Investigation of Fatigability during Repetitive Robot-Mediated Arm Training in People with Multiple Sclerosis

Background People with multiple sclerosis (MS) are encouraged to engage in exercise programs but an increased experience of fatigue may impede sustained participation in training sessions. A high number of movements is, however, needed for obtaining optimal improvements after rehabilitation. Methods This cross-sectional study investigated whether people with MS show abnormal fatigability during a robot-mediated upper limb movement trial. Sixteen people with MS and sixteen healthy controls performed five times three minutes of repetitive shoulder anteflexion movements. Movement performance, maximal strength, subjective upper limb fatigue and surface electromyography (median frequency and root mean square of the amplitude of the electromyography (EMG) signal of the anterior deltoid) were recorded during or in-between these exercises. After fifteen minutes of rest, one extra movement bout was performed to investigate how rest influences performance. Results A fifteen minutes upper limb movement protocol increased the perceived upper limb fatigue and induced muscle fatigue, given a decline in maximal anteflexion strength and changes of both the amplitude and the median frequency of EMG the anterior deltoid. In contrast, performance during the 3 minutes of anteflexion movements did not decline. There was no relation between changes in subjective fatigue and the changes in the amplitude and the median frequency of the anterior deltoid muscle, however, there was a correlation between the changes in subjective fatigue and changes in strength in people with MS. People with MS with upper limb weakness report more fatigue due to the repetitive movements, than people with MS with normal upper limb strength, who are comparable to healthy controls. The weak group could, however, keep up performance during the 15 minutes of repetitive movements. Discussion and Conclusion Albeit a protocol of repetitive shoulder anteflexion movements did not elicit a performance decline, fatigue feelings clearly increased in both healthy controls and people with MS, with the largest increase in people with MS with upper limb weakness. Objective fatigability was present in both groups with a decline in the muscle strength and increase of muscle fatigue, shown by changes in the EMG parameters. However, although weak people with multiple sclerosis experienced more fatigue, the objective signs of fatigability were less obvious in weak people with MS, perhaps because this subgroup has central limiting factors, which influence performance from the start of the movements.

[1]  J. Fridén,et al.  Intramuscular pressure and electromyographic responses of the vastus lateralis muscle during repeated maximal isokinetic knee extensions. , 2000, Acta physiologica Scandinavica.

[2]  C. D. De Luca,et al.  Myoelectrical manifestations of localized muscular fatigue in humans. , 1984, Critical reviews in biomedical engineering.

[3]  M. Ferrarin,et al.  Robot Training of Upper Limb in Multiple Sclerosis: Comparing Protocols With or WithoutManipulative Task Components , 2012, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[4]  W. L. Benedict,et al.  Multiple Sclerosis , 2007, Journal - Michigan State Medical Society.

[5]  K. Coninx,et al.  Facilitating robot-assisted training in MS patients with arm paresis: A procedure to individually determine gravity compensation , 2011, 2011 IEEE International Conference on Rehabilitation Robotics.

[6]  R. Queen,et al.  Isokinetic testing of biceps strength and endurance in dominant versus nondominant upper extremities. , 2010, Journal of shoulder and elbow surgery.

[7]  C Trenkwalder,et al.  Fatigue in multiple sclerosis: a comparison of different rating scales and correlation to clinical parameters , 2002, Multiple sclerosis.

[8]  Karin Coninx,et al.  Development of Activity-Related Muscle Fatigue during Robot-Mediated Upper Limb Rehabilitation Training in Persons with Multiple Sclerosis: A Pilot Trial , 2015, Multiple sclerosis international.

[9]  Stuart M Phillips,et al.  Bigger weights may not beget bigger muscles: evidence from acute muscle protein synthetic responses after resistance exercise. , 2012, Applied physiology, nutrition, and metabolism = Physiologie appliquee, nutrition et metabolisme.

[10]  G. Cutter,et al.  Natural history of multiple sclerosis symptoms. , 2013, International journal of MS care.

[11]  K. Coninx,et al.  Robot-supported upper limb training in a virtual learning environment : a pilot randomized controlled trial in persons with MS , 2015, Journal of NeuroEngineering and Rehabilitation.

[12]  Inge Zijdewind,et al.  Fatigue Perceived by Multiple Sclerosis Patients Is Associated With Muscle Fatigue , 2012, Neurorehabilitation and neural repair.

[13]  Karin Coninx,et al.  Adaptive Personalized Training Games for Individual and Collaborative Rehabilitation of People with Multiple Sclerosis , 2014, BioMed research international.

[14]  Tommy Öberg,et al.  Electromyogram mean power frequency in non-fatigued trapezius muscle , 2004, European Journal of Applied Physiology and Occupational Physiology.

[15]  Stephan Konz Work/rest: Part I Guidelines for the practitioner 1 The recommendations provided in this guide are , 1998 .

[16]  J Goldhahn,et al.  Age- and Gender-Specific Normative Data of Grip and Pinch Strength in a Healthy Adult Swiss Population , 2009, The Journal of hand surgery, European volume.

