Skip to main content
Top
Published in: Sports Medicine 6/2015

01-06-2015 | Systematic Review

Aerobic Capacity in Persons with Multiple Sclerosis: A Systematic Review and Meta-Analysis

Authors: Martin Langeskov-Christensen, Martin Heine, Gert Kwakkel, Ulrik Dalgas

Published in: Sports Medicine | Issue 6/2015

Login to get access

Abstract

Background

Aerobic capacity (VO2max) is a strong health and performance predictor and is regarded as a key physiological measure in the healthy population and in persons with multiple sclerosis (PwMS). However, no studies have tried to synthesize the existing knowledge regarding VO2max in PwMS.

Objectives

The objectives of this study were to (1) systematically review the psychometric properties of the VO2max test; (2) systematically review the literature on VO2max compared with healthy populations; (3) summarize correlates of VO2max; and (4) to review and conduct a meta-analysis of longitudinal exercise studies evaluating training-induced effects on VO2max in PwMS.

Data Sources and Study Selection

A systematic literature search of six databases (PubMed, EMBASE, Cochrane Library, PEDro, CINAHL and SPORTDiscus) was performed. To be included, the study had to (1) enrol participants with definite MS according to defined criteria; (2) assess aerobic capacity (VO2max) by means of a graded exercise test to voluntary exhaustion; (3) had undergone peer review; and (4) be available in English, Danish or Dutch.

Study Appraisal and Synthesis Methods

The psychometric properties of the VO2max test in PwMS were reviewed with respect to reliability, validity and responsiveness. Simple Pearson correlation analysis was used to assess the relation between key study characteristics and the reported mean VO2max. The methodological quality of the intervention studies was evaluated using the original 11-item Physiotherapy Evidence Database (PEDro) scale. A random coefficient model was used to summarize individual, weighted, standardized effects of studies that assessed the effects of exercise on aerobic capacity in PwMS.

Results

A total of 40 studies, covering 165 healthy controls and 1,137 PwMS, fulfilled the inclusion criteria. VO2max testing in PwMS can be considered a valid measure of aerobic capacity, at least in PwMS having low-to-mild disability, and an ∼10 % change between two tests performed on separate days can be considered the smallest reliable change (with 95 % certainty) in VO2max in PwMS. The average body-weight-adjusted VO2max was significantly lower in PwMS (25.5 ± 5.2 mL·kg−1·min−1) compared with healthy controls (30.9 ± 5.4 mL·kg−1·min−1). The analysis of VO2max correlates revealed associations with a variety of outcomes covering all levels of the International Classification of Functioning, Disability and Health (ICF) model. The meta-analysis showed that aerobic training in PwMS may improve VO2max by as much as 3.5 mL·kg−1·min−1.

