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Exercise Training Does Not Attenuate Cardiac Atrophy or Loss of Function in Individuals With Acute Spinal Cord Injury: A Pilot Study

Published:December 23, 2022DOI:https://doi.org/10.1016/j.apmr.2022.12.001

      Abstract

      Objective

      To investigate the effects of 2 modes of exercise training, upper-body alone, and the addition of electrical stimulation of the lower body, to attenuate cardiac atrophy and loss of function in individuals with acute spinal cord injury (SCI).

      Design

      Randomized controlled trial.

      Setting

      Rehabilitation Hospital.

      Participants

      Volunteers (N=27; 5 women, 22 men) who were <24 months post SCI.

      Interventions

      Volunteers completed either 6 months of no structured exercise (Control), arm rowing (AO), or a combination of arm rowing with electrical stimulation of lower body paralyzed muscle (functional electrical stimulation [FES] rowing).

      Main Outcome Measures

      Transthoracic echocardiography was performed on each subject prior to and 6 months after the intervention. The relations between time since injury and exercise type to cardiac structure and function were assessed via 2-way repeated-measures analysis of variance and with multilevel linear regression.

      Results

      Time since injury was significantly associated with a continuous decline in cardiac structure and systolic function, specifically, a reduction in left ventricular mass (0.197 g/month; P=.049), internal diameter during systole (0.255 mm/month; P<.001), and diastole (0.217 mm/month; P=.019), as well as cardiac output (0.048 L/month, P=.019), and left ventricular percent shortening (0.256 %/month; P=.027). These associations were not differentially affected by exercise (Control vs AO vs FES, P>.05).

      Conclusions

      These results indicate that within the subacute phase of recovery from SCI there is a linear loss of left ventricular cardiac structure and systolic function that is not attenuated by current rehabilitative aerobic exercise practices. Reductions in cardiac structure and function may increase the risk of cardiovascular disease in individuals with SCI and warrants further interventions to prevent cardiac decline.

      Keywords

      List of abbreviations:

      AO (arms only), A′S (septal wall contraction velocity during late diastole), E′S (septal wall contraction velocity during early diastole), FES (functional electrical stimulation), HR (heart rate), LV (left ventricle), LVEDV (volume of the left ventricle during diastole), LVESV (volume of the left ventricle during systole), LVIDd (internal diameter of the left ventricle during diastole), LVIDs (internal diameter of the left ventricle during systole), LVM (left ventricle mass), LVOTd (left ventricle outflow track diameter), PWT (posterior wall thickness), SCI (spinal cord injury), SV (stroke volume), TSI (time since injury), V̇o2peak (peak volume of oxygen consumed)
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      References

