Abstract
Background & purpose
In this retrospective study, we aimed at defining the clinical, paraclinical and outcome features of acute neurological syndromes associated with anti-GQ1b antibodies.
Results
We identified 166 patients with neurological symptoms appearing in less than 1 month and anti-GQ1b antibodies in serum between 2012 and 2022. Half were female (51%), mean age was 50 years (4–90), and the most frequent clinical features were areflexia (80% of patients), distal upper and lower limbs sensory symptoms (78%), ophthalmoplegia (68%), sensory ataxia (67%), limb muscle weakness (45%) and bulbar weakness (45%). Fifty-three patients (32%) presented with complete (21%) and incomplete (11%) Miller Fisher syndrome (MFS), thirty-six (22%) with Guillain–Barre syndrome (GBS), one (0.6%) with Bickerstaff encephalitis (BE), and seventy-three (44%) with mixed MFS, GBS & BE clinical features. Nerve conduction studies were normal in 46% of cases, showed demyelination in 28%, and axonal loss in 23%. Anti-GT1a antibodies were found in 56% of cases, increased cerebrospinal fluid protein content in 24%, and Campylobacter jejuni infection in 7%. Most patients (83%) were treated with intravenous immunoglobulins, and neurological recovery was complete in 69% of cases at 1 year follow-up. One patient died, and 15% of patients relapsed. Age > 70 years, initial Intensive Care Unit (ICU) admission, and absent anti-GQ1b IgG antibodies were predictors of incomplete recovery at 12 months. No predictors of relapse were identified.
Conclusion
This study from Western Europe shows acute anti-GQ1b antibody syndrome presents with a large clinical phenotype, a good outcome in 2/3 of cases, and frequent relapses.
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Data availability
All data and related documentation from this study are available on request to qualified researchers with no time limit, and subject to a standard data-sharing agreement.
References
Cutillo G, Saariaho AH, Meri S (2020) Physiology of gangliosides and the role of antiganglioside antibodies in human diseases. Cell Mol Immunol 17(4):313–322
Uchibori A (2021) Anti-GQ1b antibody: recent topics. Clin Exp Neuroimmunol 12(3):158–164
Fisher M (1956) An unusual variant of acute idiopathic polyneuritis (syndrome of ophthalmoplegia, ataxia and areflexia). N Engl J Med 255(2):57–65
Bickerstaff ER, Cloake PCP (1951) Mesencephalitis and rhombencephalitis. Br Med J 2(4723):77–81
The GBS Classification Group, Wakerley BR, Uncini A, Yuki N (2014) Guillain-Barré and Miller Fisher syndromes—new diagnostic classification. Nat Rev Neurol 10(9):537–544
Odaka M, Yuki N, Hirata K (2001) Anti-GQ1b IgG antibody syndrome: clinical and immunological range. J Neurol Neurosurg Psychiatry 70(1):50–55
Shahrizaila N, Yuki N (2013) Bickerstaff brainstem encephalitis and Fisher syndrome: anti-GQ1b antibody syndrome. J Neurol Neurosurg Psychiatry 84(5):576–583
Doets AY, Verboon C, van den Berg B, Harbo T, Cornblath DR, Willison HJ et al (2018) Regional variation of Guillain-Barré syndrome. Brain J Neurol 141(10):2866–2877
Ito M, Kuwabara S, Odaka M, Misawa S, Koga M, Hirata K et al (2008) Bickerstaff’s brainstem encephalitis and Fisher syndrome form a continuous spectrum: clinical analysis of 581 cases. J Neurol 255(5):674–682
Uchibori A, Gyohda A, Chiba A (2016) Ca2+-dependent anti-GQ1b antibody in GQ1b-seronegative Fisher syndrome and related disorders. J Neuroimmunol 298:172–177
Sejvar JJ, Kohl KS, Gidudu J, Amato A, Bakshi N, Baxter R et al (2011) Guillain-Barré syndrome and Fisher syndrome: case definitions and guidelines for collection, analysis, and presentation of immunization safety data. Vaccine 29(3):599–612
