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Journal of NeuroEngineering and Rehabilitation
Published in: Journal of NeuroEngineering and Rehabilitation 1/2019

Open Access 01-12-2019 | Ultrasound | Research

Long-term use of implanted peroneal functional electrical stimulation for stroke-affected gait: the effects on muscle and motor nerve

Authors: Frank Berenpas, Vivian Weerdesteyn, Alexander C. Geurts, Nens van Alfen

Published in: Journal of NeuroEngineering and Rehabilitation | Issue 1/2019

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Abstract

Background

Peripheral changes to muscle and motor nerves occur following stroke, which may further impair functional capacity. We investigated whether a year-long use of an implanted peroneal FES system reverses stroke-related changes in muscles and motor nerves in people with foot drop in the chronic phase after supratentorial stroke.

Methods

Thirteen persons with a chronic stroke (mean age 56.1 years, median Fugl-Meyer Assessment leg score 71%) were included and received an implanted peroneal FES system (ActiGait®). Quantitative muscle ultrasound (QMUS) images were obtained bilaterally from three leg muscles (i.e. tibialis anterior, rectus femoris, gastrocnemius). Echogenicity (muscle ultrasound gray value) and muscle thickness were assessed over a one-year follow-up and compared to age-, sex-, height- and weight-corrected reference values. Compound motor action potentials (CMAPs) and motor evoked potentials (MEPs) were obtained from the tibialis anterior muscle. Generalized estimated equation modeling was used to assess changes in QMUS, CMAPs and MEPs outcomes over the follow-up period.

Results

Echogenicity of the tibialis anterior decreased significantly during the follow-up on the paretic side. Z-scores changed from 0.88 at baseline to − 0.15 after 52 weeks. This was accompanied by a significant increase in muscle thickness on the paretic side, where z-scores changed from − 0.32 at baseline to 0.48 after 52 weeks. Echogenicity of the rectus femoris normalized on both the paretic and non-paretic side (z-scores changed from − 1.09 and − 1.51 to 0.14 and − 0.49, respectively). Amplitudes of CMAP and MEP (normalized to CMAP) were reduced during follow-up, particularly on the paretic side (ΔCMAP = 20% and ΔMEP = 14%).

