Journal of Neurology

, Volume 260, Issue 7, pp 1822–1832

Neural drive increases following resistance training in patients with multiple sclerosis

  • Ulrik Dalgas
  • Egon Stenager
  • Caroline Lund
  • Cuno Rasmussen
  • Thor Petersen
  • Henrik Sørensen
  • Thorsten Ingemann-Hansen
  • Kristian Overgaard
Original Communication

Abstract

The present study tested the hypothesis that lower body progressive resistance training (PRT) increases the neural drive expressed as surface electromyographical (EMG) activity in patients with multiple sclerosis (MS). The study was a randomised controlled trial (RCT) including a 12-week follow up period. Thirty-eight MS patients were randomized to an exercise group (n = 19) or a control group (n = 19). During the intervention period, the exercise group performed a 12-week supervised lower body PRT program, whereas the control group maintained their usual daily activity level. After the 12 week intervention period, the exercise group were encouraged to continue training on their own for a 12-week follow up period, while the control group completed the 12-week supervised PRT program. Surface EMG was recorded from vastus lateralis, rectus femoris and semitendinosus during maximal isometric knee extension and knee flexion, before and after the intervention and at follow up. From the recordings, the area under the rectified, low-pass filtered EMG signal (integrated EMG, iEMG) was calculated. Muscle strength was expressed as the angular impulse (AI) and was measured during the same period as the iEMG. After PRT significant improvements for iEMG of vastus lateralis and rectus femoris during maximal knee extension and for semitendinosus during maximal knee flexion and for AI during both maximal knee extension and flexion were found in the exercise group, when compared to the control group. When compared to the post values, all effects, except for AI during knee flexion, were maintained at follow up in the exercise group. When the control group was exposed to PRT, a similar pattern of improvements were found, albeit not all improvements were significant. In conclusion twelve weeks of intense PRT of the lower extremities improved the neural drive expressed as maximal surface EMG activity in patients with MS, with effects persisting 12 weeks after the intervention. The study was registered at clinicalTrials.gov, Protocol no. NCT00381576.