Conclusions

A valid and reliable test can be performed, in at least ambulant PwMS, by the gold standard whole-body maximal exercise test. Aerobic capacity in PwMS is impaired compared with healthy people, and is significantly associated with factors on all levels of the ICF model, including disease severity. Aerobic training can improve aerobic capacity in PwMS to a degree that is associated with secondary health benefits.
Literature
1.
go back to reference Koch-Henriksen N, Sorensen PS. The changing demographic pattern of multiple sclerosis epidemiology. Lancet Neurol. 2010;9(5):520–32.CrossRefPubMed Koch-Henriksen N, Sorensen PS. The changing demographic pattern of multiple sclerosis epidemiology. Lancet Neurol. 2010;9(5):520–32.CrossRefPubMed
3.
go back to reference Motl RW, Pilutti LA. The benefits of exercise training in multiple sclerosis. Nat Rev Neurol. 2012;8(9):487–97.CrossRefPubMed Motl RW, Pilutti LA. The benefits of exercise training in multiple sclerosis. Nat Rev Neurol. 2012;8(9):487–97.CrossRefPubMed
4.
go back to reference Confavreux C, Vukusic S. Natural history of multiple sclerosis: a unifying concept. Brain. 2006;129(Pt 3):606–16.CrossRefPubMed Confavreux C, Vukusic S. Natural history of multiple sclerosis: a unifying concept. Brain. 2006;129(Pt 3):606–16.CrossRefPubMed
5.
go back to reference Kurtzke JF. Rating neurologic impairment in multiple sclerosis: an Expanded Disability Status Scale (EDSS). Neurology. 1983;33(11):1444–52.CrossRefPubMed Kurtzke JF. Rating neurologic impairment in multiple sclerosis: an Expanded Disability Status Scale (EDSS). Neurology. 1983;33(11):1444–52.CrossRefPubMed
6.
go back to reference Marrie RA, Horwitz RI. Emerging effects of comorbidities on multiple sclerosis. Lancet Neurol. 2010;9(8):820–8.CrossRefPubMed Marrie RA, Horwitz RI. Emerging effects of comorbidities on multiple sclerosis. Lancet Neurol. 2010;9(8):820–8.CrossRefPubMed
7.
go back to reference Ehde DM, Bombardier CH. Depression in persons with multiple sclerosis. Phys Med Rehabil Clin N Am. 2005;16(2):437–48 (ix).CrossRefPubMed Ehde DM, Bombardier CH. Depression in persons with multiple sclerosis. Phys Med Rehabil Clin N Am. 2005;16(2):437–48 (ix).CrossRefPubMed
8.
go back to reference Fisk JD, Pontefract A, Ritvo PG, et al. The impact of fatigue on patients with multiple sclerosis. Can J Neurol Sci. 1994;21(1):9–14.PubMed Fisk JD, Pontefract A, Ritvo PG, et al. The impact of fatigue on patients with multiple sclerosis. Can J Neurol Sci. 1994;21(1):9–14.PubMed
9.
go back to reference Dalgas U, Ingemann-Hansen T, Stenager E. Physical exercise and MS: recommendations. Int MS J. 2009;16(1):5–11.PubMed Dalgas U, Ingemann-Hansen T, Stenager E. Physical exercise and MS: recommendations. Int MS J. 2009;16(1):5–11.PubMed
10.
go back to reference Wens I, Dalgas U, Stenager E, et al. Risk factors related to cardiovascular diseases and the metabolic syndrome in multiple sclerosis: a systematic review. Mult Scler. 2013;19(12):1556–64.CrossRefPubMed Wens I, Dalgas U, Stenager E, et al. Risk factors related to cardiovascular diseases and the metabolic syndrome in multiple sclerosis: a systematic review. Mult Scler. 2013;19(12):1556–64.CrossRefPubMed
11.
go back to reference Carnethon MR, Gulati M, Greenland P. Prevalence and cardiovascular disease correlates of low cardiorespiratory fitness in adolescents and adults. JAMA. 2005;294(23):2981–8.CrossRefPubMed Carnethon MR, Gulati M, Greenland P. Prevalence and cardiovascular disease correlates of low cardiorespiratory fitness in adolescents and adults. JAMA. 2005;294(23):2981–8.CrossRefPubMed
12.
go back to reference Eriksen L, Curtis T, Gronbaek M, et al. The association between physical activity, cardiorespiratory fitness and self-rated health. Prev Med. 2013;57(6):900–2.CrossRefPubMed Eriksen L, Curtis T, Gronbaek M, et al. The association between physical activity, cardiorespiratory fitness and self-rated health. Prev Med. 2013;57(6):900–2.CrossRefPubMed
13.
go back to reference Bassett DR Jr, Howley ET. Limiting factors for maximum oxygen uptake and determinants of endurance performance. Med Sci Sports Exerc. 2000;32(1):70–84.CrossRefPubMed Bassett DR Jr, Howley ET. Limiting factors for maximum oxygen uptake and determinants of endurance performance. Med Sci Sports Exerc. 2000;32(1):70–84.CrossRefPubMed
14.
go back to reference Marrie RA, Hanwell H. General health issues in multiple sclerosis: comorbidities, secondary conditions, and health behaviors. Continuum (Minneap Minn). 2013;19(4 Multiple Sclerosis):1046–57. Marrie RA, Hanwell H. General health issues in multiple sclerosis: comorbidities, secondary conditions, and health behaviors. Continuum (Minneap Minn). 2013;19(4 Multiple Sclerosis):1046–57.