Conclusions

We show that the structural changes to muscles following stroke are reversible with FES and that these changes might not be limited to electrically stimulated muscles. No evidence for improvement of the motor nerves was found.
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Literature
1.
Benecke R, Berthold A, Conrad B. Denervation activity in the EMG of patients with upper motor neuron lesions: time course, local distribution and pathogenetic aspects. J Neurol. 1983;230(3):143–51.PubMedCrossRef
2.
Spaans F, Wilts G. Denervation due to lesions of the central nervous system. An EMG study in cases of cerebral contusion and cerebrovascular accidents. J Neurol Sci. 1982;57(2–3):291–305.PubMedCrossRef
3.
van Kuijk AA, Pasman JW, Hendricks HT, Zwarts MJ, Geurts AC. Predicting hand motor recovery in severe stroke: the role of motor evoked potentials in relation to early clinical assessment. Neurorehabil Neural Repair. 2009;23(1):45–51.PubMedCrossRef
4.
Hara Y, Masakado Y, Chino N. The physiological functional loss of single thenar motor units in the stroke patients: when does it occur? Does it progress? Clin Neurophysiol. 2004;115(1):97–103.PubMedCrossRef
5.
Lukacs M. Electrophysiological signs of changes in motor units after ischaemic stroke. Clin Neurophysiol. 2005;116(7):1566–70.PubMedCrossRef
6.
Scherbakov N, Sandek A, Doehner W. Stroke-related sarcopenia: specific characteristics. J Am Med Dir Assoc. 2015;16(4):272–6.PubMedCrossRef
7.
English C, McLennan H, Thoirs K, Coates A, Bernhardt J. Loss of skeletal muscle mass after stroke: a systematic review. Int J Stroke. 2010;5(5):395–402.PubMedCrossRef
8.
Hafer-Macko CE, Ryan AS, Ivey FM, Macko RF. Skeletal muscle changes after hemiparetic stroke and potential beneficial effects of exercise intervention strategies. J Rehabil Res Dev. 2008;45(2):261–72.PubMedPubMedCentralCrossRef
9.
Berenpas F, Martens AM, Weerdesteyn V, Geurts AC, van Alfen N. Bilateral changes in muscle architecture of physically active people with chronic stroke: a quantitative muscle ultrasound study. Clin Neurophysiol. 2017;128(1):115–22.PubMedCrossRef
10.
Dunning K, O'Dell MW, Kluding P, McBride K. Peroneal stimulation for foot drop after stroke: a systematic review. Am J Phys Med Rehabil. 2015;94(8):649–64.PubMedCrossRef
11.
Liberson WT, Holmquest HJ, Scot D, Dow M. Functional electrotherapy: stimulation of the peroneal nerve synchronized with the swing phase of the gait of hemiplegic patients. Arch Phys Med Rehabil. 1961;42:101–5.PubMed
12.
Khaslavskaia S, Sinkjaer T. Motor cortex excitability following repetitive electrical stimulation of the common peroneal nerve depends on the voluntary drive. Exp Brain Res. 2005;162(4):497–502.PubMedCrossRef
13.
Everaert DG, Thompson AK, Chong SL, Stein RB. Does functional electrical stimulation for foot drop strengthen corticospinal connections? Neurorehabil Neural Repair. 2010;24(2):168–77.PubMedCrossRef
14.
Thibaut A, Moissenet F, Di Perri C, Schreiber C, Remacle A, Kolanowski E, et al. Brain plasticity after implanted peroneal nerve electrical stimulation to improve gait in chronic stroke patients: two case reports. NeuroRehabilitation. 2017;40(2):251–8.PubMedCrossRef
15.
Merkel C, Hausmann J, Hopf JM, Heinze HJ, Buentjen L, Schoenfeld MA. Active prosthesis dependent functional cortical reorganization following stroke. Sci Rep. 2017;7(1):8680.PubMedPubMedCentralCrossRef
16.
Stein RB, Chong S, Everaert DG, Rolf R, Thompson AK, Whittaker M, et al. A multicenter trial of a footdrop stimulator controlled by a tilt sensor. Neurorehabil Neural Repair. 2006;20(3):371–9.PubMedCrossRef
17.
Pillen S, Tak RO, Zwarts MJ, Lammens MM, Verrijp KN, Arts IM, et al. Skeletal muscle ultrasound: correlation between fibrous tissue and echo intensity. Ultrasound Med Biol. 2009;35(3):443–6.PubMedCrossRef
18.
Mul K, Horlings CGC, Vincenten SCC, Voermans NC, van Engelen BGM, van Alfen N. Quantitative muscle MRI and ultrasound for facioscapulohumeral muscular dystrophy: complementary imaging biomarkers. J Neurol. 2018;265(11):2646–55.PubMedPubMedCentralCrossRef
