Electrodiagnostic subtyping in Guillain-Barré syndrome patients in the International Guillain-Barré Outcome Study

Samuel Arends; Judith Drenthen; Laura de Koning; Peter van den Bergh; Robert D M Hadden; Satoshi Kuwabara; Ricardo C Reisin; Nortina Shahrizaila; Senda Ajroud-Driss; Giovanni Antonini; Shahram Attarian; Claudia Balducci; Tulio Bertorini; Thomas H Brannagan; Guido Cavaletti; Chi-Chao Chao; Govind Chavada; Klaus-Ulrich Dillmann; Mazen M Dimachkie; Giuliana Galassi; Gerardo Gutiérrez-Gutiérrez; Thomas Harbo; Badrul Islam; Zhahirul Islam; Hans Katzberg; Susumu Kusunoki; Fiore Manganelli; James A L Miller; Julio Pardo; Yann Pereon; Yusuf A Rajabally; Soren Sindrup; Mark Stettner; Antonino Uncini; Camiel Verhamme; Michal Vytopil; Waqar Waheed; Bart C Jacobs; David R Cornblath; IGOS Consortium

doi:10.1111/ene.16335

Electrodiagnostic subtyping in Guillain-Barré syndrome patients in the International Guillain-Barré Outcome Study

Eur J Neurol. 2024 Sep;31(9):e16335. doi: 10.1111/ene.16335. Epub 2024 Jul 4.

Authors

Samuel Arends^{1

2}, Judith Drenthen¹, Laura de Koning¹, Peter van den Bergh³, Robert D M Hadden⁴, Satoshi Kuwabara⁵, Ricardo C Reisin⁶, Nortina Shahrizaila⁷, Senda Ajroud-Driss⁸, Giovanni Antonini⁹, Shahram Attarian¹⁰, Claudia Balducci¹¹, Tulio Bertorini¹², Thomas H Brannagan¹³, Guido Cavaletti¹¹, Chi-Chao Chao¹⁴, Govind Chavada¹⁵, Klaus-Ulrich Dillmann¹⁶, Mazen M Dimachkie¹⁷, Giuliana Galassi¹⁸, Gerardo Gutiérrez-Gutiérrez¹⁹, Thomas Harbo²⁰, Badrul Islam²¹, Zhahirul Islam²², Hans Katzberg²³, Susumu Kusunoki²⁴, Fiore Manganelli²⁵, James A L Miller²⁶, Julio Pardo²⁷, Yann Pereon²⁸, Yusuf A Rajabally²⁹, Soren Sindrup³⁰, Mark Stettner³¹, Antonino Uncini³², Camiel Verhamme³³, Michal Vytopil³⁴, Waqar Waheed³⁵, Bart C Jacobs^{1

