CSF Findings in Relation to Clinical Characteristics, Subtype, and Disease Course in Patients With Guillain-Barré Syndrome

doi:10.1212/WNL.0000000000207282

. 2023 Jun 6;100(23):e2386-e2397.

doi: 10.1212/WNL.0000000000207282. Epub 2023 Apr 19.

CSF Findings in Relation to Clinical Characteristics, Subtype, and Disease Course in Patients With Guillain-Barré Syndrome

Helle Al-Hakem¹, Alex Y Doets¹, Amro Maher Stino¹, Sasha A Zivkovic¹, Henning Andersen¹, Hugh J Willison¹, David R Cornblath¹, Kenneth C Gorson¹, Zhahirul Islam¹, Quazi Deen Mohammad¹, Søren Hein Sindrup¹, Susumu Kusunoki¹, Amy Davidson¹, Carlos Casasnovas¹, Kathleen Bateman¹, James A L Miller¹, Bianca van den Berg¹, Christine Verboon¹, Joyce Roodbol¹, Sonja E Leonhard¹, Samuel Arends¹, Linda W G Luijten¹, Luana Benedetti¹, Satoshi Kuwabara¹, Peter Van den Bergh¹, Soledad Monges¹, Girolama A Marfia¹, Nortina Shahrizaila¹, Giuliana Galassi¹, Yann Pereon¹, Jan Bürmann¹, Krista Kuitwaard¹, Ruud P Kleyweg¹, Cintia Marchesoni¹, María J Sedano Tous¹, Luis Querol¹, Lorena Martín-Aguilar¹, Yuzhong Wang¹, Eduardo Nobile-Orazio¹, Simon Rinaldi¹, Angelo Schenone¹, Julio Pardo¹, Frederique H Vermeij¹, Waqar Waheed¹, Helmar C Lehmann¹, Volkan Granit¹, Beth Stein¹, Guido Cavaletti¹, Gerardo Gutiérrez-Gutiérrez¹, Fabio A Barroso¹, Leo H Visser¹, Hans D Katzberg¹, Efthimios Dardiotis¹, Shahram Attarian¹, Anneke J van der Kooi¹, Filip Eftimov¹, Paul W Wirtz¹, Johnny P A Samijn¹, H Jacobus Gilhuis¹, Robert D M Hadden¹, James K L Holt¹, Kazim A Sheikh¹, Noah Kolb¹, Summer Karafiath¹, Michal Vytopil¹, Giovanni Antonini¹, Thomas E Feasby¹, Catharina Faber¹, Hans Kramers¹, Mark Busby¹, Rhys C Roberts¹, Nicholas J Silvestri¹, Raffaella Fazio¹, Gert W van Dijk¹, Marcel P J Garssen¹, Jan Verschuuren¹, Thomas Harbo¹, Bart C Jacobs²; IGOS Consortium

Collaborators, Affiliations

Collaborators

IGOS Consortium:
R A C Hughes, H P Hartung, L C de Koning, M Mandarakas, M van Woerkom, R C Reisin, S W Reddel, S T Hsieh, J M Addington, S Ajroud-Driss, L Alessandro, U A Badrising, G Balloy, I R Bella, T E Bertorini, R Bhavaraju-Sanka, M Bianco, T H Brannagan, K Brennan, C Briani, S Butterworth, C C Chao, S Chen, K G Claeys, M E Conti, J S Cosgrove, M C Dalakas, M Derejko, M M Dimachkie, A Echaniz-Laguna, C Fokke, T Fujioka, E A Fulgenzi, T García Sobrino, C J Gijsbers, J M Gilchrist, J M Goldstein, J Goodfellow, N A Goyal, S Grisanti, L Gutmann, M Htut, K Jellema, I Jericó Pascual, M C Jimeno-Montero, K Kaida, H Kerkhoff, M Khoshnoodi, L Kiers, M Kuwahara, J Y Kwan, S S Ladha, L Landschoff Lassen, V Lawson, E Lee Pan, M P T Lunn, H Manji, C Márquez Infante, E Martinez Hernandez, G Mataluni, M G Mattiazzi, C J McDermott, G D Meekins, G Morís de la Tassa, C Nascimbene, R J Nowak, P Orizaola, M Osei-Bonsu, A Pardal, E Pascual-Goñi, R M Pascuzzi, V Prada, M Pulley, I Rojas-Marcos, S A Rudnicki, G M Sachs, L Santoro, A Savransky, L Schwindling, Y Sekiguchi, C L Sommer, C-Y Tan, H Tankisi, P T Twydell, P van Damme, T van der Ree, R van Koningsveld, J D Varrato, V Vélez Santamaria, C Walgaard, Y Yamagishi, L Zhang, Mm, L Zhou