        • Krassioukov A.
        Autonomic function following cervical spinal cord injury.
        Respir Physiol Neurobiol. 2009; 169: 157-164
        • Lujan HL
        • Janbaih H
        • DiCarlo SE.
        Structural remodeling of the heart and its premotor cardioinhibitory vagal neurons following T 5 spinal cord transection.
        J Appl Physiol. 2014; 116: 1148-1155
        • Ely MR
        • Singh TK
        • Baggish AL
        • Taylor JA.
        Reductions in cardiac structure and function 24 months after spinal cord injury: a cross-sectional study.
        Arch Phys Med Rehabil. 2021; 102: 1490-1498
        • Balthazaar SJT
        • Nightingale TE
        • Currie KD
        • et al.
        Temporal changes of cardiac structure, function, and mechanics during sub-acute cervical and thoracolumbar spinal cord injury in humans: a case-series.
        Front Cardiovasc Med. 2022; 0: 1542
        • Benjamin EJ
        • D'Agostino RB
        • Belanger AJ
        • Wolf PA
        • Levy D
        Left atrial size and the risk of stroke and death.
        Circulation. 1995; 92: 835-841
        • Bikkina M
        • Levy D
        • Evans JC
        • et al.
        Left ventricular mass and risk of stroke in an elderly cohort: the Framingham Heart Study.
        JAMA. 1994; 272: 33-36
        • Levy D
        • Garrison RJ
        • Savage DD
        • Kannel WB
        • Castelli WP.
        Prognostic implications of echocardiographically determined left ventricular mass in the Framingham Heart Study.
        J Am Med. 2004; 292: 2350-2356
        • Eguchi K
        • Ishikawa J
        • Hoshide S
        • et al.
        Differential impact of left ventricular mass and relative wall thickness on cardiovascular prognosis in diabetic and nondiabetic hypertensive subjects.
        Am Heart J. 2007; 154 (79.e9-e15)
        • Devereux RB
        • Wachtell K
        • Gerdts E
        • et al.
        Prognostic significance of left ventricular mass change during treatment of hypertension.
        J Am Med Assoc. 2004; 292: 2350-2356
        • Gidding SS
        • Carnethon MR
        • Daniels S
        • et al.
        Low cardiovascular risk is associated with favorable left ventricular mass, left ventricular relative wall thickness, and left atrial size: the CARDIA study.
        J Am Soc Echocardiogr. 2010; 23: 816-822
        • Pelliccia A
        • Maron BJ
        • Di Paolo FM
        • et al.
        Prevalence and clinical significance of left atrial remodeling in competitive athletes.
        J Am Coll Cardiol. 2005; 46: 690-696
        • Mahjoub H
        • Le Blanc OL
        • Paquette M
        • et al.
        Cardiac remodeling after six weeks of high-intensity interval training to exhaustion in endurance-trained men.
        Am J Physiol Heart Circ Physiol. 2019; 317: H685-H694
        • Baggish AL
        • Wang F
        • Weiner RB
        • et al.
        Training-specific changes in cardiac structure and function: a prospective and longitudinal assessment of competitive athletes.
        J Appl Physiol. 2008; 104: 1121-1128
        • Qiu S
        • Taylor JA.
        Hybrid functional electrical stimulation exercise for improved cardiorespiratory fitness in SCI. Taylor JA (ed.).
        The physiology of exercise in spinal cord injury. Springer, US2016: 269-286
        • Price DT
        • Davidoff R
        • Balady GJ.
        Comparison of cardiovascular adaptations to long-term arm and leg exercise in wheelchair athletes versus long-distance runners.
        Am J Cardiol. 2000; 85: 996-1001
        • Davis GM
        • Shephard RJ
        • Leenen FHH.
        Cardiac effects of short term arm crank training in paraplegics: echocardiographic evidence.
        Eur J Appl Physiol Occup Physiol. 1987; 56: 90-96
        • Huonker M
        • Schmidt A
        • Sorichter S
        • Schmidt-Trucksab A
        • Mrisek P
        • Keul J.
        Cardiovascular differences between sedentary and wheelchair-trained subjects with paraplegia.
        Med Sci Sports Exerc. 1998; 30: 609-613
        • Shaffer RF
        • Picard G
        • Taylor JA.
        Relationship of spinal cord injury level and duration to peak aerobic capacity with arms-only and hybrid functional electrical stimulation rowing.
        Am J Phys Med Rehabil. 2018; 97: 488-491
        • Sawka MN
        • Glaser RM
        • Wilde SW
        • Von Luhrte TC.
        Metabolic and circulatory responses to wheelchair and arm crank exercise.
        J Appl Physiol Respir Environ Exerc Physiol. 1980; 49: 784-788
        • Jacobs P
        • Nash M
        • Rusinowski JW.
        Circuit training provides cardiorespiratory and strength benefits in persons with paraplegia.
        Med Sci Sports Exerc. 2001; 33: 711-717
        • Ely MR
        • Taylor JA.
        The practical utility of functional electrical stimulation exercise for cardiovascular health in individuals with spinal cord injury.
        Curr Phys Med Rehabil Reports. 2021; 9: 154-162
        • Hettinga DM
        • Andrews BJ.
        Oxygen consumption during functional electrical stimulation-assisted exercise in persons with spinal cord injury: implications for fitness and health.
        Sport Med. 2008; 38: 825-838
        • Nash MS
        • Bilsker MS
        • Kearney HM
        • Ramirez JN
        • Applegate B
        • Green BA.
        Effects of electrically-stimulated exercise and passive motion on echocardiographically-derived wall motion and cardiodynamic function in tetraplegic persons.
        Paraplegia. 1995; 33: 80-89
        • Mutton DL
        • Scremin AME
        • Barstow TJ
        • Scott MD
        • Kunkel CF
        • Cagle TG.
        Physiologic responses during functional electrical stimulation leg cycling and hybrid exercise in spinal cord injured subjects.
        Arch Phys Med Rehabil. 1997; 78: 712-718
        • Laskin JJ
        • Ashley EA
        • Olenik LM
        • et al.
        Electrical stimulation-assisted rowing exercise in spinal cord injured people. A pilot study.
