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Split Phenomenon of Fasciculation between Antagonistic Muscles in Amyotrophic Lateral Sclerosis: An Ultrasound Study

Published online by Cambridge University Press:  15 May 2023

Nan Hu
Affiliation:
Department of Neurology, Peking Union Medical College Hospital, Beijing, China
Yi Li
Affiliation:
Department of Neurology, Peking Union Medical College Hospital, Beijing, China
Jingwen Liu
Affiliation:
Department of Neurology, Peking Union Medical College Hospital, Beijing, China
Liying Cui
Affiliation:
Department of Neurology, Peking Union Medical College Hospital, Beijing, China
Mingsheng Liu*
Affiliation:
Department of Neurology, Peking Union Medical College Hospital, Beijing, China
*
Corresponding author: Mingsheng Liu, Department of Neurology, Peking Union Medical College Hospital, Peking Union Medical College and Chinese Academy of Medical Sciences, Beijing 100730, China. Email: liumingsheng_pumch@163.com

Abstract:

Objective:

Paresis of muscle groups in patients with amyotrophic lateral sclerosis (ALS) tends to present split phenomena. We explored the split phenomenon of fasciculation in multiple antagonistic muscle groups in ALS patients.

Methods:

One hundred and forty ALS patients and 66 non-ALS patients were included from a single ALS center. Muscle ultrasonography (MUS) was performed to detect fasciculation in elbow flexor-extensor, wrist flexor-extensor, knee flexor-extensor, and ankle flexor-extensor. Split phenomena of fasciculation between different antagonistic muscle groups were summarized, and the possible influence factors were analyzed through stratified analysis.

Results:

The frequency of split phenomenon of fasciculation intensity was significantly higher than those of muscle strength (26.1% vs. 7.1% for elbow flexor-extensor, 38.3% vs. 5.7% for wrist flexor-extensor, 37.9% vs. 3.0% for knee extensor-flexor, and 33.6% vs. 14.4% for ankle flexor-extensor) (P < 0.01). For muscles with 0–1 level of muscle strength (the Medical Research Council, MRC, score), significance difference in mean fasciculation intensity was observed only in ankle flexor-extensor. For muscles with 2–5 level of muscle strength, significant dissociation of fasciculation grade was common, especially among patients with slow rapid progression rate and both upper and lower motor neuron (UMN and LMN) involvement. As for non-ALS patients, no significant difference was observed in fasciculation intensity between antagonistic muscles.

Conclusion:

Split phenomenon of fasciculation between antagonistic muscles was common and relatively specific in ALS patients. Muscle strength, progression rate, and UMN involvement were influence factors of the split phenomenon of fasciculation intensity.

Résumé :

RÉSUMÉ :

Étude du phénomène de fasciculation entre les muscles antagonistes dans la sclérose latérale amyotrophique, par échographie.

Objectif :

La parésie de certains groupes musculaires chez les patients atteints de sclérose latérale amyotrophique (SLA) tend à se manifester par un phénomène de dissociation musculaire. L’étude visait donc à examiner le phénomène de fasciculation qui se produit dans différents groupes de muscles antagonistes chez des patients atteints de SLA.

Méthode :

Ont participé à l’étude 140 patients atteints de SLA et 66 sujets épargnés par la maladie, provenant d’un seul centre de traitement de la SLA. Une échographie des muscles (EM) a été effectuée afin de permettre la détection du phénomène de fasciculation des groupes fléchisseurs/extenseurs (F/E) du coude, du poignet, de genou et de la cheville. Le phénomène de fasciculation observé entre les différents groupes de muscles antagonistes a été décrit dans un résumé, et une analyse stratifiée a permis d’étudier l’influence possible de différents facteurs.

Résultats :

La fréquence de l’intensité des fasciculations était passablement plus élevée que celle de la force musculaire (groupe F/E du coude : 26,1 % contre [c.] 7,1 %; groupe F/E du poignet : 38,3 % c. 5,7 %; groupe F/E du genou : 37,9 % c. 3,0 %; groupe F/E de la cheville : 33,6 % c. 14,4 %) (p < 0,01). En ce qui concerne la force musculaire de degré 01 (selon l’échelle du Medical Research Council [MRC [R.U.}], un écart important de l’intensité moyenne des fasciculations n’a été observé que dans le groupe F/E de la cheville. Pour ce qui est de la force musculaire de degré 25, une dissociation importante du degré de fasciculation était fréquente, surtout chez les patients présentant une évolution lente ou rapide de la maladie et une atteinte des motoneurones supérieurs et inférieurs (MNS et MNI). Quant aux sujets exempts de la SLA, aucun écart important de l’intensité des fasciculations n’a été relevé entre les muscles antagonistes.

