconditioning syndrome.
        Exerc Sport Sci Rev. 2012; 40: 22-29
        • Palermo A.E.
        • Maher J.L.
        • Baunsgaard C.B.
        • Nash M.S.
        Clinician-focused overview of bionic exoskeleton use after spinal cord injury.
        Top Spinal Cord Inj Rehabil. 2017; 23: 234-244
        • Kressler J.
        • Thomas C.K.
        • Field-Fote E.C.
        • et al.
        Understanding therapeutic benefits of overground bionic ambulation: exploratory case series in persons with chronic, complete spinal cord injury.
        Arch Phys Med Rehabil. 2014; 95: 1878-1887
        • Riebe D.
        • Ehrman J.K.
        • Liguori G.
        • Magal M.
        • American College of Sports Medicine
        ACSM's guidelines for exercise testing and prescription.
        10th ed. Wolters Kluwer Health, Philadelphia2018
        • Borg G.A.
        Psychophysical bases of perceived exertion.
        Med sci sports exerc. 1982; 14: 377-381
        • Asselin P.
        • Knezevic S.
        • Kornfeld S.
        • et al.
        Heart rate and oxygen demand of powered exoskeleton-assisted walking in persons with paraplegia.
        J Rehabil R D. 2015; 52: 147-158
        • Escalona M.J.
        • Brosseau R.
        • Vermette M.
        • et al.
        Cardiorespiratory demand and rate of perceived exertion during overground walking with a robotic exoskeleton in long-term manual wheelchair users with chronic spinal cord injury: a cross-sectional study.
        Ann Phys Rehabil Med. 2018; 61: 215-223
        • Evans N.
        • Hartigan C.
        • Kandilakis C.
        • Pharo E.
        • Clesson I.
        Acute cardiorespiratory and metabolic responses during exoskeleton-assisted walking overground among persons with chronic spinal cord injury.
        Top Spinal Cord Inj Rehabil. 2015; 21: 122-132
        • Kressler J.
        • Wymer T.
        • Domingo A.
        Respiratory, cardiovascular and metabolic responses during different modes of overground bionic ambulation in persons with motor-incomplete spinal cord injury: a case series.
        J Rehabil Med. 2018; 50: 173-180
        • Clinical Practice Guidelines: Spinal Cord Medicine
        Identification and management of cardiometabolic risk after spinal cord injury 2018.
        (Available at:) (Accessed April 6, 2018)
        • Strausser K.A.
        • Swift T.A.
        • Zoss A.B.
        • Kazerooni H.
        • Bennett B.C.
        Mobile exoskeleton for spinal cord injury: development and testing.
        in: Proceedings of the American Society of Mechanical Engineers; 2011 Oct 31-Nov 2. Virgina, Arlington2011: 419-425
        • Strausser K.A.
        • Kazerooni H.
        The development and testing of a human machine interface for mobile medical exoskeleton.
        in: 2011 IEEE/RSJ International Conference of Intelligent Robots and Systems; 2011 Sep 25-30. San Francisco, California, 2011: 4911-4916
        • Maher J.L.
        • Cowan R.E.
        Comparison of 1- versus 3-minute stage duration during arm ergometry in individuals with spinal cord injury.
        Arch phys med rehabil. 2016; 97: 1895-1900
        • Wallace T.M.
        • Levy J.C.
        • Matthews D.R.
        Use and abuse of HOMA modeling.
        Diabetes Care. 2004; 27: 1487-1495
        • Jacobs K.A.
        • Casazza G.A.
        • Suh S.H.
        • Horning M.A.
        • Brooks G.A.
        Fatty acid reesterification but not oxidation is increased by oral contraceptive use in women.
        J Appl Physiol. 2005; 98: 1720-1731
        • Womack C.J.
        • Sieminski D.J.
        • Katzel L.I.
        • Yataco A.
        • Gardner A.W.
        Oxygen uptake during constant-intensity exercise in patients with peripheral arterial occlusive disease.
        Vasc Med. 1997; 2: 174-178
        • Simmons O.L.
        • Kressler J.
        • Nash M.S.
        Reference fitness values in the untrained spinal cord injury population.
        Arch Phys Med Rehabil. 2014; 95: 2272-2278
        • Esquenazi A.
        • Talaty M.
        • Packel A.
        • Saulino M.
        The ReWalk powered exoskeleton to restore ambulatory function to individuals with thoracic-level motor-complete spinal cord injury.
        Am J Phys Med Rehabil. 2012; 91: 911-921
        • 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
        • Jacobs P.L.
        • Johnson B.
        • Mahoney E.T.
        Physiologic responses to electrically assisted and frame-supported standing in persons with paraplegia.
        J Spinal Cord Med. 2003; 26: 384-389
        • 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
        • Heath G.W.
        • Gavin 3rd, J.R.
        • Hinderliter J.M.
        • Hagberg J.M.
        • Bloomfield S.A.
        • Holloszy J.O.
        Effects of exercise and lack of exercise on glucose tolerance and insulin sensitivity.
        J Appl Physiol Respir Environ Exerc Physiol. 1983; 55: 512-517
        • Richter E.A.
        • Mikines K.J.
        • Galbo H.
        • Kiens B.
        Effect of exercise on insulin action in human skeletal muscle.
        J Appl Physiol. 1989; 66: 876-885
        • Devlin J.T.
        • Horton E.S.
        Effects of prior high-intensity exercise on glucose metabolism in normal and insulin-resistant men.
        Diabetes. 1985; 34: 973-979
        • Numao S.
        • Kawano H.
        • Endo N.
        • et al.
        Effects of a single bout of aerobic exercise on short-term low-carbohydrate/high-fat intake-induced postprandial glucose metabolism during an oral glucose tolerance test.
        Metabolism. 2013; 62: 1406-1415
        • Bird S.R.
        • Hawley J.A.
        Update on the effects of physical activity on insulin sensitivity in humans.
        BMJ Open Sport Exerc Med. 2016; 2e000143
        • Hayashi Y.
        • Nagasaka S.
        • Takahashi N.
        • et al.
        A single bout of exercise at higher intensity enhances glucose effectiveness in sedentary men.
        J clin endocrinol metab. 2005; 90: 4035-4040
        • 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