36}, David R Cornblath³⁷; IGOS Consortium

Collaborators

IGOS Consortium:
James M Addington, Umesh A Badrising, Fabio A Barroso, Kathleen Bateman, Isabelita Bella, Luana Benedetti, Bianca van den Berg, Ratna Bhavaraju-Sanka, Chiara Briani, Jan Buermann, Mark Busby, Steven Butterworth, Carlos Casasnovas, Shan Chen, Kristl Claeys, Eugenia Conti, Jeremy S Cosgrove, Marinos Dalakas, Philip van Damme, Efthimios Dardiotis, Amy Davidson, Alex Doets, Pieter van Doorn, Andoni Echaniz-Laguna, Filip Eftimov, Karin G Faber, Raffaella Fazio, Thomas E Feasby, Janev Fehmi, Chris Fokke, Toshiki Fujioka, Ernesto Fulgenzi, Marcel P J Garssen, Cees J Gijsbers, James M Gilchrist, Job Gilhuis, Jonathan M Goldstein, Kenneth C Gorson, Namita Goyal, Volkan Granit, Ludwig Gutmann, Hans-Peter Hartung, James K L Holt, Sung-Tsang Hsieh, Min Htut, Richard A C Hughes, Ivonne Jericó-Pascual, Kenichi Kaida, Summer Karafiath, Mohammad Ali Khoshnoodi, Lynette Kiers, Ruud P Kleiweg, Norito Kokubun, Noah A Kolb, Rinske van Koningsveld, Anneke J van der Kooi, Hans Kramers, Krista Kuitwaard, Justin Y Kwan, Shafeeq S Ladha, Lisbeth Landschoff Lassen, Victoria H Lawson, Helmar Lehmann, Luciana Leon Cejas, Sonja E Leonhard, Linda Luijten, Michael P T Lunn, Hadi Manji, Girolama A Marfia, Celedonio Márquez Infante, Lorena Martín-Aguilar, Eugenia Martinez-Hernandez, Giorgia Mataluni, Marcelo Mattiazzi, Christopher McDermott, Gregg Meekins, Quazi Deen Mohammad, Soledad Monges, Germán Moris de la Tassa, Caterina Nascimbene, Eduardo Nobile-Orazio, Richard J Nowak, Michael Osei-Bonsu, Farah Pelouto, Michael T Pulley, Luis Querol Gutiérrez, Stephen W Reddel, Taco van der Ree, Simon Rinaldi, Paolo Ripellino, Rhys C Roberts, Iñigo Rojas-Marcos, Joyce Roodbol, Stacy A Rudnicki, George M Sachs, Johnny P A Samijn, Lucio Santoro, Angelo Schenone, Maria José Sedano Tous, Kazim A Sheikh, Nicholas Joseph Silvestri, Soeren H Sundrup, Claudia Sommer, Beth Stein, Amro Maher Stino, Robin C M Thomma, Paul Twydell, Jay D Varrato, Frederique H Vermeij, Jan Verschuuren, Leo H Visser, Christa Walgaard, Yuzhong Wang, Hugh J Willison, Paul W Wirtz, Marieke van Woerkom, Sascha A Zivkovic

Affiliations

¹ Department of Neurology, Erasmus University Medical Center, Rotterdam, The Netherlands.
² Department of Neurology, HagaZiekenhuis, The Hague, The Netherlands.
³ Department of Neurology, University Hospital St-Luc, Brussels, Belgium.
⁴ Department of Neurology, King's College Hospital, London, UK.
⁵ Department of Neurology, Chiba University Hospital, Chiba, Japan.
⁶ Department of Neurology, Hospital Británico, Buenos Aires, Argentina.
⁷ Department of Neurology, University of Malaya, Kuala Lumpur, Malaysia.
⁸ Department of Neurology, Northwestern University Feinberg, Chicago, Illinois, USA.
⁹ Department of Neuroscience, Mental Health and Sensory Organs (NESMOS), Sapienza University, Rome, Italy.
¹⁰ Department Neuromuscular disorders, Hôpital de la Timone, Marseille, France.
¹¹ Department of Neurology, San Gerardo Hospital, Monza, Italy.
¹² University of Tennessee Health Science Center, Department of Neurology, Memphis, Tennessee, USA.
¹³ Department of Neurology, Colombia University, New York, New York, USA.
¹⁴ Department of Neurology, National Taiwan University Hospital, Taipei, Taiwan.
¹⁵ Department of Neurology, Southern General Hospital, University of Glasgow, Glasgow, UK.
¹⁶ Department of Neurology, Universitätsklinikum des Saarlandes, Homburg, Germany.
¹⁷ Department of Neurology, University of Kansas Medical Center, Kansas City, Kansas, USA.
¹⁸ Department of Neurology, University Hospital of Modena, Modena, Italy.
¹⁹ Department of Neurology, Hospital Universitario Infanta Sofia, Universidad Europea de Madrid, San Sebastian de los Reyes, Spain.
²⁰ Department of Neurology, Aarhus University Hospital, Aarhus, Denmark.
²¹ Department of Neurology and Neurophysiology, BRB Hospital, Dhaka, Bangladesh.
²² International Centre for Diarrhoeal Disease Research (icddr;b), Laboratory of Gut-Brain Axis, Dhaka, Bangladesh.
²³ University of Toronto, Department of Neurology, Toronto, Canada.
²⁴ Department of Neurology, Kindai University, Osaka, Japan.
²⁵ Department of Neuroscience, Reproductive Sciences and Odontostomatology, University of Naples "Federico II", Naples, Italy.
²⁶ Department of Neurology, Royal Victoria Infirmary, Newcastle, UK.
²⁷ Department of Neurology, Complejo Hospitalario Universitario de Santiago, Santiago de Compostela, Spain.
²⁸ Department of Clinical Neurophysiology, Nantes University Hospital, Nantes, France.
²⁹ Aston Medical School, Aston University, Birmingham, UK.
³⁰ Odense University Hospital, Department of Neurology, Odense, Denmark.
³¹ Department of Neurology and Center for Translational Neuro- and Behavioral Sciences (C-TNBS), University Medicine Essen, Essen, Germany.
³² Department of Neuroscience, Imaging and Clinical Sciences, University 'G. D'Annunzio', Chieti, Italy.
³³ Department of Neurology, Amsterdam Neuroscience, Amsterdam University Medical Centers, University of Amsterdam, Amsterdam, The Netherlands.
³⁴ Department of Neurology, Lahey Hospital and Medical Center, Burlington, Vermont, USA.
³⁵ Department of Neurology, University of Vermont Medical Centre, Burlington, Vermont, USA.
³⁶ Department of Immunology, Erasmus University Medical Center, Rotterdam, The Netherlands.
³⁷ Department of Neurology, Johns Hopkins University, Baltimore, Vermont, USA.

