Balance disorders in patients with multiple sclerosis and possible rehabilitation therapy – current findings from controlled clinical trials

Czech version

Authors: K. Novotná- ^{1 3*}; I. Menkyová ^1,4*; M. Janatová ^3,5
Authors‘ workplace: Autorky Novotná a Menkyová se na přípravě rukopisy podíleli stejnou mírou. ^*; Neurologická klinika a Centrum klinických neurověd 1. LF UK a VFN v Praze ¹; MSrehab z. s., Praha ²; Klinika rehabilitačního lékařství 1. LF UK a VFN v Praze ³; 2. Neurologická klinika Lékarskej fakulty UK a Univerzitnej nemocnice v Bratislave, Slovensko ⁴; Společné pracoviště biomedicínského inženýrství ČVUT a UK, Praha ⁵
Published in: Cesk Slov Neurol N 2022; 85(2): 110-126
Category: Review Article
doi: https://doi.org/10.48095/cccsnn2022110

Systematický rešeršní článek popisuje výsledky klinických rehabilitačních a fyzioterapeutických studií, které byly primárně zaměřeny na zlepšení rovnováhy u osob s RS. Byly prohledány databáze medicínské literatury PubMed a PEDro za pomoci kombinace těchto klíčových slov: balance, training, exercise, rehabilitation, multiple sclerosis (rovnováha, trénink, cvičení, rehabilitace, roztroušená skleróza). Za účelem rešerše bylo vyhledáno celkem 183 publikovaných klinických studií, z nichž 104 bylo zařazeno. Vyhledané studie byly zaměřené na různé rehabilitační intervence pro zlepšení rovnováhy. Nejčastěji se jednalo o fyzioterapeutické intervence, balanční trénink, silový trénink, trénink chůze a využití virtuální reality nebo robotiky. Nejvíce efektivní jsou programy zacílené na individuální obtíže na základě vyšetření rovnováhy, vedené buď individuální, nebo skupinovou formou. Pro dosažení dostatečného efektu však musí být balanční trénink dostatečně intenzivní.

Overview

This review article summarizes the results from rehabilitation and physiotherapeutic clinical studies with balance intervention in people with MS. The databases of medical literature PubMed and PEDro were searched using a combination of these keywords: balance, training, exercise, rehabilitation, multiple sclerosis. In total 183 papers were screened and 104 papers were included. In available studies, various rehabilitation interventions for balance improvement were used. Most frequently different types of physiotherapeutic approach, balance training, resistance training, gait trainig and virtual reality or robotics. The most effective are balance programs aimed at individual difficulties based on the individual balance assessment or organized in groups. To achieve a sufficient effect, however, balance training must be adequately intensive.

Keywords:

Falls – Multiple sclerosis – balance – rehabilitation– exercise

Sources

1. Kubala Havrdová E, Zápotocká K, Bratrychová V. Roztroušená skleróza. Praha: Mladá fronta 2013.

2. Cameron MH, Lord S. Postural control in multiple sclerosis: implications for fall prevention. Curr Neurol Neurosci Rep 2010; 10(5): 407–412. doi: 10.1007/ s11910-010- 0128-0.

3. Martin CL, Phillips BA, Kilpatrick TJ et al. Gait and balance impairment in early multiple sclerosis in the absence of clinical disability. Mult Scler 2006; 12(5): 620– 628. doi: 10.1177/ 1352458506070658.

4. Shumway-Cook A, Woollacott MH. Motor control: translating research into clinical practice. Lippincott Williams & Wilkins 2007.

5. Mansfield A, Wong JS, McIlroy W et al. Do measures of reactive balance control predict falls in people with stroke returning to the community? Physiotherapy 2015; 101(4): 373–380. doi: 10.1016/ j.physio.2015.01. 009.

6. Berg KO, Wood-Dauphinee SL, Williams JI et al. Measuring balance in the elderly: validation of an instrument. Can J Public Health 1992; 83 (Suppl 2): S7–S11.

7. Godi M, Franchignoni F, Caligari M et al. Comparison of reliability, validity, and responsiveness of the mini-BESTest and Berg Balance Scale in patients with balance disorders. Phys Ther 2013; 93(2): 158–167. doi: 10.2522/ ptj.20120171.

8. Nilsagard Y, Lundholm C, Gunnarsson LG et al. Clinical relevance using timed walk tests and „timed up and go“ testing in persons with multiple sclerosis. Physiother Res Int 2007; 12(2): 105–114. doi: 10.1002/ pri.358.

9. Kalron A, Dolev M, Givon U. Further construct validity of the Timed Up-and-Go Test as a measure of ambulation in multiple sclerosis patients. Eur J Phys Rehabil Med 2017; 53(6): 841–847. doi: 10.23736/ S1973-9087.17.045 99-3.