19.
Arts IMP, Overeem S, Pillen S, Jurgen Schelhaas H, Zwarts MJ. Muscle changes in amyotrophic lateral sclerosis: a longitudinal ultrasonography study. Clin Neurophysiol. 2011;122(3):623–8.PubMedCrossRef
20.
Pillen S, Arts IM, Zwarts MJ. Muscle ultrasound in neuromuscular disorders. Muscle Nerve. 2008;37(6):679–93.PubMedCrossRef
21.
Arts IM, van Rooij FG, Overeem S, Pillen S, Janssen HM, Schelhaas HJ, et al. Quantitative muscle ultrasonography in amyotrophic lateral sclerosis. Ultrasound Med Biol. 2008;34(3):354–61.PubMedCrossRef
22.
Berenpas F, Schiemanck S, Beelen A, Nollet F, Weerdesteyn V, Geurts A. Kinematic and kinetic benefits of implantable peroneal nerve stimulation in people with post-stroke drop foot using an ankle-foot orthosis. Restor Neurol Neurosci. 2018;36(4):547–58.PubMed
23.
World Medical A. World Medical Association Declaration of Helsinki. Ethical principles for medical research involving human subjects. Bull World Health Organ. 2001;79(4):373–4.
24.
Demeurisse G, Demol O, Robaye E. Motor evaluation in vascular hemiplegia. Eur Neurol. 1980;19(6):382–9.PubMedCrossRef
25.
Fugl-Meyer AR, Jaasko L, Leyman I, Olsson S, Steglind S. The post-stroke hemiplegic patient. 1. A method for evaluation of physical performance. Scand J Rehabil Med. 1975;7(1):13–31.PubMed
26.
Peters DM, Fritz SL, Krotish DE. Assessing the reliability and validity of a shorter walk test compared with the 10-meter walk test for measurements of gait speed in healthy, older adults. J Geriatr Phys Ther. 2013;36(1):24–30.PubMedCrossRef
27.
Burridge JH, Haugland M, Larsen B, Pickering RM, Svaneborg N, Iversen HK, et al. Phase II trial to evaluate the ActiGait implanted drop-foot stimulator in established hemiplegia. J Rehabil Med. 2007;39(3):212–8.PubMedCrossRef
28.
Ernst J, Grundey J, Hewitt M, von Lewinski F, Kaus J, Schmalz T, et al. Towards physiological ankle movements with the ActiGait implantable drop foot stimulator in chronic stroke. Restor Neurol Neurosci. 2013;31(5):557–69.PubMed
29.
Schiemanck S, Berenpas F, van Swigchem R, van den Munckhof P, de Vries J, Beelen A, et al. Effects of implantable peroneal nerve stimulation on gait quality, energy expenditure, participation and user satisfaction in patients with post-stroke drop foot using an ankle-foot orthosis. Restor Neurol Neurosci. 2015;33(6):795–807.PubMed
30.
Pillen S, van Keimpema M, Nievelstein RA, Verrips A, van Kruijsbergen-Raijmann W, Zwarts MJ. Skeletal muscle ultrasonography: Visual versus quantitative evaluation. Ultrasound Med Biol. 2006;32(9):1315–21.PubMedCrossRef
31.
O'Brien TG, Cazares Gonzalez ML, Ghosh PS, Mandrekar J, Boon AJ. Reliability of a novel ultrasound system for gray-scale analysis of muscle. Muscle Nerve. 2017;56(3):408–12.PubMedCrossRef
32.
Zaidman CM, Wu JS, Wilder S, Darras BT, Rutkove SB. Minimal training is required to reliably perform quantitative ultrasound of muscle. Muscle Nerve. 2014;50(1):124–8.PubMedPubMedCentralCrossRef
33.
van Alfen N, Mah JK. Neuromuscular ultrasound: a new tool in your toolbox. Can J Neurol Sci. 2018;45(5):504–15.PubMedCrossRef
34.
Scholten RR, Pillen S, Verrips A, Zwarts MJ. Quantitative ultrasonography of skeletal muscles in children: normal values. Muscle Nerve. 2003;27(6):693–8.PubMedCrossRef
35.
Jansen M, van Alfen N, Nijhuis van der Sanden MW, van Dijk JP, Pillen S, de Groot IJ. Quantitative muscle ultrasound is a promising longitudinal follow-up tool in Duchenne muscular dystrophy. Neuromuscul Disord. 2012;22(4):306–17.PubMedCrossRef
36.
Janssen BH, Pillen S, Voet NB, Heerschap A, van Engelen BG, van Alfen N. Quantitative muscle ultrasound versus quantitative magnetic resonance imaging in facioscapulohumeral dystrophy. Muscle Nerve. 2014;50(6):968–75.PubMedCrossRef
37.
Bickerstaffe A, Beelen A, Zwarts MJ, Nollet F, van Dijk JP. Quantitative muscle ultrasound and quadriceps strength in patients with post-polio syndrome. Muscle Nerve. 2015;51(1):24–9.PubMedCrossRef
