Autonomic dysfunction in amyotrophic lateral sclerosis: A neurophysiological and neurosonology study.


Journal

Journal of neuroimaging : official journal of the American Society of Neuroimaging
ISSN: 1552-6569
Titre abrégé: J Neuroimaging
Pays: United States
ID NLM: 9102705

Informations de publication

Date de publication:
07 2022
Historique:
revised: 07 03 2022
received: 09 02 2022
accepted: 10 03 2022
pubmed: 29 3 2022
medline: 26 7 2022
entrez: 28 3 2022
Statut: ppublish

Résumé

Amyotrophic lateral sclerosis (ALS) is a progressive neurodegenerative disorder affecting upper and lower motor neurons. Some ALS patients exhibit concomitant nonmotor signs, and thus ALS is considered a multisystem disorder. The aim of this study is to investigate autonomous nervous system involvement in ALS. We investigated 21 ALS patients and 28 age-matched controls. ALS patients were assessed for disease severity with the Revised-ALS Functional Rating Scale (ALSFSR) and for the presence of autonomic symptoms with the Composite Autonomic Symptom Score scale. Sympathetic nervous system was evaluated by sympathetic skin response (SSR) and parasympathetic nervous system by ultrasonography of vagus nerve (VN) at the level of the thyroid gland. SSR latencies were shorter and SSR amplitudes were higher in controls compared to ALS patients. The cross-sectional area (CSA) of the VN was significantly smaller in ALS patients (mean CSA right/left: 1.73±0.62 mm This study confirms the presence of autonomic dysfunction in ALS patients and provides evidence of VN atrophy that correlates with disease severity and duration and is independent of bulbar involvement. Degeneration of dorsal nucleus neurons of the VN is hypothesized.

Sections du résumé

BACKGROUND AND PURPOSE
Amyotrophic lateral sclerosis (ALS) is a progressive neurodegenerative disorder affecting upper and lower motor neurons. Some ALS patients exhibit concomitant nonmotor signs, and thus ALS is considered a multisystem disorder. The aim of this study is to investigate autonomous nervous system involvement in ALS.
METHODS
We investigated 21 ALS patients and 28 age-matched controls. ALS patients were assessed for disease severity with the Revised-ALS Functional Rating Scale (ALSFSR) and for the presence of autonomic symptoms with the Composite Autonomic Symptom Score scale. Sympathetic nervous system was evaluated by sympathetic skin response (SSR) and parasympathetic nervous system by ultrasonography of vagus nerve (VN) at the level of the thyroid gland.
RESULTS
SSR latencies were shorter and SSR amplitudes were higher in controls compared to ALS patients. The cross-sectional area (CSA) of the VN was significantly smaller in ALS patients (mean CSA right/left: 1.73±0.62 mm
CONCLUSIONS
This study confirms the presence of autonomic dysfunction in ALS patients and provides evidence of VN atrophy that correlates with disease severity and duration and is independent of bulbar involvement. Degeneration of dorsal nucleus neurons of the VN is hypothesized.

Identifiants

pubmed: 35344230
doi: 10.1111/jon.12993
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

710-719

Informations de copyright

© 2022 American Society of Neuroimaging.

