Sports Medicine

, Volume 46, Issue 9, pp 1365–1379 | Cite as

Comprehensive Profile of Cardiopulmonary Exercise Testing in Ambulatory Persons with Multiple Sclerosis

  • Rachel E. Klaren
  • Brian M. Sandroff
  • Bo Fernhall
  • Robert W. Motl
Original Research Article

Abstract

Background

The study and application of exercise in multiple sclerosis (MS) often requires cardiopulmonary exercise testing (CPET) to provide a comprehensive assessment of exercise tolerance and responses, including an evaluation of the pulmonary, cardiovascular, and skeletal muscle systems. Research on CPET in persons with MS has considerable limitations, including small sample sizes, often without controls; not reporting outcomes across disability status; and different modalities of exercise testing across studies. Although some key outcome variables of CPET have been studied in persons with MS, additional calculated variables have not been directly studied.

Objective

The objective of this study was to provide a comprehensive examination of outcome variables from CPET among persons with MS and healthy controls.

Methods

We included data from 162 persons with MS and 80 healthy controls who underwent CPET on a leg ergometer and satisfied criteria for valid testing for measuring oxygen uptake (VO2), carbon dioxide production (VCO2), ventilation (VE), respiratory exchange ratio, work rate, and heart rate (HR). Calculated variables [i.e. ventilatory anaerobic threshold (VO2/VCO2), VE/VCO2 slope, VO2/power slope, VO2/HR slope, and oxygen uptake efficiency slope] were processed using standard guidelines. We examined differences in the CPET variables between groups (e.g. MS vs. controls and categories of mild, moderate, and severe disability status) using analysis of covariance (ANCOVA), controlling for age, sex, body mass index, and disease duration.

Results

Overall, persons with MS demonstrate alterations in outcomes from CPET compared with controls, and these are generally exacerbated with increasing disability.

Conclusion

Our results provide novel information for the evaluation of CPET in MS for developing exercise prescriptions and documenting adaptations with exercise training based on the comprehensive variables obtained during CPET.