Conclusion :

Le phénomène de fasciculation entre les muscles antagonistes était fréquent et relativement spécifique de la SLA. La force musculaire, la vitesse d’évolution de la maladie et l’atteinte des MNS se sont révélées des facteurs qui influent sur l’intensité du phénomène de fasciculation.

Type
Original Article
Copyright
© The Author(s), 2023. Published by Cambridge University Press on behalf of Canadian Neurological Sciences Federation

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References

Oskarsson, B, Gendron, TF, Staff, NP. Amyotrophic lateral sclerosis: an update for 2018. Mayo Clin Proc. 2018;93:161728. DOI 10.1016/j.mayocp.2018.04.007.10.1016/j.mayocp.2018.04.007CrossRefGoogle ScholarPubMed
Rosa Silva, JP, Santiago Júnior, JB, Dos Santos, EL, et al. Quality of life and functional independence in amyotrophic lateral sclerosis: a systematic review. Neurosci Biobehav Rev. 2020;111:111. DOI 10.1016/j.neubiorev.2019.12.032.10.1016/j.neubiorev.2019.12.032CrossRefGoogle ScholarPubMed
Hu, N, Wang, J, Liu, M. Split hand in amyotrophic lateral sclerosis: a systematic review and meta-analysis. J Clin Neurosci. 2021;90:293301. DOI 10.1016/j.jocn.2021.06.015.10.1016/j.jocn.2021.06.015CrossRefGoogle ScholarPubMed
Menon, P, Bae, JS, Mioshi, E, Kiernan, MC, Vucic, S. Split-hand plus sign in ALS: differential involvement of the flexor pollicis longus and intrinsic hand muscles. Amyotroph Lateral Scler Frontotemporal Degener. 2013;14:3158. DOI 10.3109/21678421.2012.734521.10.3109/21678421.2012.734521CrossRefGoogle ScholarPubMed
Lee, JD, Heshmat, S, Heggie, S, Thorpe, KA, McCombe, PA, Henderson, RD. Clinical and electrophysiological examination of pinch strength in patients with amyotrophic lateral sclerosis. Muscle Nerve. 2021;63:10813. DOI 10.1002/mus.27111.10.1002/mus.27111CrossRefGoogle ScholarPubMed
Khalaf, R, Martin, S, Ellis, C, et al. Relative preservation of triceps over biceps strength in upper limb-onset ALS: the ’split elbow'. J Neurol Neurosurg Psychiatry. 2019;90:7303. DOI 10.1136/jnnp-2018-319894.10.1136/jnnp-2018-319894CrossRefGoogle ScholarPubMed
Ludolph, AC, Emilian, S, Dreyhaupt, J, et al. Pattern of paresis in ALS is consistent with the physiology of the corticomotoneuronal projections to different muscle groups. J Neurol Neurosurg Psychiatry. 2020;91:9918. DOI 10.1136/jnnp-2020-323331.10.1136/jnnp-2020-323331CrossRefGoogle ScholarPubMed
de Carvalho, M, Dengler, R, Eisen, A, et al. Electrodiagnostic criteria for diagnosis of ALS. Clin Neurophysiol. 2008;119:497503. DOI 10.1016/j.clinph.2007.09.143.10.1016/j.clinph.2007.09.143CrossRefGoogle ScholarPubMed
de Carvalho, M, Swash, M. Physiology of the fasciculation potentials in amyotrophic lateral sclerosis: Which motor units fasciculate? J Physiol Sci. 2017;67:56976. DOI 10.1007/s12576-016-0484-x.10.1007/s12576-016-0484-xCrossRefGoogle ScholarPubMed
de Carvalho, M, Kiernan, MC, Swash, M. Fasciculation in amyotrophic lateral sclerosis: origin and pathophysiological relevance. J Neurol Neurosurg Psychiatry. 2017;88:7739. DOI 10.1136/jnnp-2017-315574.10.1136/jnnp-2017-315574CrossRefGoogle ScholarPubMed