Affiliations

¹ From the Department of Neurology (H.A.-H., H.A., T.H.), Aarhus University Hospital, Denmark; Department of Neurology (A.Y.D., B.v.d.B., C.V., J.R., S.E.L., S. Arends, L.W.G.L., K.K., B.C.J.), Erasmus MC, University Medical Centre Rotterdam, the Netherlands; Department of Neurology (A.M.S.), University of Michigan School of Medicine, Ann Arbor; Department of Neurology (S.A.Z.), University of Pittsburgh Medical Center, PA; Department of Neurology (H.J.W., A.D.), College of Medical, Veterinary and Life Sciences, University of Glasgow, United Kingdom; Department of Neurology (D.R.C.), Johns Hopkins University School of Medicine, Baltimore, MD; Department of Neurology (K.C.G.), St. Elizabeth's Medical Centre, Tufts University, School of Medicine, Boston, MA; Laboratory of Gut-Brain Signaling (Z.I.); Laboratory Sciences and Services Division (LSSD) (Z.I.), icddr,b; National Institute of Neurosciences and Hospital (Q.D.M.), Dhaka, Bangladesh; Department of Neurology (S.H.S.), Odense University Hospital and University of Southern Denmark; Department of Neurology (S. Kusunoki), Kindai University Faculty of Medicine, Osaka-Sayama City, Japan; Department of Neurology (C.C.), Neuromuscular Unit, Bellvitge University Hospital-IDIBELL, CIBERER, Barcelona, Spain; Division of Neurology (K.B.), Department of Medicine, Groote Schuur Hospital, University of Cape Town, South Africa; Department of Neurology (J.A.L.M.), Royal Victoria Infirmary, Newcastle upon Tyne Hospitals NHS Foundation Trust, United Kingdom; Department of Neurology (B.v.d.B., H.K.), Franciscus Gasthuis & Vlietland (location: Vlietland Hospital), Schiedam; Department of Neurology (S. Arends, P.W.W.), Haga Hospital, Den Haag; Department of Neurology (L.W.G.L., L.H.V.), St. Elisabeth-TweeSteden Hospital, Tilburg, the Netherlands; Department of Neurology (L.B.), IRCCS Ospedale Policlinico San Martino, Genova, Italy; Department of Neurology (S. Kuwabara), Chiba University, Chuo-ku, Japan; Department of Neurology (P.V.d.B.), Neuromuscular Reference Centre, University Hospital Saint-Luc, University of Louvain, Brussels, Belgium; Department of Neurology (S.M.), Hospital de Pediatría J.P. Garrahan, Buenos Aires, Argentina; Dysimmune Neuropathies Unit (G.A.M.), Department of Systems Medicine, Tor Vergata University Hospital, Rome, Italy; Department of Medicine (N.S.), University of Malaya, Kuala Lumpur, Malaysia; Department of Neurology (G.G.), University Hospital of Modena, Italy; Department of Clinical Neurophysiology (Y.P.), Reference Centre for NMD, CHU Nantes, Nantes, France; Department of Neurology (J.B.), Saarland University Medical School, Homburg (previous hospital), and MVZ Pfalzklinikum (J.B.), Kusel, Germany (current hospital); Department of Neurology (K.K., R.P.K.), Albert Schweitzer Hospital, Dordrecht, the Netherlands; Department of Neurology (C.M.), Hospital Británico, Buenos Aires, Argentina; Department of Neurology (M.J.S.T.), Hospital Marques de Valdecilla, Santander; Department of Neurology (L.Q., L.M.-A.), Hospital de la Santa Creu i Sant Pau, Universitat Autònoma de Barcelona, CIBERER and ERN-NMD, Spain; Department of Neurology (Y.W.), Affiliated Hospital of Jining Medical University, Shandong Province, China; Neuromuscular and Neuroimmunology Service (E.N.-O.), IRCCS Humanitas Research Hospital, Milan University, Italy; Nuffield Department of Clinical Neurosciences (S.R.), University of Oxford and Oxford University Hospitals NHS Foundation Trust, United Kingdom; Department of Neurosciences, Ophthalmology, Rehabilitation, Genetics and Maternal Sciences (A.S.), University of Genova, and IRCCS San Martino Hospital (A.S.), Genova, Italy; Department of Neurology (J.P.), Hospital Clínico de Santiago, Travesia Choupana, Santiago de Compostela (A Coruña), Spain; Department of Neurology (F.H.V.), Franciscus Gasthuis & Vlietland (location: Franciscus Gasthuis), Rotterdam, the Netherlands; Department of Neurology (W.W., N.K.), University of Vermont Medical Centre, Burlington; Department of Neurology (H.C.L.), University Hospital of Cologne, Germany; Department of Neurology (V.G., B.S.), Montefiore Medical Center, Bronx, NY; Department of Neurology (G.C.), University Milano-Bicocca, Monza, Italy; Department of Neurology (G.G.-G.), Hospital Universitario Infanta Sofía, San Sebastián de los Reyes, Spain; Department of Neurology (F.A.B.), Instituto de Investigaciones Neurológicas Raúl Carrea, FLENI, Buenos Aires, Argentina; Department of Neurology (H.D.K.), University Health Network, University of Toronto, Ontario, Canada; Department of Neurology (E.D.), University Hospital of Larissa, Greece; Department of Neurology (S. Attarian), Reference Centre for NMD, CHU Timone ERN NMD, Marseille, France; Department of Neurology (A.J.v.d.K., F.E.), Amsterdam University Medical Centre, University of Amsterdam, Neuroscience Institute; Department of Neurology (J.P.A.S.), Maasstad Hospital, Rotterdam; Department of Neurology (H.J.G.), Reinier de Graaf Hospital, Reinier de Graafweg, Delft, the Netherlands; Department of Neurology (R.D.M.H.), King's College Hospital, Denmark Hill, London; Department of Neurology (J.K.L.H.), The Walton Centre, Liverpool, United Kingdom; Department of Neurology (K.A.S.), University of Texas Health Science Centre at Houston; Department of Biology (N.K., S. Karafiath), Utah Valley University, Orem; Department of Neurology (M.V.), Lahey Hospital and Medical Center, Tufts University School of Medicine, Burlington, MA; Department of Neurology, Mental Health and Sensory Organs (NESMOS) (G.A.), Faculty of Medicine and Psychology, University of Rome "Sapienza," Sant' Andrea Hospital, Italy; Department of Clinical Neurosciences (T.E.F.), University of Calgary, Alberta, Canada; Department of Neurology (C.F.), Maastricht University Medical Centre, the Netherlands; Department of Neurology (M.B.), Leeds Teaching Hospitals; Department of Neurology (R.C.R.), Addenbrooke's Hospital, Cambridge, United Kingdom; Department of Neurology (N.J.S.), University at Buffalo Jacobs School of Medicine and Biomedical Sciences, NY; Department of Neurology (R.F.), Scientific Institute San Raffaele, Milano, Italy; Department of Neurology (G.W.v.D.), Canisius Wilhelmina Hospital, Nijmegen; Department of Neurology (M.P.J.G.), Jeroen Bosch Hospital, 's-Hertogenbosch; Department of Neurology (J.V.), Leiden University Medical Centre; and Department of Immunology (B.C.J.), Erasmus MC, University Medical Centre Rotterdam, the Netherlands.