References

  1. 1.
    Mayr WT, Pittock SJ, McClelland RL, Jorgensen NW, Noseworthy JH, Rodriguez M. Incidence and prevalence of multiple sclerosis in Olmsted County, Minnesota, 1985–2000. Neurology. 2003;61(10):1373–7.CrossRefPubMedGoogle Scholar
  2. 2.
    Lublin FD. Clinical features and diagnosis of multiple sclerosis. Neurol Clin. 2005;23(1):1–15.CrossRefPubMedGoogle Scholar
  3. 3.
    Pilutti LA, Platta ME, Motl RW, Latimer-Cheung AE. The safety of exercise training in multiple sclerosis: a systematic review. J Neurol Sci. 2014;343(1–2):3–7.CrossRefPubMedGoogle Scholar
  4. 4.
    Motl RW, Pilutti LA. The benefits of exercise training in multiple sclerosis. Nat Rev Neurol. 2012;8(9):487–97.CrossRefPubMedGoogle Scholar
  5. 5.
    Ferrazza AM, Martolini D, Palange P. Cardiopulmonary exercise testing in the functional and prognostic evaluation of patients with pulmonary diseases. Respiration. 2009;77:3–17.CrossRefPubMedGoogle Scholar
  6. 6.
    Balady GJ, et al. Clinician’s guide to cardiopulmonary exercise testing in adults: a scientific statement from the American Heart Association. Circulation. 2010;122(2):191–225.CrossRefPubMedGoogle Scholar
  7. 7.
    Guazzi M, et al. EACPR/AHA Joint Scientific Statement. Clinical recommendations for cardiopulmonary exercise testing data assessment in specific patient populations. Eur Heart J. 2012;33(23):2917–27.CrossRefPubMedGoogle Scholar
  8. 8.
    Langeskov-Christensen M, Langeskov-Christensen D, Overgaard K, Moller AB, Dalgas U. Validity and reliability of VO2-max measurements in persons with MS. J Neurol Sci. 2014;342(1–2):79–87.CrossRefPubMedGoogle Scholar
  9. 9.
    Langeskov-Christensen M, Heine M, Kwakkel G, Dalgas U. Aerobic capacity in persons with multiple sclerosis: a systematic review and meta-analysis. Sports Med. 2015;56(6):905–23.CrossRefGoogle Scholar
  10. 10.
    Heine M, Verschuren O, Kwakkel G. Validity of the oxygen uptake efficiency slope in patients with multiple sclerosis. J Rehabil Med. 2014;46(7):656–61.CrossRefPubMedGoogle Scholar
  11. 11.
    Morrison EH, et al. Ratings of perceived exertion during aerobic exercise in multiple sclerosis. Arch Phys Med Rehabil. 2008;89(8):170–4.CrossRefGoogle Scholar
  12. 12.
    Heine M, Hoogervorst EL, Hacking HG, Verschuren O, Kwakkel G. Validity of maximal exercise testing in people with multiple sclerosis and low to moderate levels of disability. Phys Ther. 2014;94(8):1168–75.CrossRefPubMedGoogle Scholar
  13. 13.
    Koseoglu BF, Gokkaya NK, Ergun U, Inan L, Yesiltepe E. Cardiopulmonary and metabolic functions, aerobic capacity, fatigue and quality of life in patients with multiple sclerosis. Acta Neurol Scand. 2006;114(4):261–7.CrossRefPubMedGoogle Scholar
  14. 14.
    Wasserman K, Hansen JE, Sue DY, Stringer WW, Sietsema KE, Sun X, et al. Principles of exercise testing and interpretation. Philadelphia: Lippincott Williams & Wilkins; 2012.Google Scholar
  15. 15.
    Coeckelberghs E, Buys R, Goetschalckx K, Cornelissen VA, Vanhees L. Prognostic value of the oxygen uptake efficiency slope and other exercise variables in patients with coronary artery disease. Eur J Prev Cardiol. Epub 29 Jan 2015.Google Scholar
  16. 16.
    Cahalin LP, Chase P, Arena R, Myers J, Bensimhon D, Peberdy MA, et al. A meta-analysis of the prognostic significance of cardiopulmonary exercise testing in patients with heart failure. Heart Fail Rev. 2013;18(1):79–94.CrossRefPubMedGoogle Scholar
  17. 17.
    Magri D, Agostoni P, Corra U, Passino C, Scrutinio D, Perrone-Filardi P, et al. Deceptive meaning of oxygen uptake measured at the anaerobic threshold in patients with systolic heart failure and atrial fibrillation. Eur J Prev Cardiol. 2015;22(8):1046–55.CrossRefPubMedGoogle Scholar
  18. 18.
    Marrie RA, Reider N, Cohen J, Stuve O, Trojano M, Cutter G, et al. A systematic review of the incidence and prevalence of cardiac, cerebrovascular, and peripheral vascular disease in multiple sclerosis. Mult Scler. 2015;21(3):318–31.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Polman CH, Reingold SC, Banwell B, Clanet M, Cohen JA, Filippi M, et al. Diagnostic criteria for multiple sclerosis: 2010 revisions to the McDonald criteria. Ann Neurol. 2011;69(2):292–302.CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Thomas S, Reading J, Shephard RJ. Revision of the Physical Activity Readiness Questionnaire (PAR-Q). Can J Sport Sci. 1992;17(4):338–45.PubMedGoogle Scholar
  21. 21.
    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;93:490–5.CrossRefPubMedGoogle Scholar
  22. 22.
    Beier M, Bombardier CH, Hartoonian N, Motl RW, Kraft GH. Improved physical fitness correlates with improved cognition in multiple sclerosis. Arch Phys Med Rehabil. 2014;95(7):1328–34.CrossRefPubMedGoogle Scholar
  23. 23.
    Prakash RS, Snook EM, Erickson KI, Colcombe SJ, Voss MW, Motl RW, et al. Cardiorespiratory fitness: a predictor of cortical plasticity in multiple sclerosis. Neuroimage. 2007;34(3):1238–44.CrossRefPubMedGoogle Scholar