15.
go back to reference Sandroff BM, Sosnoff JJ, Motl RW. Physical fitness, walking performance, and gait in multiple sclerosis. J Neurol Sci. 2013;328(1–2):70–6.CrossRefPubMed Sandroff BM, Sosnoff JJ, Motl RW. Physical fitness, walking performance, and gait in multiple sclerosis. J Neurol Sci. 2013;328(1–2):70–6.CrossRefPubMed
16.
go back to reference Sandroff BM, Motl RW. Fitness and cognitive processing speed in persons with multiple sclerosis: a cross-sectional investigation. J Clin Exp Neuropsychol. 2012;34(10):1041–52.CrossRefPubMed Sandroff BM, Motl RW. Fitness and cognitive processing speed in persons with multiple sclerosis: a cross-sectional investigation. J Clin Exp Neuropsychol. 2012;34(10):1041–52.CrossRefPubMed
17.
go back to reference Prakash RS, Snook EM, Erickson KI, et al. Cardiorespiratory fitness: a predictor of cortical plasticity in multiple sclerosis. Neuroimage. 2007;34(3):1238–44.CrossRefPubMed Prakash RS, Snook EM, Erickson KI, et al. Cardiorespiratory fitness: a predictor of cortical plasticity in multiple sclerosis. Neuroimage. 2007;34(3):1238–44.CrossRefPubMed
18.
go back to reference Prakash RS, Snook EM, Motl RW, et al. Aerobic fitness is associated with gray matter volume and white matter integrity in multiple sclerosis. Brain Res. 2010;1341:41–51.CrossRefPubMed Prakash RS, Snook EM, Motl RW, et al. Aerobic fitness is associated with gray matter volume and white matter integrity in multiple sclerosis. Brain Res. 2010;1341:41–51.CrossRefPubMed
19.
go back to reference Cress ME, Meyer M. Maximal voluntary and functional performance levels needed for independence in adults aged 65 to 97 years. Phys Ther. 2003;83(1):37–48.PubMed Cress ME, Meyer M. Maximal voluntary and functional performance levels needed for independence in adults aged 65 to 97 years. Phys Ther. 2003;83(1):37–48.PubMed
20.
21.
go back to reference Whipp B. The peak versus maximum oxygen uptake issue. CPX International Inc.; 2010. p. 1–9. Whipp B. The peak versus maximum oxygen uptake issue. CPX International Inc.; 2010. p. 1–9.
22.
go back to reference Langeskov-Christensen M, Langeskov-Christensen D, Overgaard K, et al. Validity and reliability of VO-max measurements in persons with multiple sclerosis. J Neurol Sci. 2014;342(1–2):79–87.CrossRefPubMed Langeskov-Christensen M, Langeskov-Christensen D, Overgaard K, et al. Validity and reliability of VO-max measurements in persons with multiple sclerosis. J Neurol Sci. 2014;342(1–2):79–87.CrossRefPubMed
23.
go back to reference Mokkink LB, Terwee CB, Patrick DL, et al. The COSMIN study reached international consensus on taxonomy, terminology, and definitions of measurement properties for health-related patient-reported outcomes. J Clin Epidemiol. 2010;63(7):737–45.CrossRefPubMed Mokkink LB, Terwee CB, Patrick DL, et al. The COSMIN study reached international consensus on taxonomy, terminology, and definitions of measurement properties for health-related patient-reported outcomes. J Clin Epidemiol. 2010;63(7):737–45.CrossRefPubMed
24.
go back to reference Waschbisch A, Wenny I, Tallner A, et al. Physical activity in multiple sclerosis: a comparative study of vitamin D, brain-derived neurotrophic factor and regulatory T cell populations. Eur Neurol. 2012;68(2):122–8.CrossRefPubMed Waschbisch A, Wenny I, Tallner A, et al. Physical activity in multiple sclerosis: a comparative study of vitamin D, brain-derived neurotrophic factor and regulatory T cell populations. Eur Neurol. 2012;68(2):122–8.CrossRefPubMed
25.
go back to reference Motl RW, Goldman M. Physical inactivity, neurological disability, and cardiorespiratory fitness in multiple sclerosis. Acta Neurol Scand. 2011;123(2):98–104.CrossRefPubMedCentralPubMed Motl RW, Goldman M. Physical inactivity, neurological disability, and cardiorespiratory fitness in multiple sclerosis. Acta Neurol Scand. 2011;123(2):98–104.CrossRefPubMedCentralPubMed
26.
go back to reference Bouchard C, An P, Rice T, et al. Familial aggregation of VO(2max) response to exercise training: results from the HERITAGE family study. J Appl Physiol (1985). 1999;87(3):1003–8. Bouchard C, An P, Rice T, et al. Familial aggregation of VO(2max) response to exercise training: results from the HERITAGE family study. J Appl Physiol (1985). 1999;87(3):1003–8.
27.
go back to reference Dalgas U, Stenager E, Ingemann-Hansen T. Multiple sclerosis and physical exercise: recommendations for the application of resistance-, endurance- and combined training. Mult Scler. 2008;14(1):35–53.CrossRefPubMed Dalgas U, Stenager E, Ingemann-Hansen T. Multiple sclerosis and physical exercise: recommendations for the application of resistance-, endurance- and combined training. Mult Scler. 2008;14(1):35–53.CrossRefPubMed