Abstract

Background and purpose: Various electrodiagnostic criteria have been developed in Guillain-Barré syndrome (GBS). Their performance in a broad representation of GBS patients has not been evaluated. Motor conduction data from the International GBS Outcome Study (IGOS) cohort were used to compare two widely used criterion sets and relate these to diagnostic amyotrophic lateral sclerosis criteria.

Methods: From the first 1500 patients in IGOS, nerve conduction studies from 1137 (75.8%) were available for the current study. These patients were classified according to nerve conduction studies criteria proposed by Hadden and Rajabally.

Results: Of the 1137 studies, 68.3% (N = 777) were classified identically according to criteria by Hadden and Rajabally: 111 (9.8%) axonal, 366 (32.2%) demyelinating, 195 (17.2%) equivocal, 35 (3.1%) inexcitable and 70 (6.2%) normal. Thus, 360 studies (31.7%) were classified differently. The areas of differences were as follows: 155 studies (13.6%) classified as demyelinating by Hadden and axonal by Rajabally; 122 studies (10.7%) classified as demyelinating by Hadden and equivocal by Rajabally; and 75 studies (6.6%) classified as equivocal by Hadden and axonal by Rajabally. Due to more strictly defined cutoffs fewer patients fulfilled demyelinating criteria by Rajabally than by Hadden, making more patients eligible for axonal or equivocal classification by Rajabally. In 234 (68.6%) axonal studies by Rajabally the revised El Escorial (amyotrophic lateral sclerosis) criteria were fulfilled; in axonal cases by Hadden this was 1.8%.

Conclusions and discussion: This study shows that electrodiagnosis in GBS is dependent on the criterion set utilized, both of which are based on expert opinion. Reappraisal of electrodiagnostic subtyping in GBS is warranted.

Keywords: Guillain–Barré syndrome; amyotrophic lateral sclerosis; electrodiagnosis; nerve conduction studies; polyneuropathy.

MeSH terms

Adult
Aged
Amyotrophic Lateral Sclerosis / classification
Amyotrophic Lateral Sclerosis / diagnosis
Amyotrophic Lateral Sclerosis / physiopathology
Cohort Studies
Electrodiagnosis* / methods
Female
Guillain-Barre Syndrome* / classification
Guillain-Barre Syndrome* / diagnosis
Guillain-Barre Syndrome* / physiopathology
Humans
Male
Middle Aged
Neural Conduction* / physiology