² From the Department of Neurology (H.A.-H., H.A., T.H.), Aarhus University Hospital, Denmark; Department of Neurology (A.Y.D., B.v.d.B., C.V., J.R., S.E.L., S. Arends, L.W.G.L., K.K., B.C.J.), Erasmus MC, University Medical Centre Rotterdam, the Netherlands; Department of Neurology (A.M.S.), University of Michigan School of Medicine, Ann Arbor; Department of Neurology (S.A.Z.), University of Pittsburgh Medical Center, PA; Department of Neurology (H.J.W., A.D.), College of Medical, Veterinary and Life Sciences, University of Glasgow, United Kingdom; Department of Neurology (D.R.C.), Johns Hopkins University School of Medicine, Baltimore, MD; Department of Neurology (K.C.G.), St. Elizabeth's Medical Centre, Tufts University, School of Medicine, Boston, MA; Laboratory of Gut-Brain Signaling (Z.I.); Laboratory Sciences and Services Division (LSSD) (Z.I.), icddr,b; National Institute of Neurosciences and Hospital (Q.D.M.), Dhaka, Bangladesh; Department of Neurology (S.H.S.), Odense University Hospital and University of Southern Denmark; Department of Neurology (S. Kusunoki), Kindai University Faculty of Medicine, Osaka-Sayama City, Japan; Department of Neurology (C.C.), Neuromuscular Unit, Bellvitge University Hospital-IDIBELL, CIBERER, Barcelona, Spain; Division of Neurology (K.B.), Department of Medicine, Groote Schuur Hospital, University of Cape Town, South Africa; Department of Neurology (J.A.L.M.), Royal Victoria Infirmary, Newcastle upon Tyne Hospitals NHS Foundation Trust, United Kingdom; Department of Neurology (B.v.d.B., H.K.), Franciscus Gasthuis & Vlietland (location: Vlietland Hospital), Schiedam; Department of Neurology (S. Arends, P.W.W.), Haga Hospital, Den Haag; Department of Neurology (L.W.G.L., L.H.V.), St. Elisabeth-TweeSteden Hospital, Tilburg, the Netherlands; Department of Neurology (L.B.), IRCCS Ospedale Policlinico San Martino, Genova, Italy; Department of Neurology (S. Kuwabara), Chiba University, Chuo-ku, Japan; Department of Neurology (P.V.d.B.), Neuromuscular Reference Centre, University Hospital Saint-Luc, University of Louvain, Brussels, Belgium; Department of Neurology (S.M.), Hospital de Pediatría J.P. Garrahan, Buenos Aires, Argentina; Dysimmune Neuropathies Unit (G.A.M.), Department of Systems Medicine, Tor Vergata University Hospital, Rome, Italy; Department of Medicine (N.S.), University of Malaya, Kuala Lumpur, Malaysia; Department of Neurology (G.G.), University Hospital of Modena, Italy; Department of Clinical Neurophysiology (Y.P.), Reference Centre for NMD, CHU Nantes, Nantes, France; Department of Neurology (J.B.), Saarland University Medical School, Homburg (previous hospital), and MVZ Pfalzklinikum (J.B.), Kusel, Germany (current hospital); Department of Neurology (K.K., R.P.K.), Albert Schweitzer Hospital, Dordrecht, the Netherlands; Department of Neurology (C.M.), Hospital Británico, Buenos Aires, Argentina; Department of Neurology (M.J.S.T.), Hospital Marques de Valdecilla, Santander; Department of Neurology (L.Q., L.M.-A.), Hospital de la Santa Creu i Sant Pau, Universitat Autònoma de Barcelona, CIBERER and ERN-NMD, Spain; Department of Neurology (Y.W.), Affiliated Hospital of Jining Medical University, Shandong Province, China; Neuromuscular and Neuroimmunology Service (E.N.-O.), IRCCS Humanitas Research Hospital, Milan University, Italy; Nuffield Department of Clinical Neurosciences (S.R.), University of Oxford and Oxford University Hospitals NHS Foundation Trust, United Kingdom; Department of Neurosciences, Ophthalmology, Rehabilitation, Genetics and Maternal Sciences (A.S.), University of Genova, and IRCCS San Martino Hospital (A.S.), Genova, Italy; Department of Neurology (J.P.), Hospital Clínico de Santiago, Travesia Choupana, Santiago de Compostela (A Coruña), Spain; Department of Neurology (F.H.V.), Franciscus Gasthuis & Vlietland (location: Franciscus Gasthuis), Rotterdam, the Netherlands; Department of Neurology (W.W., N.K.), University of Vermont Medical Centre, Burlington; Department of Neurology (H.C.L.), University Hospital of Cologne, Germany; Department of Neurology (V.G., B.S.), Montefiore Medical Center, Bronx, NY; Department of Neurology (G.C.), University Milano-Bicocca, Monza, Italy; Department of Neurology (G.G.-G.), Hospital Universitario Infanta Sofía, San Sebastián de los Reyes, Spain; Department of Neurology (F.A.B.), Instituto de Investigaciones Neurológicas Raúl Carrea, FLENI, Buenos Aires, Argentina; Department of Neurology (H.D.K.), University Health Network, University of Toronto, Ontario, Canada; Department of Neurology (E.D.), University Hospital of Larissa, Greece; Department of Neurology (S. Attarian), Reference Centre for NMD, CHU Timone ERN NMD, Marseille, France; Department of Neurology (A.J.v.d.K., F.E.), Amsterdam University Medical Centre, University of Amsterdam, Neuroscience Institute; Department of Neurology (J.P.A.S.), Maasstad Hospital, Rotterdam; Department of Neurology (H.J.G.), Reinier de Graaf Hospital, Reinier de Graafweg, Delft, the Netherlands; Department of Neurology (R.D.M.H.), King's College Hospital, Denmark Hill, London; Department of Neurology (J.K.L.H.), The Walton Centre, Liverpool, United Kingdom; Department of Neurology (K.A.S.), University of Texas Health Science Centre at Houston; Department of Biology (N.K., S. Karafiath), Utah Valley University, Orem; Department of Neurology (M.V.), Lahey Hospital and Medical Center, Tufts University School of Medicine, Burlington, MA; Department of Neurology, Mental Health and Sensory Organs (NESMOS) (G.A.), Faculty of Medicine and Psychology, University of Rome "Sapienza," Sant' Andrea Hospital, Italy; Department of Clinical Neurosciences (T.E.F.), University of Calgary, Alberta, Canada; Department of Neurology (C.F.), Maastricht University Medical Centre, the Netherlands; Department of Neurology (M.B.), Leeds Teaching Hospitals; Department of Neurology (R.C.R.), Addenbrooke's Hospital, Cambridge, United Kingdom; Department of Neurology (N.J.S.), University at Buffalo Jacobs School of Medicine and Biomedical Sciences, NY; Department of Neurology (R.F.), Scientific Institute San Raffaele, Milano, Italy; Department of Neurology (G.W.v.D.), Canisius Wilhelmina Hospital, Nijmegen; Department of Neurology (M.P.J.G.), Jeroen Bosch Hospital, 's-Hertogenbosch; Department of Neurology (J.V.), Leiden University Medical Centre; and Department of Immunology (B.C.J.), Erasmus MC, University Medical Centre Rotterdam, the Netherlands. b.jacobs@erasmusmc.nl.