Keywords

Exercise Muscle strength Strength training Exercise therapy MS rehabilitation 

References

  1. 1.
    Aagaard P, Simonsen EB, Andersen JL, Magnusson P, Dyhre-Poulsen P (2002) Increased rate of force development and neural drive of human skeletal muscle following resistance training. J Appl Physiol 93:1318–1326PubMedGoogle Scholar
  2. 2.
    Aagaard P, Simonsen EB, Andersen JL, Magnusson SP, Bojsen-Moller F, Dyhre-Poulsen P (2000) Antagonist muscle coactivation during isokinetic knee extension. Scand J Med Sci Sports 10:58–67PubMedCrossRefGoogle Scholar
  3. 3.
    Aagaard P, Thorstensson A (2003) Neuromuscular aspects of exercise—adaptive responses evoked by strength training. In: Kjaer M (ed) Textbook of Sport Medicine. Blackwell Press, pp 70–106Google Scholar
  4. 4.
    Carroll CC, Gallagher PM, Seidle ME, Trappe SW (2005) Skeletal muscle characteristics of people with multiple sclerosis. Arch Phys Med Rehabil 86:224–229PubMedCrossRefGoogle Scholar
  5. 5.
    Dalgas U, Stenager E, Jakobsen J, Petersen T, Hansen H, Knudsen C, Overgaard K, Ingemann-Hansen T (2009) Resistance training improves muscle strength and functional capacity in multiple sclerosis. Neurology 73:1478–1484PubMedCrossRefGoogle Scholar
  6. 6.
    Dalgas U, Stenager E, Jakobsen J, Petersen T, Hansen H, Knudsen C, Overgaard K, Ingemann-Hansen T (2010) Fatigue, mood and quality of life improve in MS patients after progressive resistance training. Mult Scler 16:480–490PubMedCrossRefGoogle Scholar
  7. 7.
    Dalgas U, Stenager E, Jakobsen J, Petersen T, Overgaard K, Ingemann-Hansen T (2010) Muscle fiber size increases following resistance training in multiple sclerosis. Mult Scler 16:1367–1376PubMedCrossRefGoogle Scholar
  8. 8.
    de Haan A, de Ruiter CJ, Der Woude LH, Jongen PJ (2000) Contractile properties and fatigue of quadriceps muscles in multiple sclerosis. Muscle Nerve 23:1534–1541PubMedCrossRefGoogle Scholar
  9. 9.
    Dorfman LJ, Howard JE, McGill KC (1989) Motor unit firing rates and firing rate variability in the detection of neuromuscular disorders. Electroencephalogr Clin Neurophysiol 73:215–224PubMedCrossRefGoogle Scholar
  10. 10.
    Fimland MS, Helgerud J, Gruber M, Leivseth G, Hoff J (2010) Enhanced neural drive after maximal strength training in multiple sclerosis patients. Eur J Appl Physiol 110:435–443PubMedCrossRefGoogle Scholar
  11. 11.
    Folland JP, Williams AG (2007) The adaptations to strength training: morphological and neurological contributions to increased strength. Sports Med 37:145–168PubMedCrossRefGoogle Scholar
  12. 12.
    Formica CA, Cosman F, Nieves J, Herbert J, Lindsay R (1997) Reduced bone mass and fat-free mass in women with multiple sclerosis: effects of ambulatory status and glucocorticoid use. Calcif Tissue Int 61:129–133PubMedCrossRefGoogle Scholar
  13. 13.
    Gabriel DA, Kamen G, Frost G (2006) Neural adaptations to resistive exercise: mechanisms and recommendations for training practices. Sports Med 36:133–149PubMedCrossRefGoogle Scholar
  14. 14.
    Garner DJ, Widrick JJ (2003) Cross-bridge mechanisms of muscle weakness in multiple sclerosis. Muscle Nerve 27:456–464PubMedCrossRefGoogle Scholar
  15. 15.
    Ingemann-Hansen T, Halkjaer-Kristensen J (1977) Lean and fat component of the human thigh. The effects of immobilization in plaster and subsequent physical training. Scand J Rehabil Med 9:67–72PubMedGoogle Scholar
  16. 16.
    Kantarci OH (2008) Genetics and natural history of multiple sclerosis. Semin Neurol 28:7–16PubMedCrossRefGoogle Scholar
  17. 17.
    Kent-Braun JA, Ng AV, Castro M, Weiner MW, Gelinas D, Dudley GA, Miller RG (1997) Strength, skeletal muscle composition, and enzyme activity in multiple sclerosis. J Appl Physiol 83:1998–2004PubMedGoogle Scholar
  18. 18.
    Kjølhede T, Vissing K, Dalgas U (2012) Multiple sclerosis and progressive resistance training—a systematic review. Mult Scler 18:1215–1228PubMedCrossRefGoogle Scholar
  19. 19.