10. Mancini M, Horak FB. The relevance of clinical balance assessment tools to differentiate balance deficits. Eur J Phys Rehabil Med 2010; 46(2): 239–248.

11. Nilsagard Y, Carling A, Forsberg A. Activities-specific balance confidence in people with multiple sclerosis. Mult Scler Int 2012; 2012: 613925. doi: 10.1155/ 2012/ 613925.

12. van Vliet R, Hoang P, Lord S et al. Falls efficacy scaleinternational: a cross-sectional validation in people with multiple sclerosis. Arch Phys Med Rehabil 2013; 94(5): 883–889. doi: 10.1016/ j.apmr.2012.10.034.

13. Gunn H, Creanor S, Haas B et al. Frequency, characteristics, and consequences of falls in multiple sclerosis: findings from a cohort study. Arch Phys Med Rehabil 2014; 95(3): 538–545. doi: 10.1016/ j.apmr.2013.08.244.

14. Cameron MH, Thielman E, Mazumder R et al. Predicting falls in people with multiple sclerosis: fall history is as accurate as more complex measures. Mult Scler Int 2013; 2013: 496325. doi: 10.1155/ 2013/ 496325.

15. 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): 713–721.

16. Afrasiabifar A, Karami F, Najafi Doulatabad S. Comparing the effect of Cawthorne–Cooksey and Frenkel exercises on balance in patients with multiple sclerosis: a randomized controlled trial. Clin Rehabil 2018; 32(1): 57–65. doi: 10.1177/ 0269215517714592.

17. Brichetto G, Piccardo E, Pedullà L et al. Tailored balance exercises on people with multiple sclerosis: a pilot randomized, controlled study. Multiple Scler 2015; 21(8): 1055–1063. doi: 10.1177/ 1352458514557985.

18. Cattaneo D, Jonsdottir J, Regola A et al. Stabilometric assessment of context dependent balance recovery in persons with multiple sclerosis: a randomized controlled study. J Neuroeng Rehabil 2014; 11(1): 1–7. doi: 10.1186/ 1743-0003-11-100.

19. Cattaneo D, Jonsdottir J, Zocchi M et al. Effects of balance exercises on people with multiple sclerosis: a pilot study. Clin Rehabil 2007; 21(9): 771–781. doi: 10.1177/ 0269215507077602.

20. Cattaneo D, Rasova K, Gervasoni E et al. Falls prevention and balance rehabilitation in multiple sclerosis: a bi-centre randomised controlled trial. Disabil Rehabil 2018; 40(5): 522–526. doi: 10.1080/ 09638288.2016.1258 089.

21. Davies BL, Arpin DJ, Liu M et al. Two different types of high-frequency physical therapy promote improvements in the balance and mobility of persons with multiple sclerosis. Arch Phys Med Rehabil 2016; 97(12): 2095– 2101.e3. doi: 10.1016/ j.apmr.2016.05.024.

22. Fjeldstad-Pardo C, Thiessen A, Pardo G. Telerehabilitation in multiple sclerosis: results of a randomized feasibility and efficacy pilot study. Int J Telerehabil 2018; 10(2): 55–64. doi: 10.5195/ ijt.2018.6256.

23. Gandolfi M, Munari D, Geroin C et al. Sensory integration balance training in patients with multiple sclerosis: a randomized, controlled trial. Mult Scler 2015; 21(11): 1453–1462. doi: 10.1177/ 1352458514562438.

24. Gervasoni E, Cattaneo D, Montesano A et al. Effects of fatigue on balance and mobility in subjects with multiple sclerosis: a brief report. ISRN Neurol 2012; 2012: 316097. doi: 10.5402/ 2012/ 316097.

25. Keser I, Kirdi N, Meric A et al. Comparing routine neurorehabilitation program with trunk exercises based on Bobath concept in multiple sclerosis: pilot study. J Rehabil Res Dev 2013; 50(1): 133–140. doi: 10.1682/ jrrd.2011.12.0231.

26. Negahban H, Rezaie S, Goharpey S. Massage therapy and exercise therapy in patients with multiple sclerosis: a randomized controlled pilot study. Clin Rehabil 2013; 27(12): 1126–1136. doi: 10.1177/ 0269215513491586.

27. Pavlikova M, Cattaneo D, Jonsdottir J et al. The impact of balance specific physiotherapy, intensity of therapy and disability on static and dynamic balance in people with multiple sclerosis: a multi-center prospective study. Multiple Scler Relat Disord 2020; 40: 101974. doi: 10.1016/ j.msard.2020.101974.