PMID: 37076309
PMCID: PMC10256127
DOI: 10.1212/WNL.0000000000207282

CSF Findings in Relation to Clinical Characteristics, Subtype, and Disease Course in Patients With Guillain-Barré Syndrome

Helle Al-Hakem et al. Neurology. 2023.

. 2023 Jun 6;100(23):e2386-e2397.

doi: 10.1212/WNL.0000000000207282. Epub 2023 Apr 19.

Authors

Collaborators

IGOS Consortium:
R A C Hughes, H P Hartung, L C de Koning, M Mandarakas, M van Woerkom, R C Reisin, S W Reddel, S T Hsieh, J M Addington, S Ajroud-Driss, L Alessandro, U A Badrising, G Balloy, I R Bella, T E Bertorini, R Bhavaraju-Sanka, M Bianco, T H Brannagan, K Brennan, C Briani, S Butterworth, C C Chao, S Chen, K G Claeys, M E Conti, J S Cosgrove, M C Dalakas, M Derejko, M M Dimachkie, A Echaniz-Laguna, C Fokke, T Fujioka, E A Fulgenzi, T García Sobrino, C J Gijsbers, J M Gilchrist, J M Goldstein, J Goodfellow, N A Goyal, S Grisanti, L Gutmann, M Htut, K Jellema, I Jericó Pascual, M C Jimeno-Montero, K Kaida, H Kerkhoff, M Khoshnoodi, L Kiers, M Kuwahara, J Y Kwan, S S Ladha, L Landschoff Lassen, V Lawson, E Lee Pan, M P T Lunn, H Manji, C Márquez Infante, E Martinez Hernandez, G Mataluni, M G Mattiazzi, C J McDermott, G D Meekins, G Morís de la Tassa, C Nascimbene, R J Nowak, P Orizaola, M Osei-Bonsu, A Pardal, E Pascual-Goñi, R M Pascuzzi, V Prada, M Pulley, I Rojas-Marcos, S A Rudnicki, G M Sachs, L Santoro, A Savransky, L Schwindling, Y Sekiguchi, C L Sommer, C-Y Tan, H Tankisi, P T Twydell, P van Damme, T van der Ree, R van Koningsveld, J D Varrato, V Vélez Santamaria, C Walgaard, Y Yamagishi, L Zhang, Mm, L Zhou