Misawa, S, Noto, Y, Shibuya, K, et al. Ultrasonographic detection of fasciculations markedly increases diagnostic sensitivity of ALS. Neurology. 2011;77:15327. DOI 10.1212/WNL.0b013e318233b36a.10.1212/WNL.0b013e318233b36aCrossRefGoogle ScholarPubMed
Liu, J, Li, Y, Niu, J, et al. Fasciculation differences between ALS and non-ALS patients: an ultrasound study. BMC Neurol. 2021;21:441. DOI 10.1186/s12883-021-02473-5.10.1186/s12883-021-02473-5CrossRefGoogle ScholarPubMed
Arts, IM, van Rooij, FG, Overeem, S, et al. Quantitative muscle ultrasonography in amyotrophic lateral sclerosis. Ultrasound Med Biol. 2008;34:35461. DOI 10.1016/j.ultrasmedbio.2007.08.013.10.1016/j.ultrasmedbio.2007.08.013CrossRefGoogle ScholarPubMed
Tsuji, Y, Noto, YI, Kitaoji, T, Kojima, Y, Mizuno, T. Difference in distribution of fasciculations between multifocal motor neuropathy and amyotrophic lateral sclerosis. Clin Neurophysiol. 2020;131:28048. DOI 10.1016/j.clinph.2020.08.021.10.1016/j.clinph.2020.08.021CrossRefGoogle ScholarPubMed
Tsugawa, J, Dharmadasa, T, Ma, Y, Huynh, W, Vucic, S, Kiernan, MC. Fasciculation intensity and disease progression in amyotrophic lateral sclerosis. Clin Neurophysiol. 2018;129:214954. DOI 10.1016/j.clinph.2018.07.015.10.1016/j.clinph.2018.07.015CrossRefGoogle ScholarPubMed
Cedarbaum, JM, Stambler, N, Malta, E, et al. The ALSFRS-R: a revised ALS functional rating scale that incorporates assessments of respiratory function. BDNF ALS Study Group (Phase III). J Neurol Sci. 1999; 169:1321. DOI 10.1016/s0022-510x(99)00210-5.10.1016/S0022-510X(99)00210-5CrossRefGoogle ScholarPubMed
Liu, J, Wang, Z, Shen, D, Yang, X, Liu, M, Cui, L. Split phenomenon of antagonistic muscle groups in amyotrophic lateral sclerosis: relative preservation of flexor muscles. Neurol Res. 2021;43:37280. DOI 10.1080/01616412.2020.1866354.10.1080/01616412.2020.1866354CrossRefGoogle ScholarPubMed
Labra, J, Menon, P, Byth, K, Morrison, S, Vucic, S. Rate of disease progression: a prognostic biomarker in ALS. J Neurol Neurosurg Psychiatry. 2016;87:62832. DOI 10.1136/jnnp-2015-310998.10.1136/jnnp-2015-310998CrossRefGoogle ScholarPubMed
Simon, NG, Lee, M, Bae, JS, et al. Dissociated lower limb muscle involvement in amyotrophic lateral sclerosis. J Neurol. 2015;262:142432. DOI 10.1007/s00415-015-7721-8.10.1007/s00415-015-7721-8CrossRefGoogle ScholarPubMed
Eisen, A, Vucic, S. Fasciculation potentials: a diagnostic biomarker of early ALS? J Neurol Neurosurg Psychiatry. 2013;84:948. DOI 10.1136/jnnp-2013-305036.10.1136/jnnp-2013-305036CrossRefGoogle ScholarPubMed
Bokuda, K, Shimizu, T, Kimura, H, et al. Quantitative analysis of the features of fasciculation potentials and their relation with muscle strength in amyotrophic lateral sclerosis. Neurol Sci. 2016;37:193945. DOI 10.1007/s10072-016-2692-9.10.1007/s10072-016-2692-9CrossRefGoogle ScholarPubMed
Juan, W, Fang, L, Qi, W, et al. Muscle ultrasonography in the diagnosis of amyotrophic lateral sclerosis. Neurol Res. 2020;42:45862. DOI 10.1080/01616412.2020.1738100.10.1080/01616412.2020.1738100CrossRefGoogle ScholarPubMed