Références

Shefner JM, Al-Chalabi A, Baker MR, et al. A proposal for new diagnostic criteria for ALS. Clin Neurophysiol 2020;131:1975-8.
Kiernan MC, Vucic S, Cheah BC, et al. Amyotrophic lateral sclerosis. Lancet 2011;377:942-55.
Consonni M, Dalla Bella E, Bersano E, Lauria G. Cognitive and behavioural impairment in amyotrophic lateral sclerosis: a landmark of the disease? A mini review of longitudinal studies. Neurosci Lett 2021;754:135898.
Constantinidis J. [A familial syndrome: a combination of Pick's disease and amyotrophic lateral sclerosis]. Encephale 1987;13:285-93.
Mccluskey L, Vandriel S, Elman L, et al. ALS-Plus syndrome: non-pyramidal features in a large ALS cohort. J Neurol Sci 2014;345:118-24.
Riku Y, Yoshida M, Tamura T, et al. Unexpected postmortem diagnoses in cases of clinically diagnosed amyotrophic lateral sclerosis. Neuropathology 2021;41:457-67.
Pimentel RMM, Macedo H, Valenti VE, et al. Decreased heart rate variability in individuals with amyotrophic lateral sclerosis. Respir Care 2019;64:1088-95.
Giess R, Werner E, Beck M. Impaired salivary gland function reveals autonomic dysfunction in amyotrophic lateral sclerosis. J Neurol 2002;249:1246-9.
Cellura E. [Extramotor disorders in amyotrophic lateral sclerosis: multisystem disease?]. Clin Ter 2011;162:457-9.
Baltadzhieva R, Gurevich T, Korczyn AD. Autonomic impairment in amyotrophic lateral sclerosis. Curr Opin Neurol 2005;18:487-93.
Merico A, Cavinato M. Autonomic dysfunction in the early stage of ALS with bulbar involvement. Amyotroph Lateral Scler 2011;12:363-7.
Pisano F, Miscio G, Mazzuero G, Lanfranchi P, Colombo R, Pinelli P. Decreased heart rate variability in amyotrophic lateral sclerosis. Muscle Nerve 1995;18:1225-31.
Pinto S, Pinto A, De Carvalho M. Decreased heart rate variability predicts death in amyotrophic lateral sclerosis. Muscle Nerve 2012;46:341-5.
Shimizu T, Hayashi H, Kato S, Hayashi M, Tanabe H, Oda M. Circulatory collapse and sudden death in respirator-dependent amyotrophic lateral sclerosis. J Neurol Sci 1994;124:45-55.
Barron SA, Mazliah J, Bental E. Sympathetic cholinergic dysfunction in amyotrophic lateral sclerosis. Acta Neurol Scand 1987;75:62-3.
Hu F, Jin J, Qu Q, Dang J. Sympathetic skin response in amyotrophic lateral sclerosis. J Clin Neurophysiol 2016;33:60-5.
Oey PL, Vos PE, Wieneke GH, Wokke JHJ, Blankestijn PJ, Karemaker JM. Subtle involvement of the sympathetic nervous system in amyotrophic lateral sclerosis. Muscle Nerve 2002;25:402-8.
Dettmers C, Fatepour D, Faust H, Jerusalem F. Sympathetic skin response abnormalities in amyotrophic lateral sclerosis. Muscle Nerve 1993;16:930-4.
Miscio G, Pisano F. Sympathetic skin response in amyotrophic lateral sclerosis. Acta Neurol Scand 1998;98:276-9.
Masur H, Schulte-Oversohl U, Papke K, Oberwittler C, Vollmer J. Sympathetic skin response in patients with amyotrophic lateral sclerosis. Funct Neurol 1995;10:131-5.
Pelz JO, Belau E, Fricke C, Classen J, Weise D. Axonal degeneration of the vagus nerve in Parkinson's disease-a high-resolution ultrasound study. Front Neurol 2018;9:951.
Sartucci F, Bocci T, Santin M, Bongioanni P, Orlandi G. High-resolution ultrasound changes of the vagus nerve in idiopathic Parkinson's disease (IPD): a possible additional index of disease. Neurol Sci 2021;42:5205-11.
Tsukita K, Taguchi T, Sakamaki-Tsukita H, Tanaka K, Suenaga T. The vagus nerve becomes smaller in patients with Parkinson's disease: a preliminary cross-sectional study using ultrasonography. Parkinsonism Relat Disord 2018;55:148-9.
Laucius O, Balnytė R, Petrikonis K, et al. Ultrasonography of the vagus nerve in the diagnosis of Parkinson's disease. Parkinsons Dis 2020;2020:2627471.
Horsager J, Walter U, Fedorova TD, et al. Vagus nerve cross-sectional area in patients with Parkinson's disease-an ultrasound case-control study. Front Neurol 2021;12:681413.
Abdelnaby R, Elsayed M, Mohamed KA, et al. Vagus nerve ultrasonography in Parkinson's disease: a systematic review and meta-analysis. Auton Neurosci Basic Clin 2021;234:102835.
Fedtke N, Witte OW, Prell T. Ultrasonography of the vagus nerve in Parkinson's disease. Front Neurol 2018;9:525.
Tawfik EA, Walker FO, Cartwright MS, El-Hilaly RA. Diagnostic ultrasound of the vagus nerve in patients with diabetes. J Neuroimaging 2017;27:589-93.
Tawfik EA. Vagus nerve ultrasound in a patient with amyotrophic lateral sclerosis. Muscle Nerve 2016;54:978-9.
Holzapfel K, Naumann M. Ultrasound detection of vagus nerve atrophy in bulbar amyotrophic lateral sclerosis. J Neuroimaging 2020;30:762-5.
World Medical Association. World Medical Association Declaration of Helsinki: ethical principles for medical research involving human subjects. JAMA 2013;310:2191-4.
Brooks BR, Miller RG, Swash M, Munsat TL World Federation of Neurology Research Group on Motor Neuron Diseases. El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotroph Lateral Scler Mot Neuron Disord 2000;1:293-9.
Sletten DM, Suarez GA, Low PA, Mandrekar J, Singer W. COMPASS 31: a refined and abbreviated Composite Autonomic Symptom Score. Mayo Clin Proc 2012;87:1196-201.
Kim Y, Seok JM, Park J, et al. The composite autonomic symptom scale 31 is a useful screening tool for patients with Parkinsonism. PLoS One 2017;12:e0180744.
Krbot Skorić M, Crnošija L, Tereza G, et al. Autonomic symptom burden can predict disease activity in early multiple sclerosis. Mult Scler Relat Disord 2019;28:250-5.
D'amato C, Greco C, Lombardo G, et al. The diagnostic usefulness of the combined COMPASS 31 questionnaire and electrochemical skin conductance for diabetic cardiovascular autonomic neuropathy and diabetic polyneuropathy. J Peripher Nerv Syst 2020;25:44-53.
Treister R, O'neil K, Downs HM, Oaklander AL. Validation of the composite autonomic symptom scale 31 (COMPASS-31) in patients with and without small fiber polyneuropathy. Eur J Neurol 2015;22:1124-30.
Crnošija L, Krbot Skorić M, Andabaka M, et al. Autonomic dysfunction in people with neuromyelitis optica spectrum disorders. Mult Scler 2020;26:688-95.
Kang JH, Kim JK, Hong SH, Lee CH, Choi BY. Heart rate variability for quantification of autonomic dysfunction in fibromyalgia. Ann Rehabil Med 2016;40:301-9.
Adler BL, Russell JW, Hummers LK, Mcmahan ZH. Symptoms of autonomic dysfunction in systemic sclerosis assessed by the COMPASS-31 questionnaire. J Rheumatol 2018;45:1145-52.
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;169:13-21.
Shahani BT, Halperin JJ, Boulu P, Cohen J. Sympathetic skin response-a method of assessing unmyelinated axon dysfunction in peripheral neuropathies. J Neurol Neurosurg Psychiatry 1984;47:536-42.
Pelz JO, Belau E, Henn P, Hammer N, Classen J, Weise D. Sonographic evaluation of the vagus nerves: protocol, reference values, and side-to-side differences. Muscle Nerve 2018;57:766-71.
Papadopoulou M, Papapostolou A, Bakola E, et al. Neurophysiological and ultrasonographic comparative study of autonomous nervous system in patients suffering from fibromyalgia and generalized anxiety disorder. Neurol Sci 2021;43:2813-2821.
Kerasnoudis A, Tsivgoulis G. Nerve ultrasound in peripheral neuropathies: a review. J Neuroimaging 2015;25:528-38.
Takahashi H, Oyanagi K, Ohama E, Ikuta F. Clarke's column in sporadic amyotrophic lateral sclerosis. Acta Neuropathol 1992;84:465-70.
Takahashi H, Oyanagi K, Ikuta F. The intermediolateral nucleus in sporadic amyotrophic lateral sclerosis. Acta Neuropathol 1993;86:190-2.
Cartwright MS, Passmore LV, Yoon J-S, Brown ME, Caress JB, Walker FO. Cross-sectional area reference values for nerve ultrasonography. Muscle Nerve 2008;37:566-71.
Walter U, Tsiberidou P, Kersten M, Storch A, Löhle M. Atrophy of the vagus nerve in Parkinson's disease revealed by high-resolution ultrasonography. Front Neurol 2018;9:805.
Grimm A, Décard BF, Athanasopoulou I, Schweikert K, Sinnreich M, Axer H. Nerve ultrasound for differentiation between amyotrophic lateral sclerosis and multifocal motor neuropathy. J Neurol 2015;262:870-80.
Gray H. 1918. Anatomy of the human body. Accessed January 29, 2022. https://www.bartleby.com/107/
Shimizu T. Sympathetic hyperactivity and sympathovagal imbalance in amyotrophic lateral sclerosis. Eur Neurol Rev 2013;8:46-50.
Xu L, Pu J. Alpha-synuclein in Parkinson's disease: from pathogenetic dysfunction to potential clinical application. Parkinsons Dis 2016;2016:1720621.