28.
go back to reference Petajan JH, White AT. Recommendations for physical activity in patients with multiple sclerosis. Sports Med. 1999;27(3):179–91.CrossRefPubMed Petajan JH, White AT. Recommendations for physical activity in patients with multiple sclerosis. Sports Med. 1999;27(3):179–91.CrossRefPubMed
29.
go back to reference Latimer-Cheung AE, Pilutti LA, Hicks AL, et al. Effects of exercise training on fitness, mobility, fatigue, and health-related quality of life among adults with multiple sclerosis: a systematic review to inform guideline development. Arch Phys Med Rehabil. 2013;94(9):1800–28.CrossRefPubMed Latimer-Cheung AE, Pilutti LA, Hicks AL, et al. Effects of exercise training on fitness, mobility, fatigue, and health-related quality of life among adults with multiple sclerosis: a systematic review to inform guideline development. Arch Phys Med Rehabil. 2013;94(9):1800–28.CrossRefPubMed
30.
go back to reference Liberati A, Altman DG, 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.CrossRefPubMedCentralPubMed Liberati A, Altman DG, 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.CrossRefPubMedCentralPubMed
31.
go back to reference Polman CH, Reingold SC, Banwell B, et al. Diagnostic criteria for multiple sclerosis: 2010 revisions to the McDonald criteria. Ann Neurol. 2011;69(2):292–302.CrossRefPubMedCentralPubMed Polman CH, Reingold SC, Banwell B, et al. Diagnostic criteria for multiple sclerosis: 2010 revisions to the McDonald criteria. Ann Neurol. 2011;69(2):292–302.CrossRefPubMedCentralPubMed
32.
go back to reference Howley ET, Bassett DR Jr, Welch HG. Criteria for maximal oxygen uptake: review and commentary. Med Sci Sports Exerc. 1995;27(9):1292–301.CrossRefPubMed Howley ET, Bassett DR Jr, Welch HG. Criteria for maximal oxygen uptake: review and commentary. Med Sci Sports Exerc. 1995;27(9):1292–301.CrossRefPubMed
33.
go back to reference Duncan GE, Howley ET, Johnson BN. Applicability of VO2max criteria: discontinuous versus continuous protocols. Med Sci Sports Exerc. 1997;29(2):273–8.CrossRefPubMed Duncan GE, Howley ET, Johnson BN. Applicability of VO2max criteria: discontinuous versus continuous protocols. Med Sci Sports Exerc. 1997;29(2):273–8.CrossRefPubMed
34.
go back to reference Midgley AW, McNaughton LR, Polman R, et al. Criteria for determination of maximal oxygen uptake: a brief critique and recommendations for future research. Sports Med. 2007;37(12):1019–28.CrossRefPubMed Midgley AW, McNaughton LR, Polman R, et al. Criteria for determination of maximal oxygen uptake: a brief critique and recommendations for future research. Sports Med. 2007;37(12):1019–28.CrossRefPubMed
35.
go back to reference Maher CG, Sherrington C, Herbert RD, et al. Reliability of the PEDro scale for rating quality of randomized controlled trials. Phys Ther. 2003;83(8):713–21.PubMed Maher CG, Sherrington C, Herbert RD, et al. Reliability of the PEDro scale for rating quality of randomized controlled trials. Phys Ther. 2003;83(8):713–21.PubMed
36.
go back to reference Herbert R, Moseley A, Sherrington C. PEDro: a database of randomised controlled trials in physiotherapy. Health Inf Manag. 1998;28(4):186–8.PubMed Herbert R, Moseley A, Sherrington C. PEDro: a database of randomised controlled trials in physiotherapy. Health Inf Manag. 1998;28(4):186–8.PubMed
37.
go back to reference Caspersen CJ, Powell KE, Christenson GM. Physical activity, exercise, and physical fitness: definitions and distinctions for health-related research. Public Health Rep. 1985;100(2):126–31.PubMedCentralPubMed Caspersen CJ, Powell KE, Christenson GM. Physical activity, exercise, and physical fitness: definitions and distinctions for health-related research. Public Health Rep. 1985;100(2):126–31.PubMedCentralPubMed
38.
go back to reference Stroup DF, Berlin JA, Morton SC, et al. Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA. 2000;283(15):2008–12.CrossRefPubMed Stroup DF, Berlin JA, Morton SC, et al. Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA. 2000;283(15):2008–12.CrossRefPubMed
39.
go back to reference Higgins J, Green S, editors. Cochrane handbook for systematic reviews of interventions. Version 5.1.0 [updated March 2011]. The Cochrane Collaboration. Available at: www.cochrane-handbook.org. Accessed 24 Nov 2014 Higgins J, Green S, editors. Cochrane handbook for systematic reviews of interventions. Version 5.1.0 [updated March 2011]. The Cochrane Collaboration. Available at: www.​cochrane-handbook.​org. Accessed 24 Nov 2014
40.