    Lambert CP, Lee AR, Evans WJ (2002) Body composition in ambulatory women with multiple sclerosis. Arch Phys Med Rehabil 83:1559–1561PubMedCrossRefGoogle Scholar
  20. 20.
    Lexell J, Taylor CC (1989) Variability in muscle fibre areas in whole human quadriceps muscle. How much and why? Acta Physiol Scand 136:561–568PubMedCrossRefGoogle Scholar
  21. 21.
    McDonald WI, Compston A, Edan G, Goodkin D, Hartung HP, Lublin FD, McFarland HF, Paty DW, Polman CH, Reingold SC, Sandberg-Wollheim M, Sibley W, Thompson A, Van den NS, Weinshenker BY, Wolinsky JS (2001) Recommended diagnostic criteria for multiple sclerosis: guidelines from the International Panel on the diagnosis of multiple sclerosis. Ann Neurol 50:121–127PubMedCrossRefGoogle Scholar
  22. 22.
    Moritani T, deVries HA (1980) Potential for gross muscle hypertrophy in older men. J Gerontol 35:672–682PubMedCrossRefGoogle Scholar
  23. 23.
    Ng AV, Miller RG, Gelinas D, Kent-Braun JA (2004) Functional relationships of central and peripheral muscle alterations in multiple sclerosis. Muscle Nerve 29:843–852PubMedCrossRefGoogle Scholar
  24. 24.
    Rice CL, Vollmer TL, Bigland-Ritchie B (1992) Neuromuscular responses of patients with multiple sclerosis. Muscle Nerve 15:1123–1132PubMedCrossRefGoogle Scholar
  25. 25.
    Rosenfalck A, Andreassen S (1980) Impaired regulation of force and firing pattern of single motor units in patients with spasticity. J Neurol Neurosurg Psychiatry 43:907–916PubMedCrossRefGoogle Scholar
  26. 26.
    Savci S, Inal-Inc Arikan H, Guclu-Gunduz A, Cetisli-Korkmaz N, Armutlu K, Karabudak R (2005) Six-minute walk distance as a measure of functional exercise capacity in multiple sclerosis. Disabil Rehabil 27:1365–1371PubMedCrossRefGoogle Scholar
  27. 27.
    Schwid SR, Thornton CA, Pandya S, Manzur KL, Sanjak M, Petrie MD, McDermott MP, Goodman AD (1999) Quantitative assessment of motor fatigue and strength in MS. Neurology 53:743–750PubMedCrossRefGoogle Scholar
  28. 28.
    Scott SM, Hughes AR, Galloway SD, Hunter AM (2011) Surface EMG characteristics of people with multiple sclerosis during static contractions of the knee extensors. Clin Physiol Funct Imaging 31:11–17PubMedCrossRefGoogle Scholar
  29. 29.
    Sharma KR, Kent-Braun J, Mynhier MA, Weiner MW, Miller RG (1995) Evidence of an abnormal intramuscular component of fatigue in multiple sclerosis. Muscle Nerve 18:1403–1411PubMedCrossRefGoogle Scholar
  30. 30.
    Sheean GL, Murray NM, Rothwell JC, Miller DH, Thompson AJ (1997) An electrophysiological study of the mechanism of fatigue in multiple sclerosis. Brain 120(Pt 2):299–315PubMedCrossRefGoogle Scholar
  31. 31.
    Thickbroom GW, Sacco P, Faulkner DL, Kermode AG, Mastaglia FL (2008) Enhanced corticomotor excitability with dynamic fatiguing exercise of the lower limb in multiple sclerosis. J Neurol 255:1001–1005PubMedCrossRefGoogle Scholar
  32. 32.
    Thoumie P, Mevellec E (2002) Relation between walking speed and muscle strength is affected by somatosensory loss in multiple sclerosis. J Neurol Neurosurg Psychiatry 73:313–315PubMedCrossRefGoogle Scholar
  33. 33.
    White LJ, McCoy SC, Castellano V, Gutierrez G, Stevens JE, Walter GA, Vandenborne K (2004) Resistance training improves strength and functional capacity in persons with multiple sclerosis. Mult Scler 10:668–674PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Ulrik Dalgas
    • 1
  • Egon Stenager
    • 2
    • 3
  • Caroline Lund
    • 1
  • Cuno Rasmussen
    • 1
  • Thor Petersen
    • 4
  • Henrik Sørensen
    • 1
  • Thorsten Ingemann-Hansen
    • 1
  • Kristian Overgaard
    • 1
  1. 1.Section of Sport Science, Department of Public HealthAarhus UniversityAarhus CDenmark
  2. 2.Department of Neurology, MS-Clinic of Southern Jutland (Sønderborg, Esbjerg, Vejle)Sønderborg HospitalSønderborgDenmark
  3. 3.Institute of Regional Health ResearchUniversity of Southern DenmarkOdenseDenmark
  4. 4.Department of NeurologyAarhus University HospitalAarhusDenmark

Personalised recommendations