Affiliations

¹ From the Department of Neurology (H.A.-H., H.A., T.H.), Aarhus University Hospital, Denmark; Department of Neurology (A.Y.D., B.v.d.B., C.V., J.R., S.E.L., S. Arends, L.W.G.L., K.K., B.C.J.), Erasmus MC, University Medical Centre Rotterdam, the Netherlands; Department of Neurology (A.M.S.), University of Michigan School of Medicine, Ann Arbor; Department of Neurology (S.A.Z.), University of Pittsburgh Medical Center, PA; Department of Neurology (H.J.W., A.D.), College of Medical, Veterinary and Life Sciences, University of Glasgow, United Kingdom; Department of Neurology (D.R.C.), Johns Hopkins University School of Medicine, Baltimore, MD; Department of Neurology (K.C.G.), St. Elizabeth's Medical Centre, Tufts University, School of Medicine, Boston, MA; Laboratory of Gut-Brain Signaling (Z.I.); Laboratory Sciences and Services Division (LSSD) (Z.I.), icddr,b; National Institute of Neurosciences and Hospital (Q.D.M.), Dhaka, Bangladesh; Department of Neurology (S.H.S.), Odense University Hospital and University of Southern Denmark; Department of Neurology (S. Kusunoki), Kindai University Faculty of Medicine, Osaka-Sayama City, Japan; Department of Neurology (C.C.), Neuromuscular Unit, Bellvitge University Hospital-IDIBELL, CIBERER, Barcelona, Spain; Division of Neurology (K.B.), Department of Medicine, Groote Schuur Hospital, University of Cape Town, South Africa; Department of Neurology (J.A.L.M.), Royal Victoria Infirmary, Newcastle upon Tyne Hospitals NHS Foundation Trust, United Kingdom; Department of Neurology (B.v.d.B., H.K.), Franciscus Gasthuis & Vlietland (location: Vlietland Hospital), Schiedam; Department of Neurology (S. Arends, P.W.W.), Haga Hospital, Den Haag; Department of Neurology (L.W.G.L., L.H.V.), St. Elisabeth-TweeSteden Hospital, Tilburg, the Netherlands; Department of Neurology (L.B.), IRCCS Ospedale Policlinico San Martino, Genova, Italy; Department of Neurology (S. Kuwabara), Chiba University, Chuo-ku, Japan; Department of Neurology (P.V.d.B.), Neuromuscular Reference Centre, University Hospital Saint-Luc, University of Louvain, Brussels, Belgium; Department of Neurology (S.M.), Hospital de Pediatría J.P. Garrahan, Buenos Aires, Argentina; Dysimmune Neuropathies Unit (G.A.M.), Department of Systems Medicine, Tor Vergata University Hospital, Rome, Italy; Department of Medicine (N.S.), University of Malaya, Kuala Lumpur, Malaysia; Department of Neurology (G.G.), University Hospital of Modena, Italy; Department of Clinical Neurophysiology (Y.P.), Reference Centre for NMD, CHU Nantes, Nantes, France; Department of Neurology (J.B.), Saarland University Medical School, Homburg (previous hospital), and MVZ Pfalzklinikum (J.B.), Kusel, Germany (current hospital); Department of Neurology (K.K., R.P.K.), Albert Schweitzer Hospital, Dordrecht, the Netherlands; Department of Neurology (C.M.), Hospital Británico, Buenos Aires, Argentina; Department of Neurology (M.J.S.T.), Hospital Marques de Valdecilla, Santander; Department of Neurology (L.Q., L.M.-A.), Hospital de la Santa Creu i Sant Pau, Universitat Autònoma de Barcelona, CIBERER and ERN-NMD, Spain; Department of Neurology (Y.W.), Affiliated Hospital of Jining Medical University, Shandong Province, China; Neuromuscular and Neuroimmunology Service (E.N.-O.), IRCCS Humanitas Research Hospital, Milan University, Italy; Nuffield Department of Clinical Neurosciences (S.R.), University of Oxford and Oxford University Hospitals NHS Foundation Trust, United Kingdom; Department of Neurosciences, Ophthalmology, Rehabilitation, Genetics and Maternal Sciences (A.S.), University of Genova, and IRCCS San Martino Hospital (A.S.), Genova, Italy; Department of Neurology (J.P.), Hospital Clínico de Santiago, Travesia Choupana, Santiago de Compostela (A Coruña), Spain; Department of Neurology (F.H.V.), Franciscus Gasthuis & Vlietland (location: Franciscus Gasthuis), Rotterdam, the Netherlands; Department of Neurology (W.W., N.K.), University of Vermont Medical Centre, Burlington; Department of Neurology (H.C.L.), University Hospital of Cologne, Germany; Department of Neurology (V.G., B.S.), Montefiore Medical Center, Bronx, NY; Department of Neurology (G.C.), University Milano-Bicocca, Monza, Italy; Department of Neurology (G.G.-G.), Hospital Universitario Infanta Sofía, San Sebastián de los Reyes, Spain; Department of Neurology (F.A.B.), Instituto de Investigaciones Neurológicas Raúl Carrea, FLENI, Buenos Aires, Argentina; Department of Neurology (H.D.K.), University Health Network, University of Toronto, Ontario, Canada; Department of Neurology (E.D.), University Hospital of Larissa, Greece; Department of Neurology (S. Attarian), Reference Centre for NMD, CHU Timone ERN NMD, Marseille, France; Department of Neurology (A.J.v.d.K., F.E.), Amsterdam University Medical Centre, University of Amsterdam, Neuroscience Institute; Department of Neurology (J.P.A.S.), Maasstad Hospital, Rotterdam; Department of Neurology (H.J.G.), Reinier de Graaf Hospital, Reinier de Graafweg, Delft, the Netherlands; Department of Neurology (R.D.M.H.), King's College Hospital, Denmark Hill, London; Department of Neurology (J.K.L.H.), The Walton Centre, Liverpool, United Kingdom; Department of Neurology (K.A.S.), University of Texas Health Science Centre at Houston; Department of Biology (N.K., S. Karafiath), Utah Valley University, Orem; Department of Neurology (M.V.), Lahey Hospital and Medical Center, Tufts University School of Medicine, Burlington, MA; Department of Neurology, Mental Health and Sensory Organs (NESMOS) (G.A.), Faculty of Medicine and Psychology, University of Rome "Sapienza," Sant' Andrea Hospital, Italy; Department of Clinical Neurosciences (T.E.F.), University of Calgary, Alberta, Canada; Department of Neurology (C.F.), Maastricht University Medical Centre, the Netherlands; Department of Neurology (M.B.), Leeds Teaching Hospitals; Department of Neurology (R.C.R.), Addenbrooke's Hospital, Cambridge, United Kingdom; Department of Neurology (N.J.S.), University at Buffalo Jacobs School of Medicine and Biomedical Sciences, NY; Department of Neurology (R.F.), Scientific Institute San Raffaele, Milano, Italy; Department of Neurology (G.W.v.D.), Canisius Wilhelmina Hospital, Nijmegen; Department of Neurology (M.P.J.G.), Jeroen Bosch Hospital, 's-Hertogenbosch; Department of Neurology (J.V.), Leiden University Medical Centre; and Department of Immunology (B.C.J.), Erasmus MC, University Medical Centre Rotterdam, the Netherlands.