go back to reference Bjarnadottir OH, Konradsdottir AD, Reynisdottir K, et al. Multiple sclerosis and brief moderate exercise. A randomised study. Mult Scler. 2007;13(6):776–82.CrossRefPubMed Bjarnadottir OH, Konradsdottir AD, Reynisdottir K, et al. Multiple sclerosis and brief moderate exercise. A randomised study. Mult Scler. 2007;13(6):776–82.CrossRefPubMed
41.
go back to reference Rasova K, Havrdova E, Brandejsky P, et al. Comparison of the influence of different rehabilitation programmes on clinical, spirometric and spiroergometric parameters in patients with multiple sclerosis. Mult Scler. 2006;12(2):227–34.CrossRefPubMed Rasova K, Havrdova E, Brandejsky P, et al. Comparison of the influence of different rehabilitation programmes on clinical, spirometric and spiroergometric parameters in patients with multiple sclerosis. Mult Scler. 2006;12(2):227–34.CrossRefPubMed
42.
go back to reference Cohen J. Statistical power analysis for the behavioral sciences. New York: Academic Press; 1988. Cohen J. Statistical power analysis for the behavioral sciences. New York: Academic Press; 1988.
43.
go back to reference Romberg A, Virtanen A, Ruutiainen J, et al. Effects of a 6-month exercise program on patients with multiple sclerosis: a randomized study. Neurology. 2004;63(11):2034–8.CrossRefPubMed Romberg A, Virtanen A, Ruutiainen J, et al. Effects of a 6-month exercise program on patients with multiple sclerosis: a randomized study. Neurology. 2004;63(11):2034–8.CrossRefPubMed
44.
go back to reference Heine M, Hoogervorst EL, Hacking HG, et al. Validity of maximal exercise testing in patients with low to moderate multiple sclerosis. Phys Ther. 2014;94(8):1168–75.CrossRefPubMed Heine M, Hoogervorst EL, Hacking HG, et al. Validity of maximal exercise testing in patients with low to moderate multiple sclerosis. Phys Ther. 2014;94(8):1168–75.CrossRefPubMed
45.
go back to reference Briken S, Gold SM, Patra S, et al. Effects of exercise on fitness and cognition in progressive MS: a randomized, controlled pilot trial. Mult Scler. 2014;20(3):382–90.CrossRefPubMed Briken S, Gold SM, Patra S, et al. Effects of exercise on fitness and cognition in progressive MS: a randomized, controlled pilot trial. Mult Scler. 2014;20(3):382–90.CrossRefPubMed
46.
go back to reference Schulz KH, Gold SM, Witte J, et al. Impact of aerobic training on immune-endocrine parameters, neurotrophic factors, quality of life and coordinative function in multiple sclerosis. J Neurol Sci. 2004;225(1–2):11–8.CrossRefPubMed Schulz KH, Gold SM, Witte J, et al. Impact of aerobic training on immune-endocrine parameters, neurotrophic factors, quality of life and coordinative function in multiple sclerosis. J Neurol Sci. 2004;225(1–2):11–8.CrossRefPubMed
47.
go back to reference Koseoglu BF, Gokkaya NK, Ergun U, et al. Cardiopulmonary and metabolic functions, aerobic capacity, fatigue and quality of life in patients with multiple sclerosis. Acta Neurol Scand. 2006;114(4):261–7.CrossRefPubMed Koseoglu BF, Gokkaya NK, Ergun U, et al. Cardiopulmonary and metabolic functions, aerobic capacity, fatigue and quality of life in patients with multiple sclerosis. Acta Neurol Scand. 2006;114(4):261–7.CrossRefPubMed
48.
go back to reference Motl RW, Fernhall B. Accurate prediction of cardiorespiratory fitness using cycle ergometry in minimally disabled persons with relapsing-remitting multiple sclerosis. Arch Phys Med Rehabil. 2012;93(3):490–5.CrossRefPubMed Motl RW, Fernhall B. Accurate prediction of cardiorespiratory fitness using cycle ergometry in minimally disabled persons with relapsing-remitting multiple sclerosis. Arch Phys Med Rehabil. 2012;93(3):490–5.CrossRefPubMed
49.
go back to reference Jette AM. Toward a common language for function, disability, and health. Phys Ther. 2006;86(5):726–34.PubMed Jette AM. Toward a common language for function, disability, and health. Phys Ther. 2006;86(5):726–34.PubMed
50.
go back to reference Golzari Z, Shabkhiz F, Soudi S, et al. Combined exercise training reduces IFN-(gamma) and IL-17 levels in the plasma and the supernatant of peripheral blood mononuclear cells in women with multiple sclerosis. Int Immunopharmacol. 2010;10(11):1415–9.CrossRefPubMed Golzari Z, Shabkhiz F, Soudi S, et al. Combined exercise training reduces IFN-(gamma) and IL-17 levels in the plasma and the supernatant of peripheral blood mononuclear cells in women with multiple sclerosis. Int Immunopharmacol. 2010;10(11):1415–9.CrossRefPubMed
51.
go back to reference Petajan JH, Gappmaier E, White AT, et al. Impact of aerobic training on fitness and quality of life in multiple sclerosis. Ann Neurol. 1996;39(4):432–41.CrossRefPubMed Petajan JH, Gappmaier E, White AT, et al. Impact of aerobic training on fitness and quality of life in multiple sclerosis. Ann Neurol. 1996;39(4):432–41.CrossRefPubMed