  24. 24.
    Gordon D, Mehter M, Gernigon M, Caddy O, Keiller D, Barnes R. The effects of exercise modality on the incidence of plateau at VO2max. Clin Physiol Funct Imaging. 2012;32(5):394–9.CrossRefPubMedGoogle Scholar
  25. 25.
    Learmonth YC, Motl RW, Sandroff BM, Pula JH, Cadavid D. Validation of patient determined disease steps (PDDS) scale scores in persons with multiple sclerosis. BMC Neurol. 2013;13:37.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Marrie RA, Goldman M. Validity of performance scales for disability assessment in multiple sclerosis. Mult Scler. 2007;13(9):1176–82.CrossRefPubMedGoogle Scholar
  27. 27.
    Marrie RA, Cutter G, Tyry T, Vollmer T, Campagnolo D. Does multiple sclerosis-associated disability differ between races? Neurology. 2006;66(8):1235–40.CrossRefPubMedGoogle Scholar
  28. 28.
    Mezzani A, et al. Standards for the use of cardiopulmonary exercise testing for the functional evaluation of cardiac patients: a report from the Exercise Physiology Section of the European Association for Cardiovascular Prevention and Rehabilitation. Eur J Cardiovas Prev Rehabil. 2009;16(3):249–67.CrossRefGoogle Scholar
  29. 29.
    Hollenberg M, Tager IB. Oxygen uptake efficiency slope: an index of exercise performance and cardiopulmonary reserve requiring only submaximal exercise. J Am Coll Cardiol. 2000;36(1):194–201.CrossRefPubMedGoogle Scholar
  30. 30.
    Cohen J. Statistical power analysis for the behavioral sciences. 2nd ed. Hillsdale: Lawrence Erlbaum; 1988.Google Scholar
  31. 31.
    Klaren RE, Motl RW, Dlugonski D, Sandroff BM, Pilutti LA. Objectively quantified physical activity in persons with multiple sclerosis. Arch Phys Med Rehabil. 2013;94(12):2342–8.CrossRefPubMedGoogle Scholar
  32. 32.
    Christou DD, Seals DR. Decreased maximal heart rate with aging is related to reduced β-adrenergic responsiveness but is largely explained by a reduction in intrinsic heart rate. J Appl Physiol. 2008;105:24–9.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Sandroff BM, Klaren RE, Motl RW. Relationships among physical inactivity, deconditioning, and walking impairment in persons with multiple sclerosis. J Neurol Phys Ther. 2015;39(2):103–10.CrossRefPubMedGoogle Scholar
  34. 34.
    Davis JA, Vodak P, Wilmore JH, Vodak J, Kurtz P. Anaerobic threshold and maximal aerobic power for three modes of exercise. J Appl Physiol. 1976;41(4):544–50.PubMedGoogle Scholar
  35. 35.
    Sun XG, Hansen JE, Garatachea N, Storer TW, Wasserman K. Ventilatory efficiency during exercise in healthy subjects. Am J Respir Crit Care Med. 2002;166:1443–8.CrossRefPubMedGoogle Scholar
  36. 36.
    Task Force of the Italian Working Group on Cardiac Rehabilitation Prevention, Working Group on Cardiac Rehabilitation and Exercise Physiology of the European Society of Cardiology, Piepoli MF, et al. Statement on cardiopulmonary exercise testing in chronic heart failure due to left ventricular dysfunction: recommendations for performance and interpretation. Part I: definition of cardiopulmonary exercise testing parameters for appropriate use in chronic heart failure. Eur J Cardiovasc Prev Rehabil. 2006;13(2):150–64.CrossRefGoogle Scholar
  37. 37.
    Kjølhede T, Vissing K, Dalgas U. Multiple sclerosis and progressive resistance training: a systematic review. Mult Scler. 2012;18:1215–28.CrossRefPubMedGoogle Scholar
  38. 38.
    Tantucci C, Massucci M, Piperno R, Grassi V, Sorbini CA. Energy cost of exercise in multiple sclerosis patients with low degree of disability. Mult Scler. 1996;2:161–7.PubMedGoogle Scholar
  39. 39.
    Piepoli MF. Exercise tolerance measurements in pulmonary vascular diseases and chronic heart failure. Respiration. 2009;77:241–51.CrossRefPubMedGoogle Scholar
  40. 40.
    Kurtzke JF. Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS). Neurology. 1983;33(11):1444–52.CrossRefPubMedGoogle Scholar
  41. 41.
    Sutherland G, Andersen MB. Exercise and multiple sclerosis: physiological, psychological, and quality of life issues. J Sports Med Phys Fitness. 2001;41(4):421–32.PubMedGoogle Scholar
  42. 42.
    Frohman EM, Racke MK, Raine CS. Multiple sclerosis: the plaque and its pathogenesis. N Engl J Med. 2006;354:942–55.CrossRefPubMedGoogle Scholar
  43. 43.
    Ashtrand RO, Rodahl K. Textbook of work physiology. New York: McGraw-Hill; 1977.Google Scholar
  44. 44.
    Tesch PA. Exercise performance and beta-blockade. Sports Med. 1985;2(6):389–412.CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Rachel E. Klaren
    • 1
  • Brian M. Sandroff
    • 1
  • Bo Fernhall
    • 2
  • Robert W. Motl
    • 1
  1. 1.Department of Kinesiology and Community HealthUniversity of Illinois at Urbana–ChampaignUrbanaUSA
  2. 2.Department of Kinesiology and NutritionUniversity of Illinois at ChicagoChicagoUSA

Personalised recommendations