28. Prosperini L, Leonardi L, De Carli P et al. Visuo-proprioceptive training reduces risk of falls in patients with multiple sclerosis. Multiple Scler 2010; 16(4): 491–499. doi: 10.1177/ 1352458509359923.

29. Salcı Y, Fil A, Armutlu K et al. Effects of different exercise modalities on ataxia in multiple sclerosis patients: a randomized controlled study. Disabil Rehabil 2017; 39(26): 2626–2632. doi: 10.1080/ 09638288.2016.1236 411.

30. Tramontano M, Martino Cinnera A, Manzari L et al. Vestibular rehabilitation has positive effects on balance, fatigue and activities of daily living in highly disabled multiple sclerosis people: a preliminary randomized controlled trial. Restor Neurol Neurosci 2018; 36(6): 709–718. doi: 10.3233/ RNN-180850.

31. Arntzen EC, Straume B, Odeh F et al. Group-based, individualized, comprehensive core stability and balance intervention provides immediate and long-term improvements in walking in individuals with multiple sclerosis: a randomized controlled trial. Physiother Res Int 2020; 25(1): e1798. doi: 10.1002/ pri.1798.

32. Carling A, Forsberg A, Gunnarsson M et al. CoDuSe group exercise programme improves balance and reduces falls in people with multiple sclerosis: a multi-centre, randomized, controlled pilot study. Multiple Scler 2017; 23(10): 1394–1404. doi: 10.1177/ 1352458516677591.

33. Cattaneo D, Gervasoni E, Pupillo E et al. Educational and exercise intervention to prevent falls and improve participation in subjects with neurological conditions: the NEUROFALL randomized controlled trial. Front Neurol 2019; 10: 865. doi: 10.3389/ fneur.2019.00 865.

34. Gunn H, Andrade J, Paul L et al. A self-management programme to reduce falls and improve safe mobility in people with secondary progressive MS: the BRiMS feasibility RCT. Health Technol Assess 2019; 23(27): 1–166. doi: 10.3310/ hta23270.

35. Hebert JR, Corboy JR, Vollmer T et al. Efficacy of balance and eye-movement exercises for persons with multiple sclerosis (BEEMS). Neurology 2018; 90(9): e797–e807. doi: 10.1212/ WNL.0000000000005013.

36. Ozkul C, Guclu-Gunduz A, Eldemir K et al. Effect of task-oriented circuit training on motor and cognitive performance in patients with multiple sclerosis: a singleblinded randomized controlled trial. NeuroRehabilitation 2020; 46(3): 343–353. doi: 10.3233/ NRE-203029.

37. Straudi S, Martinuzzi C, Pavarelli C et al. A taskoriented circuit training in multiple sclerosis: a feasibility study. BMC Neurol 2014; 14(1): 124. doi: 10.1186/ 1471- 2377-14-124.

38. Tarakci E, Yeldan I, Huseyinsinoglu BE et al. Group exercise training for balance, functional status, spasticity, fatigue and quality of life in multiple sclerosis: a randomized controlled trial. Clin Rehabil 2013; 27(9): 813–822.

39. Aidar FJ, Carneiro AL, Costa Moreira O et al. Effects of resistance training on the physical condition of people with multiple sclerosis. J Sports Med Phys Fitness 2018; 58(7–8): 1127–1134. doi: 10.23736/ S0022-4707.17.07621-6.

40. Amiri B, Sahebozamani M, Sedighi B. The effects of 10-week core stability training on balance in women with multiple sclerosis according to Expanded Disability Status Scale: a single-blinded randomized controlled trial. Eur J Phys Rehabil Med 2019; 55(2): 199–208. doi: 10.23736/ S1973-9087.18.04778-0.

41. Cakit BD, Nacir B, Genç H et al. Cycling progressive resistance training for people with multiple sclerosis: a randomized controlled study. Am J Phys Med Rehabil 2010; 89(6): 446–457. doi: 10.1097/ PHM.0b013e3181d3e71f.

42. Callesen J, Cattaneo D, Brincks J et al. How do resistance training and balance and motor control training affect gait performance and fatigue impact in people with multiple sclerosis? A randomized controlled multi-center study. Mult Scler 2020; 26(11): 1420–1432. doi: 10.1177/ 1352458519865740.

43. Coote S, Hughes L, Rainsford G et al. Pilot randomized trial of progressive resistance exercise augmented by neuromuscular electrical stimulation for people with multiple sclerosis who use walking aids. Arch Phys Med Rehabil 2015; 96(2): 197–204. doi: 10.1016/ j.apmr.2014.09.021.

44. DeBolt LS, McCubbin JA. The effects of home-based resistance exercise on balance, power, and mobility in adults with multiple sclerosis. Arch Phys Med Rehabil 2004; 85(2): 290–297. doi: 10.1016/ j.apmr.2003.06.003.