Auteurs

Marianna Papadopoulou (M)

Department of Physiotherapy, Laboratory of Neuromuscular and Cardiovascular Study of Motion, University of West Attica, Athens, Greece.
Second Department of Neurology, National and Kapodistrian University of Athens, School of Medicine, Attikon University Hospital, Athens, Greece.

Eleni Bakola (E)

Second Department of Neurology, National and Kapodistrian University of Athens, School of Medicine, Attikon University Hospital, Athens, Greece.

Apostolos Papapostolou (A)

Second Department of Neurology, National and Kapodistrian University of Athens, School of Medicine, Attikon University Hospital, Athens, Greece.

Maria Ioanna Stefanou (MI)

Second Department of Neurology, National and Kapodistrian University of Athens, School of Medicine, Attikon University Hospital, Athens, Greece.

Christos Moschovos (C)

Second Department of Neurology, National and Kapodistrian University of Athens, School of Medicine, Attikon University Hospital, Athens, Greece.

Stavroula Salakou (S)

Second Department of Neurology, National and Kapodistrian University of Athens, School of Medicine, Attikon University Hospital, Athens, Greece.

Panagiotis Zis (P)

Second Department of Neurology, National and Kapodistrian University of Athens, School of Medicine, Attikon University Hospital, Athens, Greece.
Medical School, University of Cyprus, Nicosia, Cyprus.
Medical School, University of Sheffield, Sheffield, UK.

Vasiliki Zouvelou (V)

First Department of Neurology, National and Kapodistrian University of Athens, School of Medicine, Eginitio University Hospital, Athens, Greece.

Vasilios K Kimiskidis (VK)

First Department of Neurology, School of Medicine, Aristotle University of Thessaloniki, Thessaloniki, Greece.

Elisabeth Chroni (E)

Department of Neurology, School of Medicine, University of Patras, Rio-Patras, Greece.

Georgios Tsivgoulis (G)

Second Department of Neurology, National and Kapodistrian University of Athens, School of Medicine, Attikon University Hospital, Athens, Greece.

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