52.
go back to reference Skjerbaek AG, Naesby M, Lutzen K, et al. Endurance training is feasible in severely disabled patients with progressive multiple sclerosis. Mult Scler. 2014;20(5):627–30.CrossRefPubMed Skjerbaek AG, Naesby M, Lutzen K, et al. Endurance training is feasible in severely disabled patients with progressive multiple sclerosis. Mult Scler. 2014;20(5):627–30.CrossRefPubMed
53.
go back to reference Bansi J, Bloch W, Gamper U, et al. Endurance training in MS: short-term immune responses and their relation to cardiorespiratory fitness, health-related quality of life, and fatigue. J Neurol. 2013;260(12):2993–3001.CrossRefPubMed Bansi J, Bloch W, Gamper U, et al. Endurance training in MS: short-term immune responses and their relation to cardiorespiratory fitness, health-related quality of life, and fatigue. J Neurol. 2013;260(12):2993–3001.CrossRefPubMed
54.
go back to reference Bansi J, Bloch W, Gamper U, et al. Training in MS: influence of two different endurance training protocols (aquatic versus overland) on cytokine and neurotrophin concentrations during three week randomized controlled trial. Mult Scler. 2013;19(5):613–21.CrossRefPubMed Bansi J, Bloch W, Gamper U, et al. Training in MS: influence of two different endurance training protocols (aquatic versus overland) on cytokine and neurotrophin concentrations during three week randomized controlled trial. Mult Scler. 2013;19(5):613–21.CrossRefPubMed
55.
go back to reference Feltham MG, Collett J, Izadi H, et al. Cardiovascular adaptation in people with multiple sclerosis following a twelve week exercise programme suggest deconditioning rather than autonomic dysfunction caused by the disease. Results from a randomized controlled trial. Eur J Phys Rehabil Med. 2013;49(6):765–74.PubMed Feltham MG, Collett J, Izadi H, et al. Cardiovascular adaptation in people with multiple sclerosis following a twelve week exercise programme suggest deconditioning rather than autonomic dysfunction caused by the disease. Results from a randomized controlled trial. Eur J Phys Rehabil Med. 2013;49(6):765–74.PubMed
56.
go back to reference Collett J, Dawes H, Meaney A, et al. Exercise for multiple sclerosis: a single-blind randomized trial comparing three exercise intensities. Mult Scler. 2011;17(5):594–603.CrossRefPubMed Collett J, Dawes H, Meaney A, et al. Exercise for multiple sclerosis: a single-blind randomized trial comparing three exercise intensities. Mult Scler. 2011;17(5):594–603.CrossRefPubMed
57.
go back to reference Rampello A, Franceschini M, Piepoli M, et al. Effect of aerobic training on walking capacity and maximal exercise tolerance in patients with multiple sclerosis: a randomized crossover controlled study. Phys Ther. 2007;87(5):545–55.CrossRefPubMed Rampello A, Franceschini M, Piepoli M, et al. Effect of aerobic training on walking capacity and maximal exercise tolerance in patients with multiple sclerosis: a randomized crossover controlled study. Phys Ther. 2007;87(5):545–55.CrossRefPubMed
58.
go back to reference Mostert S, Kesselring J. Effects of a short-term exercise training program on aerobic fitness, fatigue, health perception and activity level of subjects with multiple sclerosis. Mult Scler. 2002;8(2):161–8.CrossRefPubMed Mostert S, Kesselring J. Effects of a short-term exercise training program on aerobic fitness, fatigue, health perception and activity level of subjects with multiple sclerosis. Mult Scler. 2002;8(2):161–8.CrossRefPubMed
59.
go back to reference Ponichtera-Mulcare JA, Mathews T, Barrett PJ, et al. Change in aerobic fitness of patients with multiple sclerosis during a 6-month training program. Sports Med Train Rehabil. 1997;7(3–4):265–72.CrossRef Ponichtera-Mulcare JA, Mathews T, Barrett PJ, et al. Change in aerobic fitness of patients with multiple sclerosis during a 6-month training program. Sports Med Train Rehabil. 1997;7(3–4):265–72.CrossRef
60.
go back to reference Rodgers MM, Mulcare JA, King DL, et al. Gait characteristics of individuals with multiple sclerosis before and after a 6-month aerobic training program. J Rehabil Res Dev. 1999;36(3):183–8.PubMed Rodgers MM, Mulcare JA, King DL, et al. Gait characteristics of individuals with multiple sclerosis before and after a 6-month aerobic training program. J Rehabil Res Dev. 1999;36(3):183–8.PubMed
61.
go back to reference Buchfuhrer MJ, Hansen JE, Robinson TE, et al. Optimizing the exercise protocol for cardiopulmonary assessment. J Appl Physiol Respir Environ Exerc Physiol. 1983;55(5):1558–64.PubMed Buchfuhrer MJ, Hansen JE, Robinson TE, et al. Optimizing the exercise protocol for cardiopulmonary assessment. J Appl Physiol Respir Environ Exerc Physiol. 1983;55(5):1558–64.PubMed