² From the Department of Neurology (H.A.-H., H.A., T.H.), Aarhus University Hospital, Denmark; Department of Neurology (A.Y.D., B.v.d.B., C.V., J.R., S.E.L., S. Arends, L.W.G.L., K.K., B.C.J.), Erasmus MC, University Medical Centre Rotterdam, the Netherlands; Department of Neurology (A.M.S.), University of Michigan School of Medicine, Ann Arbor; Department of Neurology (S.A.Z.), University of Pittsburgh Medical Center, PA; Department of Neurology (H.J.W., A.D.), College of Medical, Veterinary and Life Sciences, University of Glasgow, United Kingdom; Department of Neurology (D.R.C.), Johns Hopkins University School of Medicine, Baltimore, MD; Department of Neurology (K.C.G.), St. Elizabeth's Medical Centre, Tufts University, School of Medicine, Boston, MA; Laboratory of Gut-Brain Signaling (Z.I.); Laboratory Sciences and Services Division (LSSD) (Z.I.), icddr,b; National Institute of Neurosciences and Hospital (Q.D.M.), Dhaka, Bangladesh; Department of Neurology (S.H.S.), Odense University Hospital and University of Southern Denmark; Department of Neurology (S. Kusunoki), Kindai University Faculty of Medicine, Osaka-Sayama City, Japan; Department of Neurology (C.C.), Neuromuscular Unit, Bellvitge University Hospital-IDIBELL, CIBERER, Barcelona, Spain; Division of Neurology (K.B.), Department of Medicine, Groote Schuur Hospital, University of Cape Town, South Africa; Department of Neurology (J.A.L.M.), Royal Victoria Infirmary, Newcastle upon Tyne Hospitals NHS Foundation Trust, United Kingdom; Department of Neurology (B.v.d.B., H.K.), Franciscus Gasthuis & Vlietland (location: Vlietland Hospital), Schiedam; Department of Neurology (S. Arends, P.W.W.), Haga Hospital, Den Haag; Department of Neurology (L.W.G.L., L.H.V.), St. Elisabeth-TweeSteden Hospital, Tilburg, the Netherlands; Department of Neurology (L.B.), IRCCS Ospedale Policlinico San Martino, Genova, Italy; Department of Neurology (S. Kuwabara), Chiba University, Chuo-ku, Japan; Department of Neurology (P.V.d.B.), Neuromuscular Reference Centre, University Hospital Saint-Luc, University of Louvain, Brussels, Belgium; Department of Neurology (S.M.), Hospital de Pediatría J.P. Garrahan, Buenos Aires, Argentina; Dysimmune Neuropathies Unit (G.A.M.), Department of Systems Medicine, Tor Vergata University Hospital, Rome, Italy; Department of Medicine (N.S.), University of Malaya, Kuala Lumpur, Malaysia; Department of Neurology (G.G.), University Hospital of Modena, Italy; Department of Clinical Neurophysiology (Y.P.), Reference Centre for NMD, CHU Nantes, Nantes, France; Department of Neurology (J.B.), Saarland University Medical School, Homburg (previous hospital), and MVZ Pfalzklinikum (J.B.), Kusel, Germany (current hospital); Department of Neurology (K.K., R.P.K.), Albert Schweitzer Hospital, Dordrecht, the Netherlands; Department of Neurology (C.M.), Hospital Británico, Buenos Aires, Argentina; Department of Neurology (M.J.S.T.), Hospital Marques de Valdecilla, Santander; Department of Neurology (L.Q., L.M.-A.), Hospital de la Santa Creu i Sant Pau, Universitat Autònoma de Barcelona, CIBERER and ERN-NMD, Spain; Department of Neurology (Y.W.), Affiliated Hospital of Jining Medical University, Shandong Province, China; Neuromuscular and Neuroimmunology Service (E.N.-O.), IRCCS Humanitas Research Hospital, Milan University, Italy; Nuffield Department of Clinical Neurosciences (S.R.), University of Oxford and Oxford University Hospitals NHS Foundation Trust, United Kingdom; Department of Neurosciences, Ophthalmology, Rehabilitation, Genetics and Maternal Sciences (A.S.), University of Genova, and IRCCS San Martino Hospital (A.S.), Genova, Italy; Department of Neurology (J.P.), Hospital Clínico de Santiago, Travesia Choupana, Santiago de Compostela (A Coruña), Spain; Department of Neurology (F.H.V.), Franciscus Gasthuis & Vlietland (location: Franciscus Gasthuis), Rotterdam, the Netherlands; Department of Neurology (W.W., N.K.), University of Vermont Medical Centre, Burlington; Department of Neurology (H.C.L.), University Hospital of Cologne, Germany; Department of Neurology (V.G., B.S.), Montefiore Medical Center, Bronx, NY; Department of Neurology (G.C.), University Milano-Bicocca, Monza, Italy; Department of Neurology (G.G.-G.), Hospital Universitario Infanta Sofía, San Sebastián de los Reyes, Spain; Department of Neurology (F.A.B.), Instituto de Investigaciones Neurológicas Raúl Carrea, FLENI, Buenos Aires, Argentina; Department of Neurology (H.D.K.), University Health Network, University of Toronto, Ontario, Canada; Department of Neurology (E.D.), University Hospital of Larissa, Greece; Department of Neurology (S. Attarian), Reference Centre for NMD, CHU Timone ERN NMD, Marseille, France; Department of Neurology (A.J.v.d.K., F.E.), Amsterdam University Medical Centre, University of Amsterdam, Neuroscience Institute; Department of Neurology (J.P.A.S.), Maasstad Hospital, Rotterdam; Department of Neurology (H.J.G.), Reinier de Graaf Hospital, Reinier de Graafweg, Delft, the Netherlands; Department of Neurology (R.D.M.H.), King's College Hospital, Denmark Hill, London; Department of Neurology (J.K.L.H.), The Walton Centre, Liverpool, United Kingdom; Department of Neurology (K.A.S.), University of Texas Health Science Centre at Houston; Department of Biology (N.K., S. Karafiath), Utah Valley University, Orem; Department of Neurology (M.V.), Lahey Hospital and Medical Center, Tufts University School of Medicine, Burlington, MA; Department of Neurology, Mental Health and Sensory Organs (NESMOS) (G.A.), Faculty of Medicine and Psychology, University of Rome "Sapienza," Sant' Andrea Hospital, Italy; Department of Clinical Neurosciences (T.E.F.), University of Calgary, Alberta, Canada; Department of Neurology (C.F.), Maastricht University Medical Centre, the Netherlands; Department of Neurology (M.B.), Leeds Teaching Hospitals; Department of Neurology (R.C.R.), Addenbrooke's Hospital, Cambridge, United Kingdom; Department of Neurology (N.J.S.), University at Buffalo Jacobs School of Medicine and Biomedical Sciences, NY; Department of Neurology (R.F.), Scientific Institute San Raffaele, Milano, Italy; Department of Neurology (G.W.v.D.), Canisius Wilhelmina Hospital, Nijmegen; Department of Neurology (M.P.J.G.), Jeroen Bosch Hospital, 's-Hertogenbosch; Department of Neurology (J.V.), Leiden University Medical Centre; and Department of Immunology (B.C.J.), Erasmus MC, University Medical Centre Rotterdam, the Netherlands. b.jacobs@erasmusmc.nl.

