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

Al-Hakem H 1 , Doets AY 1 , Stino AM 1 , Zivkovic SA 1 , Andersen H 1 , Willison HJ 1 Show all authors , Cornblath DR 1 , Gorson KC 1 , Islam Z 1 , Mohammad QD 1 , Sindrup SH 1 , Kusunoki S 1 , Davidson A 1 , Casasnovas C 1 , Bateman K 1 , Miller JAL 1 , van den Berg B 1 , Verboon C 1 , Roodbol J 1 , Leonhard SE 1 , Arends S 1 , Luijten LWG 1 , Benedetti L 1 , Kuwabara S 1 , Van den Bergh P 1 , Monges S 1 , Marfia GA 1 , Shahrizaila N 1 , Galassi G 1 , Pereon Y 1 , Bürmann J 1 , Kuitwaard K 1 , Kleyweg RP 1 , Marchesoni C 1 , Sedano Tous MJ 1 , Querol L 1 , Martín-Aguilar L 1 , Wang Y 1 , Nobile-Orazio E 1 , Rinaldi S 1 , Schenone A 1 , Pardo J 1 , Vermeij FH 1 , Waheed W 1 , Lehmann HC 1 , Granit V 1 , Stein B 1 , Cavaletti G 1 , Gutiérrez-Gutiérrez G 1 , Barroso FA 1 , Visser LH 1 , Katzberg HD 1 , Dardiotis E 1 , Attarian S 1 , van der Kooi AJ 1 , Eftimov F 1 , Wirtz PW 1 , Samijn JPA 1 , Gilhuis HJ 1 , Hadden RDM 1 , Holt JKL 1 , Sheikh KA 1 , Kolb N 1 , Karafiath S 1 , Vytopil M 1 , Antonini G 1 , Feasby TE 1 , Faber C 1 , Kramers H 1 , Busby M 1 , Roberts RC 1 , Silvestri NJ 1 , Fazio R 1 , van Dijk GW 1 , Garssen MPJ 1 , Verschuuren J 1 , Harbo T 1 , Jacobs BC 2 , IGOS Consortium

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
Neurology, 2023 Jun 06;100(23):e2386-e2397.
PMID: 37076309 DOI: 10.1212/WNL.0000000000207282

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.

* Title and MeSH Headings from MEDLINE®/PubMed®, a database of the U.S. National Library of Medicine.

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