45. Eftekhari E, Mostahfezian M, Etemadifar M et al. Resistance training and vibration improve muscle strength and functional capacity in female patients with multiple sclerosis. Asian J Sports Med 2012; 3(4): 279–284. doi: 10.5812/ asjsm.34552.

46. Hayes HA, Gappmaier E, LaStayo PC. Effects of highintensity resistance training on strength, mobility, balance, and fatigue in individuals with multiple sclerosis: a randomized controlled trial. J Neurol Phys Ther 2011; 35(1): 2–10. doi: 10.1097/ NPT.0b013e31820b5a9d.

47. Tavazzi E, Bergsland N, Cattaneo D et al. Effects of motor rehabilitation on mobility and brain plasticity in multiple sclerosis: a structural and functional MRI study. J Neurol 2018; 265(6): 1393–1401. doi: 10.1007/ s00415- 018-8859-y.

48. Moradi M, Sahraian MA, Aghsaie A et al. Effects of eight-week resistance training program in men with multiple sclerosis. Asian J Sports Med 2015; 6(2): e22838. doi: 10.5812/ asjsm.6(2)2015.22838.

49. Huisinga JM, Filipi ML, Stergiou N. Supervised resistance training results in changes in postural control in patients with multiple sclerosis. Motor Control 2012; 16(1): 50–63. doi: 10.1123/ mcj.16.1.50.

50. Learmonth Y, Paul L, Miller L et al. The effects of a 12- week leisure centre-based, group exercise intervention for people moderately affected with multiple sclerosis: a randomized controlled pilot study. Clin Rehabil 2012; 26(7): 579–593. doi: 10.1177/ 0269215511423946.

51. 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): 2034–2038. doi: 10.1212/ 01.wnl.0000145761.38400.65.

52. Sabapathy NM, Minahan CL, Turner GT et al. Comparing endurance- and resistance-exercise training in people with multiple sclerosis: a randomized pilot study. Clin Rehabil 2011; 25(1): 14–24. doi: 10.1177/ 0269215510375908.

53. Sangelaji B, Nabavi SM, Estebsari F et al. Effect of combination exercise therapy on walking distance, postural balance, fatigue and quality of life in multiple sclerosis patients: a clinical trial study. Iran Red Crescent Med J 2014; 16(6): e17173. doi: 10.5812/ ircmj.17173.

54. Sangelaji B, Kordi M, Banihashemi F et al. A combined exercise model for improving muscle strength, balance, walking distance, and motor agility in multiple sclerosis doi: 10.1177/ 0269215513481047. patients: a randomized clinical trial. Iran J Neurol 2016; 15(3): 111–120.

55. Grazioli E, Tranchita E, Borriello G et al. The effects of concurrent resistance and aerobic exercise training on functional status in patients with multiple sclerosis. Curr Sports Med Rep 2019; 18(12): 452–457. doi: 10.1249/ JSR.0000000000000661.

56. Ahmadi A, Arastoo AA, Nikbakht M. The effects of a treadmill training programme on balance, speed and endurance walking, fatigue and quality of life in people with multiple sclerosis. Int SportMed J 2010; 11(4): 389– 397.

57. Brændvik SM, Koret T, Helbostad JL et al. Treadmill training or progressive strength training to improve walking in people with multiple sclerosis? A randomized parallel group trial. Physiother Res Int 2016; 21(4): 228– 236. doi: 10.1002/ pri.1636.

58. Jonsdottir J, Gervasoni E, Bowman T et al. Intensive multimodal training to improve gait resistance, mobility, balance and cognitive function in persons with multiple sclerosis: a pilot randomized controlled trial. Front Neurol 2018; 9: 800. doi: 10.3389/ fneur.2018.00800.

59. Kalron A, Fonkatz I, Frid L et al. The effect of balance training on postural control in people with multiple sclerosis using the CAREN virtual reality system: a pilot randomized controlled trial. J Neuroeng Rehabil 2016; 13(1): 13. doi: 10.1186/ s12984-016-0124-y.

60. Monjezi S, Negahban H, Tajali S et al. Effects of dualtask balance training on postural performance in patients with multiple sclerosis: a double-blind, randomized controlled pilot trial. Clin Rehabil 2017; 31(2): 234–241. doi: 10.1177/ 0269215516639735.

61. Peruzzi A, Zarbo IR, Cereatti A et al. An innovative training program based on virtual reality and treadmill: effects on gait of persons with multiple sclerosis. Disabil Rehabil 2017; 39(15): 1557–1563. doi: 10.1080/ 09638288.2016.1224935.