63.
go back to reference Hale LA, Nukada H, Du Plessis LJ, et al. Clinical screening of autonomic dysfunction in multiple sclerosis. Physiother Res Int. 2009;14(1):42–55.CrossRefPubMed Hale LA, Nukada H, Du Plessis LJ, et al. Clinical screening of autonomic dysfunction in multiple sclerosis. Physiother Res Int. 2009;14(1):42–55.CrossRefPubMed
64.
go back to reference Gallien P, Nicolas B, Robineau S, et al. Physical training and multiple sclerosis. Ann Readapt Med Phys. 2007;50(6):373–6 (369–72).CrossRefPubMed Gallien P, Nicolas B, Robineau S, et al. Physical training and multiple sclerosis. Ann Readapt Med Phys. 2007;50(6):373–6 (369–72).CrossRefPubMed
65.
go back to reference Ponichtera-Mulcare JA, Mathews T, Glaser RM, et al. Maximal aerobic exercise of individuals with multiple sclerosis using three modes of ergometry. Clin Kinesiol. 1995;49(1):4–13. Ponichtera-Mulcare JA, Mathews T, Glaser RM, et al. Maximal aerobic exercise of individuals with multiple sclerosis using three modes of ergometry. Clin Kinesiol. 1995;49(1):4–13.
66.
go back to reference Morrison EH, Cooper DM, White LJ, et al. Ratings of perceived exertion during aerobic exercise in multiple sclerosis. Arch Phys Med Rehabil. 2008;89(8):1570–4.CrossRefPubMed Morrison EH, Cooper DM, White LJ, et al. Ratings of perceived exertion during aerobic exercise in multiple sclerosis. Arch Phys Med Rehabil. 2008;89(8):1570–4.CrossRefPubMed
67.
go back to reference Ng AV, Kent-Braun JA. Quantitation of lower physical activity in persons with multiple sclerosis. Med Sci Sports Exerc. 1997;29(4):517–23.CrossRefPubMed Ng AV, Kent-Braun JA. Quantitation of lower physical activity in persons with multiple sclerosis. Med Sci Sports Exerc. 1997;29(4):517–23.CrossRefPubMed
68.
go back to reference Christou DD, Seals DR. Decreased maximal heart rate with aging is related to reduced {beta}-adrenergic responsiveness but is largely explained by a reduction in intrinsic heart rate. J Appl Physiol (1985). 2008;105(1):24–9.CrossRef Christou DD, Seals DR. Decreased maximal heart rate with aging is related to reduced {beta}-adrenergic responsiveness but is largely explained by a reduction in intrinsic heart rate. J Appl Physiol (1985). 2008;105(1):24–9.CrossRef
69.
go back to reference Foglio K, Clini E, Facchetti D, et al. Respiratory muscle function and exercise capacity in multiple sclerosis. Eur Respir J. 1994;7(1):23–8.CrossRefPubMed Foglio K, Clini E, Facchetti D, et al. Respiratory muscle function and exercise capacity in multiple sclerosis. Eur Respir J. 1994;7(1):23–8.CrossRefPubMed
70.
go back to reference Taylor HL, Buskirk E, Henschel A. Maximal oxygen intake as an objective measure of cardio-respiratory performance. J Appl Physiol. 1955;8(1):73–80.PubMed Taylor HL, Buskirk E, Henschel A. Maximal oxygen intake as an objective measure of cardio-respiratory performance. J Appl Physiol. 1955;8(1):73–80.PubMed
71.
go back to reference 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(19):2024–35.CrossRefPubMed 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(19):2024–35.CrossRefPubMed
72.
go back to reference Romberg A, Virtanen A, Aunola S, et al. Exercise capacity, disability and leisure physical activity of subjects with multiple sclerosis. Mult Scler. 2004;10(2):212–8.CrossRefPubMed Romberg A, Virtanen A, Aunola S, et al. Exercise capacity, disability and leisure physical activity of subjects with multiple sclerosis. Mult Scler. 2004;10(2):212–8.CrossRefPubMed
73.
go back to reference Motl RW, Goldman MD. Physical inactivity, neurological disability, and cardiorespiratory fitness in multiple sclerosis. Mult Scler. 2010;16(8):1019. Motl RW, Goldman MD. Physical inactivity, neurological disability, and cardiorespiratory fitness in multiple sclerosis. Mult Scler. 2010;16(8):1019.
74.
go back to reference Konecny L, Pospisil P, Dufek M, et al. Functional impairment in multiple sclerosis. Scr Med Fac Med Univ Brun Masarykianae. 2007;80(5):225–32. Konecny L, Pospisil P, Dufek M, et al. Functional impairment in multiple sclerosis. Scr Med Fac Med Univ Brun Masarykianae. 2007;80(5):225–32.
76.
go back to reference Hobart J, Freeman J, Thompson A. Kurtzke scales revisited: the application of psychometric methods to clinical intuition. Brain. 2000;123(Pt 5):1027–40.CrossRefPubMed Hobart J, Freeman J, Thompson A. Kurtzke scales revisited: the application of psychometric methods to clinical intuition. Brain. 2000;123(Pt 5):1027–40.CrossRefPubMed
77.
go back to reference Sharrack B, Hughes RA, Soudain S, et al. The psychometric properties of clinical rating scales used in multiple sclerosis. Brain. 1999;122(Pt 1):141–59.CrossRefPubMed Sharrack B, Hughes RA, Soudain S, et al. The psychometric properties of clinical rating scales used in multiple sclerosis. Brain. 1999;122(Pt 1):141–59.CrossRefPubMed