        Paraplegia. 1993; 31: 534-541
        • Taylor JA
        • Picard G
        • Widrick JJ.
        Aerobic capacity with hybrid FES rowing in spinal cord injury: comparison with arms-only exercise and preliminary findings with regular training.
        PMR. 2011; 3: 817-824
        • Ely MR
        • Ely BR
        • Solinsky RJ
        • Taylor JA.
        Methods to enhance the beneficial effects of exercise in individuals with spinal cord injuries.
        in: Greising SM Call JA Regenerative rehabilitation. Physiology in health and disease. Springer, Cham2022: 387-407
        • Mitchell C
        • Rahko PS
        • Blauwet LA
        • et al.
        Guidelines for performing a comprehensive transthoracic echocardiographic examination in adults: recommendations from the American Society of Echocardiography.
        J Am Soc Echocardiogr. 2019; 32: 1-64
        • Utomi V
        • Oxborough D
        • Whyte GP
        • et al.
        Systematic review and meta-analysis of training mode, imaging modality and body size influences on the morphology and function of the male athlete's heart.
        Heart. 2013; 99: 1727-1733
        • Lang RM
        • Badano LP
        • Mor-Avi V
        • et al.
        Recommendations for cardiac chamber quantification by echocardiography in adults: an update from the American Society of Echocardiography and the European Association of Cardiovascular Imaging.
        Eur Heart J Cardiovasc Imaging. 2015; 16: 233-271
        • Du Bois D
        • Du Bois EF
        Clinical calorimetry: tenth paper a formula to estimate the approximate surface area if height and weight be known.
        Arch Intern Med. 1916; XVII: 863-871
        • Hastings JL
        • Krainski F
        • Snell PG
        • et al.
        Effect of rowing ergometry and oral volume loading on cardiovascular structure and function during bed rest.
        J Appl Physiol. 2012; 112: 1735-1743
        • Kou S
        • Caballero L
        • Dulgheru R
        • et al.
        Echocardiographic reference ranges for normal cardiac chamber size: results from the NORRE study.
        Eur Heart J Cardiovasc Imaging. 2014; 15: 680-690
        • Williams AM
        • Gee CM
        • Voss C
        • West CR.
        Cardiac consequences of spinal cord injury: systematic review and meta-analysis.
        Heart. 2019; 105: 217-225
        • West CR
        • Campbell IG
        • Shave RE
        • Romer LM.
        Resting cardiopulmonary function in paralympic athletes with cervical spinal cord injury.
        Med Sci Sports Exerc. 2012; 44: 323-329
        • Driussi C
        • Ius A
        • Bizzarini E
        • et al.
        Structural and functional left ventricular impairment in subjects with chronic spinal cord injury and no overt cardiovascular disease.
        J Spinal Cord Med. 2014; 37: 85-92
        • de Groot PC
        • van Dijk A
        • Dijk E
        • Hopman MT.
        Preserved cardiac function after chronic spinal cord injury.
        Arch Phys Med Rehabil. 2006; 87: 1195-1200
        • Matos-Souza JR
        • Pithon KR
        • Oliveira RTD
        • et al.
        Altered left ventricular diastolic function in subjects with spinal cord injury.
        Spinal Cord. 2011; 49: 65-69
        • Squair JW
        • Deveau KM
        • Harman KA
        • et al.
        Spinal cord injury causes systolic dysfunction and cardiomyocyte atrophy.
        J Neurotrauma. 2018; 35: 424-434
        • Wilson MG
        • Ellison GM
        • Cable NT.
        Basic science behind the cardiovascular benefits of exercise.
        Br J Sports Med. 2016; 50: 93-99
        • Perhonen MA
        • Franco F
        • Lane LD
        • et al.
        Cardiac atrophy after bed rest and spaceflight.
        J Appl Physiol. 2001; 91: 645-653
        • West CR
        • Crawford MA
        • Poormasjedi-Meibod MS
        • et al.
        Passive hind-limb cycling improves cardiac function and reduces cardiovascular disease risk in experimental spinal cord injury.
        J Physiol. 2014; 592: 1771-1783
        • Nash MS
        • Bilsker S
        • Marciuo AE
        • et al.
        Reversal of adaptive left ventricular atrophy following electrically-stimulated exercise training in human tetraplegics.
        Paraplegia. 1991; 29: 590-599
        • Maggioni MA
        • Ferratini M
        • Pezzano A
        • et al.
        Heart adaptations to long-term aerobic training in paraplegic subjects: an echocardiographic study.
        Spinal Cord. 2012; 50: 538-542
        • Williams AM
        • Ma JK
        • Martin Ginis KA
        • West CR
        Effects of a tailored physical activity intervention on cardiovascular structure and function in individuals with spinal cord injury.
        Neurorehabil Neural Repair. 2021; 35: 692-703
        • Gates PE
        • Campbell IG
        • George KP.
        Absence of training-specific cardiac adaptation in paraplegic athletes.
        Med Sci Sports Exerc. 2002; 34: 1699-1704
        • Mercier HW
        • Picard G
        • Taylor JA
        • Vivodtzev I.
        Gains in aerobic capacity with whole-body functional electrical stimulation row training and generalization to arms-only exercise after spinal cord injury.
        Spinal Cord. 2021; 59: 74-81
        • Phillips WT
        • Kiratli BJ
        • Sarkarati M
        • et al.
        Effect of spinal cord injury on the heart and cardiovascular fitness.
        Curr Probl Cardiol. 1998; 23: 641-716
        • Myers J
        • Lee M
        • Kiratli J.
        Cardiovascular disease in spinal cord injury.
        Am J Phys Med Rehabil. 2007; 86: 142-152
        • Currie KD
        • Coates AM
        • Slysz JT
        • et al.
        Left ventricular structure and function in elite swimmers and runners.
        Front Physiol. 2018; 9: 1-6
        • 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
        • Shibata S
        • Perhonen M
        • Levine BD.
        Supine cycling plus volume loading prevent cardiovascular deconditioning during bed rest.
        J Appl Physiol. 2010; 108: 1177-1186