PMID: 37076309
PMCID: PMC10256127
DOI: 10.1212/WNL.0000000000207282

Erratum in

CSF Findings in Relation to Clinical Characteristics, Subtype, and Disease Course in Patients With Guillain-Barré Syndrome.
[No authors listed] [No authors listed] Neurology. 2023 Sep 26;101(13):592. doi: 10.1212/WNL.0000000000207874. Epub 2023 Aug 29. Neurology. 2023. PMID: 37643890 No abstract available.

Abstract

Background and objectives: To investigate CSF findings in relation to clinical and electrodiagnostic subtypes, severity, and outcome of Guillain-Barré syndrome (GBS) based on 1,500 patients in the International GBS Outcome Study.

Methods: Albuminocytologic dissociation (ACD) was defined as an increased protein level (>0.45 g/L) in the absence of elevated white cell count (<50 cells/μL). We excluded 124 (8%) patients because of other diagnoses, protocol violation, or insufficient data. The CSF was examined in 1,231 patients (89%).

Results: In 846 (70%) patients, CSF examination showed ACD, which increased with time from weakness onset: ≤4 days 57%, >4 days 84%. High CSF protein levels were associated with a demyelinating subtype, proximal or global muscle weakness, and a reduced likelihood of being able to run at week 2 (odds ratio [OR] 0.42, 95% CI 0.25-0.70; p = 0.001) and week 4 (OR 0.44, 95% CI 0.27-0.72; p = 0.001). Patients with the Miller Fisher syndrome, distal predominant weakness, and normal or equivocal nerve conduction studies were more likely to have lower CSF protein levels. CSF cell count was <5 cells/μL in 1,005 patients (83%), 5-49 cells/μL in 200 patients (16%), and ≥50 cells/μL in 13 patients (1%).

Discussion: ACD is a common finding in GBS, but normal protein levels do not exclude this diagnosis. High CSF protein level is associated with an early severe disease course and a demyelinating subtype. Elevated CSF cell count, rarely ≥50 cells/μL, is compatible with GBS after a thorough exclusion of alternative diagnoses.

Classification of evidence: This study provides Class IV evidence that CSF ACD (defined by the Brighton Collaboration) is common in patients with GBS.

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Conflict of interest statement

H. Al-Hakem and A.Y. Doets report no disclosures relevant to the manuscript. A. Stino served on the Scientific Advisory Board for CSL Behring and received research support through Bristol Myers Squibb. S.A. Zivkovic, H. Andersen, and H. Willison report no disclosures relevant to the manuscript. D.R. Cornblath has received consultancy honoraria from Annexon Biosciences, Argenx, Biotest Pharmaceuticals, Cigna Health Management, CSL Behring, DP Clinical, Grifols, Hansa Biopharma, New Enterprise Associates, Octapharma, Pharnext SAS, Polyneuron Pharmaceuticals, Seattle Genetics, Stealth BioTherapeutics, and Syntimmune. David R. Cornblath is also on a data safety monitoring board for Pfizer, Sanofi, Alnylam Pharmaceuticals, PledPharma, and Momenta Pharma. Johns Hopkins University has licensed technology to AstraZeneca Pharmaceuticals, Genentech, Levicept, Seattle Genetics, Merrimack Pharmaceuticals, Levicept, and Disarm Therapeutics, for which David R. Cornblath receives royalties. K.C. Gorson is a consultant for UCB, Pfizer, Annexon, Momenta, and Genentech. Q.D. Mohammad and S.H. Sindrup report no disclosures relevant to the manuscript. S. Kusunoki reports grants from Teijin, grants from Japan Blood Product Organization, grants from Nihon Pharmaceutical, personal fees from Teijin, personal fees from Japan Blood Product Organization, personal fees from Nihon Pharmaceutical, and personal fees from CSL Behring, outside the submitted work. A. Davidson, C. Casasnovas, K. Bateman, J.A.L. Miller, B. van den Berg, C. Verboon, J. Roodbol, S.E. Leonhard, S. Arends, L. Luijten, L. Benedetti. S. Kuwabara, P. Van den Bergh, S. Monges, G.A. Marfia, N. Shahrizaila, G. Galassi, Y. Pereon, J. Bürmann, K. Kuitwaard, R.P. Kleyweg, C. Marchesoni, and M.J. Sedano Tous report no disclosures relevant to the manuscript. L. Querol received research grants from Instituto de Salud Carlos III—Ministry of Economy and Innovation (Spain), GBS-CIDP Foundation International, Novartis Pharma Spain, Roche, UCB and Grifols. L. Querol provided expert testimony to Grifols, CSL Behring, Novartis, Sanofi-Genzyme, Merck, Annexon, Johnson and Johnson, Alexion, UCB, and Roche. Luis Querol serves at Clinical Trial Steering Committee for Sanofi Genzyme and is the principal investigator for UCB’s CIDP01 trial. L. Martín-Aguilar And Y. Wang report no disclosures relevant to the manuscript. E. Nobile-Orazio Eduardo Nobile-Orazio received honorarium for participating in Steering or Advisory Board form Argenx, Belgium; Astellas, the Netherlands; Baxter/Takeda, Italy & USA; CSL Behring, Italy & Switzerland; Janssen, USA; Kedrion, Italy; LFB, France; Novartis, Switzerland; Roche, Switzerland; Sanofi, USA; UCB, UK. He received honorarium for giving lectures from Baxter, USA, & Italy; CSL Behring, Italy; Grifols, Spain; and Kedrion, Italy and travel grants to attend Scientific Meetings from Baxter, Grifols, and Kedrion, Italy. None of these contributions had any relevance for this study. S. Rinaldi, A. Schenone, J. Pardo, F.H. Vermeij, and W. Waheed report no disclosures relevant to the manuscript. H.C. Lehmann reports personal fees from Biogen, CSL Behring, Grifols, Takeda, and Celgene and grants and personal fees from Alnylam and Novartis. V. Granit, B. Stein, G. Cavaletti, G. Gutiérrez-Gutiérrez, F.A. Barroso, L.H. Visser, H.D. Katzberg, E. Dardiotis, S. Attarian, A.J. van der Kooi, P.W. Wirtz, J.P.A. Samijn, and H.J. Gilhuis report no disclosures relevant to the manuscript. R.D.M. Hadden received payments from CSL Behring, Grifols, Argenx, and Alnylam. J.K.L. Holt, K.A. Sheikh, N. Kolb, S. Karafiath, M. Vytopil, G. Antonini, and T.E. Feasby report no disclosures relevant to the manuscript. C.G. Faber reports grants from European Union's Horizon 2020 research and innovation program Marie Sklodowska-Curie grant for PAIN-Net, Molecule-to-man pain network (grant no. 721841), grants from Grifols and Lamepro for a trial on IVIg in small fiber neuropathy, grants from Prinses Beatrix Spierfonds, and Steering committees/advisory board for studies in small fiber neuropathy of Biogen/Convergence, Vertex, Lilly, and OliPass, outside the submitted work. H. Kramers, M. Busby, R.C. Roberts, N.J. Silvestri, R. Fazio, G.W. van Dijk, M.P.J. Garssen, J. Verschuuren, T. Harbo, and B.C. Jacobs report no disclosures relevant to the manuscript. Go to Neurology.org/N for full disclosures.