[17]  Arja Virtanen,et al.  Assessment of muscle strength and motor fatigue with a knee dynamometer in subjects with multiple sclerosis: a new fatigue index , 2004, Clinical rehabilitation.

[18]  M. Zwarts,et al.  Clinical neurophysiology of fatigue , 2008, Clinical Neurophysiology.

[19]  S. Hunter,et al.  Sex differences in human fatigability: mechanisms and insight to physiological responses , 2014, Acta physiologica.

[20]  The specificity of fatiguing protocols affects scapular orientation: Implications for subacromial impingement. , 2011, Clinical biomechanics.

[21]  Bruce H Dobkin,et al.  Fatigue Versus Activity-Dependent Fatigability in Patients With Central or Peripheral Motor Impairments , 2008, Neurorehabilitation and neural repair.

[22]  Serge H. Roy,et al.  Median frequency of the myoelectric signal , 2004, European Journal of Applied Physiology and Occupational Physiology.

[23]  Davide Cattaneo,et al.  Unilateral and bilateral upper limb dysfunction at body functions, activity and participation levels in people with multiple sclerosis , 2015, Multiple sclerosis.

[24]  H. Hermens,et al.  SENIAM 8: European recommendations for surface electromyography , 1999 .

[25]  Ilse Lamers,et al.  Perceived and actual arm performance in multiple sclerosis: relationship with clinical tests according to hand dominance , 2013, Multiple sclerosis.

[26]  L. Grevendonk,et al.  Multiple Sclerosis Affects Skeletal Muscle Characteristics , 2014, PloS one.

[27]  S. Brauer,et al.  Interventions to promote upper limb recovery in stroke survivors with severe paresis: a systematic review , 2010, Disability and rehabilitation.

[28]  G. Moonen,et al.  Motor Fatigue Measurement by Distance-Induced Slow Down of Walking Speed in Multiple Sclerosis , 2012, PloS one.

[29]  P. Feys,et al.  The Armeo Spring as training tool to improve upper limb functionality in multiple sclerosis: a pilot study , 2011, Journal of NeuroEngineering and Rehabilitation.

[30]  H. Hermens,et al.  European recommendations for surface electromyography: Results of the SENIAM Project , 1999 .

[31]  Kimberly Szucs,et al.  Scapular muscle activation and co-activation following a fatigue task , 2009, Medical & Biological Engineering & Computing.

[32]  A Achiron,et al.  Fatigue in multiple sclerosis compared with chronic fatigue syndrome , 1996, Neurology.

[33]  Ilse Lamers,et al.  Hand grip fatigability in persons with multiple sclerosis according to hand dominance and disease progression. , 2015, Journal of rehabilitation medicine.

[34]  Richard W. Bohannon Hand-grip dynamometry provides a valid indication of upper extremity strength impairment in home care patients. , 1998, Journal of Hand Therapy.

[35]  H. J. Hansen,et al.  Fatigue, mood and quality of life improve in MS patients after progressive resistance training , 2010, Multiple sclerosis.

[36]  Karen V. Lomond,et al.  Posture-movement changes following repetitive motion-induced shoulder muscle fatigue. , 2009, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[37]  Mario Cifrek,et al.  Surface EMG based muscle fatigue evaluation in biomechanics. , 2009, Clinical biomechanics.

[38]  Neville Hogan,et al.  Robotic Therapy: The Tipping Point , 2012, American journal of physical medicine & rehabilitation.

[39]  Ilse Lamers,et al.  Upper limb assessment in multiple sclerosis: a systematic review of outcome measures and their psychometric properties. , 2014, Archives of physical medicine and rehabilitation.

[40]  M. Pozzo,et al.  Relationship between perceived exertion and mean power frequency of the EMG signal from the upper trapezius muscle during isometric shoulder elevation , 2005, European Journal of Applied Physiology.

[41]  Guy Nagels,et al.  Assessing fatigue in multiple sclerosis: Dutch modified fatigue impact scale. , 2003, Acta neurologica Belgica.

[42]  Anneke Steens,et al.  Mechanisms underlying muscle fatigue differ between multiple sclerosis patients and controls: A combined electrophysiological and neuroimaging study , 2012, NeuroImage.

[43]  S. Pandya,et al.  Cortical motor reorganization after paraplegia , 1999, Neurology.

[44]  Annegret Mündermann,et al.  Objective assessment of motor fatigue in multiple sclerosis using kinematic gait analysis: a pilot study , 2011, Journal of NeuroEngineering and Rehabilitation.

[45]  Roger M Enoka,et al.  Fatigue and fatigability in neurologic illnesses , 2013, Neurology.

[46]  Niels Birbaumer,et al.  Neurophysiology of Robot-Mediated Training and Therapy: A Perspective for Future Use in Clinical Populations , 2013, Front. Neurol..

[47]  R. Enoka,et al.  Handedness but not dominance influences variability in endurance time for sustained, submaximal contractions. , 2012, Journal of neurophysiology.

[48]  G. Thickbroom,et al.  Central motor drive and perception of effort during fatigue in multiple sclerosis , 2006, Journal of Neurology.