38.
Arts IM, Pillen S, Schelhaas HJ, Overeem S, Zwarts MJ. Normal values for quantitative muscle ultrasonography in adults. Muscle Nerve. 2010;41(1):32–41.PubMedCrossRef
39.
Verhulst FV, Leeuwesteijn AE, Louwerens JW, Geurts AC, Van Alfen N, Pillen S. Quantitative ultrasound of lower leg and foot muscles: feasibility and reference values. Foot Ankle Surg. 2011;17(3):145–9.PubMedCrossRef
40.
Chaudhry V, Cornblath DR, Mellits ED, Avila O, Freimer ML, Glass JD, et al. Inter- and intra-examiner reliability of nerve conduction measurements in normal subjects. Ann Neurol. 1991;30(6):841–3.PubMedCrossRef
41.
Picelli A, Tamburin S, Cavazza S, Scampoli C, Manca M, Cosma M, et al. Relationship between ultrasonographic, electromyographic, and clinical parameters in adult stroke patients with spastic equinus: an observational study. Arch Phys Med Rehabil. 2014;95(8):1564–70.PubMedCrossRef
42.
Ryan AS, Buscemi A, Forrester L, Hafer-Macko CE, Ivey FM. Atrophy and intramuscular fat in specific muscles of the thigh: associated weakness and hyperinsulinemia in stroke survivors. Neurorehabil Neural Repair. 2011;25(9):865–72.PubMedPubMedCentralCrossRef
43.
Ryan AS, Dobrovolny CL, Smith GV, Silver KH, Macko RF. Hemiparetic muscle atrophy and increased intramuscular fat in stroke patients. Arch Phys Med Rehabil. 2002;83(12):1703–7.PubMedCrossRef
44.
Klein CS, Brooks D, Richardson D, McIlroy WE, Bayley MT. Voluntary activation failure contributes more to plantar flexor weakness than antagonist coactivation and muscle atrophy in chronic stroke survivors. J Appl Physiol (1985). 2010;109(5):1337–46.CrossRef
45.
Akazawa N, Harada K, Okawa N, Tamura K, Hayase A, Moriyama H. Relationships between muscle mass, intramuscular adipose and fibrous tissues of the quadriceps, and gait independence in chronic stroke survivors: a cross-sectional study. Physiotherapy. 2018;104(4):438–45.PubMedCrossRef
46.
Dudley-Javoroski S, McMullen T, Borgwardt MR, Peranich LM, Shields RK. Reliability and responsiveness of musculoskeletal ultrasound in subjects with and without spinal cord injury. Ultrasound Med Biol. 2010;36(10):1594–607.PubMedPubMedCentralCrossRef
47.
Ryan TE, Brizendine JT, Backus D, McCully KK. Electrically induced resistance training in individuals with motor complete spinal cord injury. Arch Phys Med Rehabil. 2013;94(11):2166–73.PubMedCrossRef
48.
Kern H, Carraro U, Adami N, Biral D, Hofer C, Forstner C, et al. Home-based functional electrical stimulation rescues permanently denervated muscles in paraplegic patients with complete lower motor neuron lesion. Neurorehabil Neural Repair. 2010;24(8):709–21.PubMedCrossRef
49.
Jacobs J, Jansen M, Janssen H, Raijmann W, Van Alfen N, Pillen S. Quantitative muscle ultrasound and muscle force in healthy children: a 4-year follow-up study. Muscle Nerve. 2013;47(6):856–63.PubMedCrossRef
50.
Burke D, Kiernan MC, Bostock H. Excitability of human axons. Clin Neurophysiol. 2001;112(9):1575–85.PubMedCrossRef
51.
Estigoni EH, Fornusek C, Hamzaid NA, Hasnan N, Smith RM, Davis GM. Evoked EMG versus muscle torque during fatiguing functional electrical stimulation-evoked muscle contractions and short-term recovery in individuals with spinal cord injury. Sensors (Basel). 2014;14(12):22907–20.CrossRef
52.
Ibitoye MO, Hamzaid NA, Hasnan N, Abdul Wahab AK, Davis GM. Strategies for rapid muscle fatigue reduction during FES exercise in individuals with spinal cord injury: a systematic review. PLoS One. 2016;11(2):e0149024.PubMedPubMedCentralCrossRef
53.
Michael KM, Allen JK, Macko RF. Reduced ambulatory activity after stroke: the role of balance, gait, and cardiovascular fitness. Arch Phys Med Rehabil. 2005;86(8):1552–6.PubMedCrossRef
Metadata
Title
Long-term use of implanted peroneal functional electrical stimulation for stroke-affected gait: the effects on muscle and motor nerve
Authors
Frank Berenpas
Vivian Weerdesteyn
Alexander C. Geurts
Nens van Alfen
Publication date
01-12-2019

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