Figures

**Figure 1. Time to LP and CSF-TP**
Number/total (%) of patients (y-axis) with increased CSF protein concentration (>0.45 g/L) in relation to timing of lumbar puncture after onset of weakness (x-axis). CSF-TP = CSF total protein; LP = lumbar puncture.

**Figure 2. Distribution of Weakness and CSF-TP**
Median (box) with 95% CIs (whiskers) CSF-TP in the distribution of muscle weakness in 1,226 patients with Guillain-Barré syndrome stratified for the timing of LP as defined by the median time to LP in the cohort (early ≤4 days, late >4 days). Distribution was defined by bilateral MRC sum scores in shoulder abductors, wrist extensors, hip flexors, and ankle dorsiflexors. Comparison of CSF-TP across the groups with a different distribution of muscle weakness with the Kruskal-Wallis test yields the p value <0.01. Early LP global, n = 382; proximal, n = 98; distal, n = 59; no weakness, n = 76. Late LP global, n = 412; proximal, n = 73; distal, n = 51; no weakness, n = 58. CSF-TP = CSF total protein; LP = lumbar puncture; MRC = Medical Research Council.

**Figure 3. CSF-TP and Cell Count**
Grouped scatterplot of CSF-TP (y-axis) in relation to categories of CSF cell count (x-axis) in 1,194 patients with Guillain-Barré syndrome. Line and number indicate the median CSF-TP. Grid line at y = 0.45 g/L. Tukey methods have been applied to remove outliers. Comparison of distribution of CSF-TP across the groups with the Kruskal-Wallis test yields the p value <0.001. CSF-TP = CSF total protein.

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Comment in

CSF in Guillain-Barré Syndrome: It's a Matter of Timing.
Sejvar J. Sejvar J. Neurology. 2023 Jun 6;100(23):1081-1082. doi: 10.1212/WNL.0000000000207203. Epub 2023 Apr 19. Neurology. 2023. PMID: 37076306 No abstract available.

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References

1. Guillain G, Barre JA, Strohl A. Radiculoneuritis syndrome with hyperalbuminosis of cerebrospinal fluid without cellular reaction. Notes on clinical features and graphs of tendon reflexes. 1916 [in French]. Ann Med Interne (Paris). 1916;150(1):24-32. - PubMed
1. Asbury AK, Cornblath DR. Assessment of current diagnostic criteria for Guillain-Barré syndrome. Ann Neurol. 1990;27(suppl):S21-S24. - PubMed
1. Sejvar JJ, Kohl KS, Gidudu J, et al. . Guillain-Barré syndrome and Fisher syndrome: case definitions and guidelines for collection, analysis, and presentation of immunization safety data. Vaccine. 2011;29(3):599-612. - PubMed
1. Hadden RD, Karch H, Hartung HP, et al. . Preceding infections, immune factors, and outcome in Guillain-Barré syndrome. Neurology. 2001;56(6):758-765. - PubMed
1. Haymaker WE, Kernohan JW. The Landry-Guillain-Barré syndrome; a clinicopathologic report of 50 fatal cases and a critique of the literature. Medicine (Baltimore). 1949;28(1):59-141. - PubMed

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[1] Guillain G, Barre JA, Strohl A. Radiculoneuritis syndrome with hyperalbuminosis of cerebrospinal fluid without cellular reaction. Notes on clinical features and graphs of tendon reflexes. 1916 [in French]. Ann Med Interne (Paris). 1916;150(1):24-32. - PubMed

[2] Guillain G, Barre JA, Strohl A. Radiculoneuritis syndrome with hyperalbuminosis of cerebrospinal fluid without cellular reaction. Notes on clinical features and graphs of tendon reflexes. 1916 [in French]. Ann Med Interne (Paris). 1916;150(1):24-32. - PubMed

[3] Asbury AK, Cornblath DR. Assessment of current diagnostic criteria for Guillain-Barré syndrome. Ann Neurol. 1990;27(suppl):S21-S24. - PubMed

[4] Asbury AK, Cornblath DR. Assessment of current diagnostic criteria for Guillain-Barré syndrome. Ann Neurol. 1990;27(suppl):S21-S24. - PubMed

[5] Sejvar JJ, Kohl KS, Gidudu J, et al. . Guillain-Barré syndrome and Fisher syndrome: case definitions and guidelines for collection, analysis, and presentation of immunization safety data. Vaccine. 2011;29(3):599-612. - PubMed

[6] Sejvar JJ, Kohl KS, Gidudu J, et al. . Guillain-Barré syndrome and Fisher syndrome: case definitions and guidelines for collection, analysis, and presentation of immunization safety data. Vaccine. 2011;29(3):599-612. - PubMed

[7] Hadden RD, Karch H, Hartung HP, et al. . Preceding infections, immune factors, and outcome in Guillain-Barré syndrome. Neurology. 2001;56(6):758-765. - PubMed

[8] Hadden RD, Karch H, Hartung HP, et al. . Preceding infections, immune factors, and outcome in Guillain-Barré syndrome. Neurology. 2001;56(6):758-765. - PubMed

[9] Haymaker WE, Kernohan JW. The Landry-Guillain-Barré syndrome; a clinicopathologic report of 50 fatal cases and a critique of the literature. Medicine (Baltimore). 1949;28(1):59-141. - PubMed

[10] Haymaker WE, Kernohan JW. The Landry-Guillain-Barré syndrome; a clinicopathologic report of 50 fatal cases and a critique of the literature. Medicine (Baltimore). 1949;28(1):59-141. - PubMed

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CSF Findings in Relation to Clinical Characteristics, Subtype, and Disease Course in Patients With Guillain-Barré Syndrome

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CSF Findings in Relation to Clinical Characteristics, Subtype, and Disease Course in Patients With Guillain-Barré Syndrome

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