62. Prokopiusova T, Pavlikova M, Markova M et al. Randomized comparison of functional electric stimulation in posturally corrected position and motor program activating therapy: treating foot drop in people with multiple sclerosis. Eur J Phys Rehabil Med 2020; 56(4): 394– 402. doi: 10.23736/ S1973-9087.20.06104-3.

63. Samaei A, Bakhtiary AH, Hajihasani A et al. Uphill and downhill walking in multiple sclerosis: a randomized controlled trial. Int J MS Care 2016; 18(1): 34–41. doi: 10.7224/ 1537-2073.2014-072.

64. Sosnoff JJ, Wajda DA, Sandroff BM et al. Dual task training in persons with multiple sclerosis: a feasability randomized controlled trial. Clin Rehabil 2017; 31(10): 1322–1331. doi: 10.1177/ 0269215517698028.

65. Veldkamp R, Baert I, Kalron A et al. Structured cognitive- motor dual task training compared to single mobility training in persons with multiple sclerosis, a multicenter RCT. J Clin Med 2019; 8(12): 2177. doi: 10.3390/ jcm8122177.

66. Calabrò RS, Russo M, Naro A et al. Robotic gait training in multiple sclerosis rehabilitation: can virtual reality make the difference? Findings from a randomized controlled trial. J Neurol Sci 2017; 377: 25–30. doi: 10.1016/ j. jns.2017.03.047.

67. Gandolfi M, Geroin C, Picelli A et al. Robot-assisted vs. sensory integration training in treating gait and balance dysfunctions in patients with multiple sclerosis: a randomized controlled trial. Front Hum Neurosci 2014; 8: 318. doi: 10.3389/ fnhum.2014.00318.

68. McGibbon CA, Sexton A, Jayaraman A et al. Evaluation of the Keeogo exoskeleton for assisting ambulatory activities in people with multiple sclerosis: an open-label, randomized, cross-over trial. J Neuroeng Rehabil 2018; 15(1): 117. doi: 10.1186/ s12984-018-0468-6.

69. Munari D, Fonte C, Varalta V et al. Effects of robotassisted gait training combined with virtual reality on motor and cognitive functions in patients with multiple sclerosis: a pilot, single-blind, randomized controlled trial. Restor Neurol Neurosci 2020; 38(2): 151–164. doi: 10.3233/ RNN-190974.

70. Ruiz J, Labas MP, Triche EW et al. Combination of robot- assisted and conventional body-weight-supported treadmill training improves gait in persons with multiple sclerosis: a pilot study. J Neurol Phys Ther 2013; 37(4): 187– 193. doi: 10.1097/ NPT.0000000000000018.

71. Russo M, Dattola V, De Cola MC et al. The role of robotic gait training coupled with virtual reality in boosting the rehabilitative outcomes in patients with multiple sclerosis. Int J Rehabil Res 2018; 41(2): 166–172. doi: 10.1097/ MRR.0000000000000270.

72. Schwartz I, Sajin A, Moreh E et al. Robot-assisted gait training in multiple sclerosis patients: a randomized trial. Mult Scler 2012; 18(6): 881–890. doi: 10.1177/ 1352458511431075.

73. Straudi S, Fanciullacci C, Martinuzzi C et al. The effects of robot-assisted gait training in progressive multiple sclerosis: a randomized controlled trial. Mult Scler 2016; 22(3): 373–384. doi: 10.1177/ 1352458515620933.

74. Straudi S, Manfredini F, Lamberti N et al. Robot-assisted gait training is not superior to intensive overground walking in multiple sclerosis with severe disability (the RAGTIME study): a randomized controlled trial. Mult Scler 2020; 26(6): 716–724. doi: 10.1177/ 1352458519833901.

75. Vaney C, Gattlen B, Lugon-Moulin V et al. Robotic-assisted step training (lokomat) not superior to equal intensity of over-ground rehabilitation in patients with multiple sclerosis. Neurorehabil Neural Rep 2012; 26(3): 212–221. doi: 10.1177/ 1545968311425923.

76. Abbasi M, Yoosefinejad AK, Poursadeghfard M et al. Whole body vibration improves core muscle strength and endurance in ambulant individuals with multiple sclerosis: a randomized clinical trial. Mult Scler Relat Disord 2019; 32: 88–93. doi: 10.1016/ j.msard.2019.04.028.

77. Broekmans T, Roelants M, Alders G et al. Exploring the effects of a 20-week whole-body vibration training programme on leg muscle performance and function in persons with multiple sclerosis. J Rehabil Med 2010; 42(9): 866–872. doi: 10.2340/ 16501977-0609.