Avidan, R, Fainmesser, Y, Drory, VE, Bril, V, Abraham, A. Fasciculation frequency at the biceps brachii and brachialis muscles is associated with amyotrophic lateral sclerosis disease burden and activity. Muscle Nerve. 2021;63:2048. DOI 10.1002/mus.27125.10.1002/mus.27125CrossRefGoogle ScholarPubMed
Abdul Aziz, NA, Toh, TH, Loh, EC, et al. The utility of ALS staging systems in a multi-ethnic patient cohort. Amyotroph Lateral Scler Frontotemporal Degener. 2021;22:34149. DOI 10.1080/21678421.2021.1893336.10.1080/21678421.2021.1893336CrossRefGoogle Scholar
de Carvalho, M, Swash, M. Origin of fasciculations in amyotrophic lateral sclerosis and benign fasciculation syndrome. JAMA Neurol. 2013;70:15625. DOI 10.1001/jamaneurol.2013.4437.Google ScholarPubMed
Kleine, BU, Stegeman, DF, Schelhaas, HJ, Zwarts, MJ. Firing pattern of fasciculations in ALS: evidence for axonal and neuronal origin. Neurology. 2008;70:3539. DOI 10.1212/01.wnl.0000300559.14806.2a.10.1212/01.wnl.0000300559.14806.2aCrossRefGoogle ScholarPubMed
Roth, G. Fasciculations and their F-response: localisation of their axonal origin. J Neurol Sci. 1984;63:299306. DOI 10.1016/0022-510x(84)90152-7.10.1016/0022-510X(84)90152-7CrossRefGoogle ScholarPubMed
de Carvalho, M, Turkman, A, Pinto, S, Swash, M. Modulation of fasciculation frequency in amyotrophic lateral sclerosis. J Neurol Neurosurg Psychiatry. 2016;87:2268. DOI 10.1136/jnnp-2014-309686.Google ScholarPubMed
Cleveland, DW, Bruijn, LI, Wong, PC, et al. Mechanisms of selective motor neuron death in transgenic mouse models of motor neuron disease. Neurology. 1996;47:S5461; discussion S61–2. DOI 10.1212/wnl.47.4_suppl_2.54s.10.1212/WNL.47.4_Suppl_2.54SCrossRefGoogle ScholarPubMed
de Carvalho, M, Miranda, PC, Lourdes Sales Luís, M, Ducla-Soares, E. Neurophysiological features of fasciculation potentials evoked by transcranial magnetic stimulation in amyotrophic lateral sclerosis. J Neurol. 2000;247:18994. DOI 10.1007/s004150050561.10.1007/s004150050561CrossRefGoogle ScholarPubMed
Mills, KR. Motor neuron disease: studies of the corticospinal excitation of single motor neurons by magnetic brain stimulation. Brain. 1995;118:97182. DOI 10.1093/brain/118.4.971.10.1093/brain/118.4.971CrossRefGoogle ScholarPubMed
Eisen, A, Weber, M. The motor cortex and amyotrophic lateral sclerosis. Muscle Nerve. 2001;24:56473. DOI 10.1002/mus.1042.10.1002/mus.1042CrossRefGoogle ScholarPubMed
Menon, P, Kiernan, MC, Vucic, S. Cortical hyperexcitability precedes lower motor neuron dysfunction in ALS. Clin Neurophysiol. 2015;126:8039. DOI 10.1016/j.clinph.2014.04.023.CrossRefGoogle ScholarPubMed
Eisen, A, Braak, H, Del Tredici, K, Lemon, R, Ludolph, AC, Kiernan, MC. Cortical influences drive amyotrophic lateral sclerosis. J Neurol Neurosurg Psychiatry. 2017;88:91724. DOI 10.1136/jnnp-2017-315573.10.1136/jnnp-2017-315573CrossRefGoogle ScholarPubMed
Eisen, A, Turner, MR, Lemon, R. Tools and talk: an evolutionary perspective on the functional deficits associated with amyotrophic lateral sclerosis. Muscle Nerve. 2014;49:46977. DOI 10.1002/mus.24132.10.1002/mus.24132CrossRefGoogle ScholarPubMed
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