78.
go back to reference Geidl W, Semrau J, Pfeifer K. Health behaviour change theories: contributions to an ICF-based behavioural exercise therapy for individuals with chronic diseases. Disabil Rehabil. 2014;36(24):2091–100.CrossRefPubMed Geidl W, Semrau J, Pfeifer K. Health behaviour change theories: contributions to an ICF-based behavioural exercise therapy for individuals with chronic diseases. Disabil Rehabil. 2014;36(24):2091–100.CrossRefPubMed
79.
go back to reference Heine M, Verschuren O, Kwakkel G. Validity of oxygen uptake efficiency slope in patients with multiple sclerosis. J Rehabil Med. 2014;46(7):656–61.CrossRefPubMed Heine M, Verschuren O, Kwakkel G. Validity of oxygen uptake efficiency slope in patients with multiple sclerosis. J Rehabil Med. 2014;46(7):656–61.CrossRefPubMed
80.
go back to reference Petruzzello SJ, Motl RW. Acute moderate-intensity cycling exercise is associated with reduced fatigue in persons with multiple sclerosis. Ment Health Phys Act. 2011;4(1):1–4.CrossRef Petruzzello SJ, Motl RW. Acute moderate-intensity cycling exercise is associated with reduced fatigue in persons with multiple sclerosis. Ment Health Phys Act. 2011;4(1):1–4.CrossRef
81.
go back to reference Petruzzello SJ, Snook EM, Gliottoni RC, et al. Anxiety and mood changes associated with acute cycling in persons with multiple sclerosis. Anxiety Stress Coping. 2009;22(3):297–307.CrossRefPubMed Petruzzello SJ, Snook EM, Gliottoni RC, et al. Anxiety and mood changes associated with acute cycling in persons with multiple sclerosis. Anxiety Stress Coping. 2009;22(3):297–307.CrossRefPubMed
82.
go back to reference Kuspinar A, Andersen RE, Teng SY, et al. Predicting exercise capacity through submaximal fitness tests in persons with multiple sclerosis. Arch Phys Med Rehabil. 2010;91(9):1410–7.CrossRefPubMed Kuspinar A, Andersen RE, Teng SY, et al. Predicting exercise capacity through submaximal fitness tests in persons with multiple sclerosis. Arch Phys Med Rehabil. 2010;91(9):1410–7.CrossRefPubMed
83.
go back to reference Skjerbaek AG, Møller AB, Jensen E, et al. Heat sensitive persons with multiple sclerosis are more tolerant to resistance exercise than to endurance exercise. Mult Scler. 2013;19(7):932–40.CrossRefPubMed Skjerbaek AG, Møller AB, Jensen E, et al. Heat sensitive persons with multiple sclerosis are more tolerant to resistance exercise than to endurance exercise. Mult Scler. 2013;19(7):932–40.CrossRefPubMed
84.
go back to reference Møller AB, Bibby BM, Skjerbaek AG, et al. Validity and variability of the 5-repetition sit-to-stand test in patients with multiple sclerosis. Disabil Rehabil. 2012;34(26):2251–8.CrossRefPubMed Møller AB, Bibby BM, Skjerbaek AG, et al. Validity and variability of the 5-repetition sit-to-stand test in patients with multiple sclerosis. Disabil Rehabil. 2012;34(26):2251–8.CrossRefPubMed
85.
go back to reference Gold SM, Schulz KH, Hartmann S, et al. Basal serum levels and reactivity of nerve growth factor and brain-derived neurotrophic factor to standardized acute exercise in multiple sclerosis and controls. J Neuroimmunol. 2003;138(1–2):99–105.CrossRefPubMed Gold SM, Schulz KH, Hartmann S, et al. Basal serum levels and reactivity of nerve growth factor and brain-derived neurotrophic factor to standardized acute exercise in multiple sclerosis and controls. J Neuroimmunol. 2003;138(1–2):99–105.CrossRefPubMed
86.
go back to reference White AT, Wilson TE, Davis SL, et al. Effect of precooling on physical performance in multiple sclerosis. Mult Scler. 2000;6(3):176–80.CrossRefPubMed White AT, Wilson TE, Davis SL, et al. Effect of precooling on physical performance in multiple sclerosis. Mult Scler. 2000;6(3):176–80.CrossRefPubMed
87.
go back to reference Heesen C, Gold SM, Hartmann S, et al. Endocrine and cytokine responses to standardized physical stress in multiple sclerosis. Brain Behav Immun. 2003;17(6):473–81.CrossRefPubMed Heesen C, Gold SM, Hartmann S, et al. Endocrine and cytokine responses to standardized physical stress in multiple sclerosis. Brain Behav Immun. 2003;17(6):473–81.CrossRefPubMed
Metadata
Title
Aerobic Capacity in Persons with Multiple Sclerosis: A Systematic Review and Meta-Analysis
Authors
Martin Langeskov-Christensen
Martin Heine
Gert Kwakkel
Ulrik Dalgas
Publication date
01-06-2015
Publisher
Springer International Publishing
Published in
Sports Medicine / Issue 6/2015
Print ISSN: 0112-1642
Electronic ISSN: 1179-2035
DOI
https://doi.org/10.1007/s40279-015-0307-x

Other articles of this Issue 6/2015

Sports Medicine 6/2015 Go to the issue