78. Claerbout M, Gebara B, Ilsbroukx S et al. Effects of 3 weeks’ whole body vibration training on muscle strength and functional mobility in hospitalized persons with multiple sclerosis. Mult Scler 2012; 18(4): 498–505. doi: 10.1177/ 1352458511423267.

79. Ebrahimi A, Eftekhari E, Etemadifar M. Effects of whole body vibration on hormonal & functional indices in patients with multiple sclerosis. IndianJ MedRes2015; 142(4): 450–458. doi: 10.4103/ 0971-5916.169 210.

80. Freitas ED, Frederiksen C, Miller RM et al. Acute and chronic effects of whole-body vibration on balance, postural stability, and mobility in women with multiple sclerosis. Dose Response 2018; 16(4): 1559325818816577. doi: 10.1177/ 1559325818816577.

81. Hilgers C, Mündermann A, Riehle H et al. Effects of whole-body vibration training on physical function in patients with multiple sclerosis. NeuroRehabilitation 2013; 32(3): 655–663. doi: 10.3233/ NRE-130888.

82. Krause A, Lee K, Freyler K et al. Whole-body vibration impedes the deterioration of postural control in patients with multiple sclerosis. Mult Scler Relat Disord 2019; 31: 134–140. doi: 10.1016/ j.msard.2019.03.026.

83. Schyns F, Paul L, Finlay K et al. Vibration therapy in multiple sclerosis: a pilot study exploring its effects on tone, muscle force, sensation and functional performance. Clin Rehabil 2009; 23(9): 771–781. doi: 10.1177/ 0269215508101758.

84. Uszynski MK, Purtill H, Donnelly A et al. Comparing the effects of whole-body vibration to standard exercise in ambulatory people with multiple sclerosis: a randomised controlled feasibility study. Clin Rehabil 2016; 30(7): 657–668. doi: 10.1177/ 0269215515595522.

85. Wolfsegger T, Assar H, Topakian R. 3-week whole body vibration does not improve gait function in mildly affected multiple sclerosis patients – a randomized controlled trial. J Neurol Sci 2014; 347(1–2): 119–123. doi: 10.1016/ j.jns.2014.09.030.

86. Eftekhari E, Mostahfezian M, Etemadifar M et al. Resistance training and vibration improve muscle strength and functional capacity in female patients with multiple sclerosis. Asian J Sports Med 2012; 3(4): 279–284. doi: 10.5812/ asjsm.34552.

87. Brichetto G, Spallarossa P, de Carvalho MLL et al. The effect of Nintendo® Wii® on balance in people with multiple sclerosis: a pilot randomized control study. Mult Scler 2013; 19(9): 1219–1221. doi: 10.1177/ 1352458512472747.

88. Hoang P, Schoene D, Gandevia S et al. Effects of a home-based step training programme on balance, stepping, cognition and functional performance in people with multiple sclerosis – a randomized controlled trial. Mult Scler 2016; 22(1): 94–103. doi: 10.1177/ 1352458515579442.

89. Khalil H, Al-Sharman A, El-Salem K et al. The development and pilot evaluation of virtual reality balance scenarios in people with multiple sclerosis (MS): a feasibility study. NeuroRehabilitation 2018; 43(4): 473–482. doi: 10.3233/ NRE-182471.

90. Kramer A, Dettmers C, Gruber M. Exergaming with additional postural demands improves balance and gait in patients with multiple sclerosis as much as conventional balance training and leads to high adherence to home-based balance training. Arch Phys Med Rehabil 2014; 95(10): 1803–1809. doi: 10.1016/ j.apmr.2014.04.020.

91. Nilsagård YE, Forsberg AS, von Koch L. Balance exercise for persons with multiple sclerosis using Wii games: a randomised, controlled multi-centre study. Mult Scler 2013; 19(2): 209–216. doi: 10.1177/ 1352458512450088.

92. Prosperini L, Fanelli F, Petsas N et al. Multiple sclerosis: changes in microarchitecture of white matter tracts after training with a video game balance board. Radiology 2014; 273(2): 529–538. doi: 10.1148/ radiol.14140168.

93. Prosperini L, Fortuna D, Giannì C et al. Home-based balance training using the Wii balance board: a randomized, crossover pilot study in multiple sclerosis. Neurorehabil Neural Repair 2013; 27(6): 516–525. doi: 10.1177/ 1545968313478484.

94. Robinson J, Dixon J, Macsween A et al. The effects of exergaming on balance, gait, technology acceptance and flow experience in people with multiple sclerosis: a randomized controlled trial. BMC Sports Sci Med Rehabil 2015; 7(1): 8. doi: 10.1186/ s13102-015-0001-1.

95. Thomas S, Fazakarley L, Thomas PW et al. Mii-vitaliSe: a pilot randomised controlled trial of a home gaming system (Nintendo Wii) to increase activity levels, vitality and well-being in people with multiple sclerosis. BMJ Open 2017; 7(9): e016966. doi: 10.1136/ bmjopen- 2017-016966.

96. Yazgan YZ, Tarakci E, Tarakci D et al. Comparison of the effects of two different exergaming systems on balance, functionality, fatigue, and quality of life in people with multiple sclerosis: a randomized controlled trial. Mult Scler Relat Disord 2020; 39: 101902. doi: 10.1016/ j. msard.2019.101902.

97. Conroy SS, Zhan M, Culpepper WJ et al. Self-directed exercise in multiple sclerosis: evaluation of a home automated tele-management system. J Telemed Telecare 2018; 24(6): 410–419. doi: 10.1177/ 1357633X17702757.

98. McAuley E, Wójcicki TR, Learmonth YC et al. Effects of a DVD-delivered exercise intervention on physical function in older adults with multiple sclerosis: a pilot randomized controlled trial. Mult Scler J Exp Transl Clin 2015; 1: 2055217315584838. doi: 10.1177/ 2055217315584838.

99. Novotna K, Janatova M, Hana K et al. Biofeedback based home balance training can improve balance but not gait in people with multiple sclerosis. Mult Scler Int 2019; 2019: 2854130. doi: 10.1155/ 2019/ 2854130.

100. Pfalzer L, Fry D. Effects of a 10-week inspiratory muscle training program on lower-extremity mobility in people with multiple sclerosis: a randomized controlled trial. Int J MS Care 2011; 13(1): 32–42. doi: 10.7224/ 1537- 2073-13.1.32.

101. Sosnoff JJ, Moon Y, Wajda DA et al. Fall risk and incidence reduction in high risk individuals with multiple sclerosis: a pilot randomized control trial. Clin Rehabil 2015; 29(10): 952–960. doi: 10.1177/ 0269215514564899.

102. Sosnoff JJ, Finlayson M, McAuley E et al. Homebased exercise program and fall-risk reduction in older adults with multiple sclerosis: phase 1 randomized controlled trial. Clin Rehabil 2014; 28(3): 254–263. doi: 10.1177/ 0269215513501092.

103. Abasıyanık Z, Ertekin Ö, Kahraman T et al. The effects of clinical pilates training on walking, balance, fall risk, respiratory, and cognitive functions in persons with multiple sclerosis: a randomized controlled trial. Explore 2020; 16(1): 12–20. doi: 10.1016/ j.explore.2019.07.010.

104. Duff WRD, Andrushko JW, Renshaw DW et al. Impact of pilates exercise in multiple sclerosis: a randomized controlled trial. Int J MS Care 2018; 20(2): 92–100. doi: 10.7224/ 1537-2073.2017-066.

105. Fox EE, Hough AD, Creanor S et al. Effects of pilatesbased core stability training in ambulant people with multiple sclerosis: multicenter, assessor-blinded, randomized controlled trial. Phys Ther 2016; 96(8): 1170–1178. doi: 10.2522/ ptj.20150166.

106. Guclu-Gunduz A, Citaker S, Irkec C et al. The effects of pilates on balance, mobility and strength in patients with multiple sclerosis. NeuroRehabilitation 2014; 34(2): 337–342. doi: 10.3233/ NRE-130957.

107. Kalron A, Rosenblum U, Frid L et al. Pilates exercise training vs. physical therapy for improving walking and balance in people with multiple sclerosis: a randomized controlled trial. Clin Rehabil 2017; 31(3): 319–328. doi: 10.1177/ 0269215516637202.

108. Marandi SM, Nejad VS, Shanazari Z et al. A comparison of 12 weeks of pilates and aquatic training on the dynamic balance of women with mulitple sclerosis. Int J Prev Med 2013; 4(Suppl 1): S110–117.

109. Leonard G, Lapierre Y, Chen J-K et al. Noninvasive tongue stimulation combined with intensive cognitive and physical rehabilitation induces neuroplastic changes in patients with multiple sclerosis: a multimodal neuroimaging study. Mult Scler J Exp Transl Clin 2017; 3(1): 2055217317690561. doi: 10.1177/ 2055217317690561.

110. Burschka JM, Keune PM, Hofstadt-van Oy U et al. Mindfulness-based interventions in multiple sclerosis: beneficial effects of Tai Chi on balance, coordination, fatigue and depression. BMC Neurol 2014; 14(1): 165. doi: 10.1186/ s12883-014-0165-4.

111. Ultramari VRLM, Calvo APC, Rodrigues RAS et al. Physical and functional aspects of persons with multiple sclerosis practicing Tai-Geiko: randomized trial. Clinics 2020; 75: e1272. doi: 10.6061/ clinics/ 2020/ e1272.

112. de Oliveira G, Fernandes MdCCG, de Faria Oliveira JD et al. Yoga training has positive effects on postural balance and its influence on activities of daily living in people with multiple sclerosis: a pilot study. Explore 2016; 12(5): 325–332. doi: 10.1016/ j.explore.2016.06.005.

113. Stephens J, DuShuttle D, Hatcher C et al. Use of awareness through movement improves balance and balance confidence in people with multiple sclerosis: a randomized controlled study. Neurol Rep 2001; 25(2): 39–49.

114. Silkwood-Sherer D, Warmbier H. Effects of hippotherapy on postural stability, in persons with multiple sclerosis: a pilot study. J Neurol Phys Ther 2007; 31(2): 77– 84. doi: 10.1097/ NPT.0b013e31806769f7.

115. Aidar FJ, Gama de Matos D, de Souza RF et al. Influence of aquatic exercises in physical condition in patients with multiple sclerosis. J Sports Med Phys Fitness 2018; 58(5): 684–689. doi: 10.23736/ S0022-4707.17.07151- 1.

116. Gurpinar B, Kara B, Idiman E. Effects of aquatic exercises on postural control and hand function in multiple sclerosis: Halliwick versus Aquatic plyometric exercises: a randomised trial. J Musculoskelet Neuronal Interact 2020; 20(2): 249–255.

117. Kargarfard M, Shariat A, Ingle L et al. Randomized controlled trial to examine the impact of aquatic exercise training on functional capacity, balance, and perceptions of fatigue in female patients with multiple sclerosis. Arch Phys Med Rehabil 2018; 99(2): 234–241. doi: 10.1016/ j.apmr.2017.06.015.

118. Marandi SM, Nejad VS, Shanazari Z et al. A comparison of 12 weeks of pilates and aquatic training on the dynamic balance of women with mulitple sclerosis. Int J Prev Med 2013; 4 (Suppl 1): S110–S117.

119. Sanders EA, Arts RJ. Paraesthesiae in multiple sclerosis. J Neurol Sci 1986; 74(2–3): 297–305. doi: 10.1016/ 0022- 510x(86)90115-2.

120. Merchut MP, Gruener G. Quantitative sensory threshold testing in patients with multiple sclerosis. Electromyogr Clin Neurophysiol 1993; 33(2): 119–124.

121. Kelleher KJ, Spence WD, Solomonidis SE et al. The effect of impaired plantar sensation on gait in people with multiple sclerosis. Int J MS Care 2009; 11(1): 25–31.

122. Citaker S, Gunduz AG, Guclu MB et al. Relationship between foot sensation and standing balance in patients with multiple sclerosis. Gait Posture 2011; 34(2): 275–278. doi: 10.1016/ j.gaitpost.2011.05.015.

123. Roeing KL, Wajda DA, Sosnoff JJ. Time dependent structure of postural sway in individuals with multiple sclerosis. Gait Posture 2016; 48: 19–23. doi: 10.1016/ j.gaitpost. 2016.04.023.

124. Jamali A, Sadeghi-Demneh E, Fereshtenajad N et al. Somatosensory impairment and its association with balance limitation in people with multiple sclerosis. Gait Posture 2017; 57: 224–229. doi: 10.1016/ j. gaitpost.2017.06.020.

125. Kanekar N, Lee YJ, Aruin AS. Effect of light finger touch in balance control of individuals with multiple sclerosis. Gait Posture 2013; 38(4): 643–647. doi: 10.1016/ j. gaitpost.2013.02.017.

126. Mulligan H, Treharne GJ, Hale LA et al. Combining self-help and professional help to minimize barriers to physical activity in persons with multiple sclerosis: a trial of the „Blue Prescription“ approach in New Zealand. J Neurol Phys Ther 2013; 37(2): 51–57. doi: 10.1097/ NPT.0b013e318292799e.

127. Sherrington C, Whitney JC, Lord SR et al. Effective exercise for the prevention of falls: a systematic review and meta-analysis. J Am Geriatr Soc 2008; 56(12): 2234– 2243. doi: 10.1111/ j.1532-5415.2008.02014.x.

128. Nilsagård Y, Lundholm C, Denison E et al. Predicting accidental falls in people with multiple sclerosis – a longitudinal study. Clin Rehabil 2009; 23(3): 259–269. doi: 10.1177/ 0269215508095087.

129. Coote S, Hughes L, Rainsford G et al. Pilot randomized trial of progressive resistance exercise augmented by neuromuscular electrical stimulation for people with multiple sclerosis who use walking aids. Arch Phys Med Rehabil 2015; 96(2): 197–204. doi: 10.1016/ j.apmr.2014.09.021.