Shahrizaila N, Lehmann HC, Kuwabara S (2021) Guillain-Barré syndrome. Lancet 397(10280):1214–1228
Chabraoui F, Derrington EA, Mallie-Didier F, Confavreux C, Quincy C, Caudie C (1993) Dot-blot immunodetection of antibodies against GM1 and other gangliosides on PVDF-P membranes. J Immunol Methods 165(2):225–230
Willison HJ, Yuki N (2002) Peripheral neuropathies and anti-glycolipid antibodies. Brain J Neurol 125(Pt 12):2591–2625
Peillet C, Adams D, Attarian S, Bouhour F, Cauquil C, Cassereau J et al (2022) Anti-disialosyl-immunoglobulin m chronic autoimmune neuropathies: a nationwide multicenter retrospective study. Eur J Neurol 29(12):3547–3555
Ishii J, Yuki N, Kawamoto M, Yoshimura H, Kusunoki S, Kohara N (2016) Recurrent Guillain-Barré syndrome, Miller Fisher syndrome and Bickerstaff brainstem encephalitis. J Neurol Sci 364:59–64
Chida K, Nomura H, Konno H, Takase S, Itoyama Y (1999) Recurrent Miller Fisher syndrome: clinical and laboratory features and HLA antigens. J Neurol Sci 165(2):139–143
Chiba A, Kusunoki S, Obata H, Machinami R, Kanazawa I (1993) Serum anti-GQ1b IgG antibody is associated with ophthalmoplegia in Miller Fisher syndrome and Guillain-Barré syndrome: clinical and immunohistochemical studies. Neurology 43(10):1911–1917
Kim JK, Bae JS, Kim DS, Kusunoki S, Kim JE, Kim JS et al (2014) Prevalence of anti-ganglioside antibodies and their clinical correlates with Guillain-Barré syndrome in Korea: a nationwide multicenter study. J Clin Neurol Seoul Korea 10(2):94–100
Shahrizaila N, Goh KJ, Kokubun N, Tan AH, Tan CY, Yuki N (2014) Sensory nerves are frequently involved in the spectrum of fisher syndrome: sensory nerve involvement in FS. Muscle Nerve 49(4):558–563
Alberti MA, Povedano M, Montero J, Casasnovas C (2020) Early electrophysiological findings in Fisher-Bickerstaff syndrome. Neurol Engl Ed 35(1):40–45
Overell JR, Hseih ST, Odaka M, Yuki N, Willison HJ (2007) Treatment for Fisher syndrome, Bickerstaff’s brainstem encephalitis and related disorders. Cochrane Neuromuscular Group, editor. Cochrane Database Syst Rev. https://doi.org/10.1002/14651858.CD004761.pub2
Bai HX, Wang ZL, Tan LM, Xiao B, Goldstein JM, Yang L (2013) The effectiveness of immunomodulating treatment on Miller Fisher syndrome: a retrospective analysis of 65 Chinese patients. J Peripher Nerv Syst JPNS 18(2):195–196
Van Doorn PA, Van den Bergh PYK, Hadden RDM, Avau B, Vankrunkelsven P, Attarian S et al (2023) European Academy of Neurology/Peripheral Nerve Society Guideline on diagnosis and treatment of guillain-barré syndrome. Eur J Neurol 30(12):3646–3674
Tavee J, Brannagan TH, Lenihan MW, Muppidi S, Kellermeyer L, Donofrio PD et al (2023) Updated consensus statement: Intravenous immunoglobulin in the treatment of neuromuscular disorders report of the AANEM ad hoc committee. Muscle Nerve. https://doi.org/10.1002/mus.27922
Uncini A, Susuki K, Yuki N (2013) Nodo-paranodopathy: beyond the demyelinating and axonal classification in anti-ganglioside antibody-mediated neuropathies. Clin Neurophysiol 124(10):1928–1934
Saito K, Shimizu F, Koga M, Sano Y, Tasaki A, Abe M et al (2013) Blood-brain barrier destruction determines Fisher/Bickerstaff clinical phenotypes: an in vitro study. J Neurol Neurosurg Psychiatry 84(7):756–765
Lardone RD, Alaniz ME, Irazoqui FJ, Nores GA (2006) Unusual presence of anti-GM1 IgG-antibodies in a healthy individual, and their possible involvement in the origin of disease-associated anti-GM1 antibodies. J Neuroimmunol 173(1–2):174–179
Conrad K, Schneider H, Ziemssen T, Talaska T, Reinhold D, Humbel RL et al (2007) A new line immunoassay for the multiparametric detection of antiganglioside autoantibodies in patients with autoimmune peripheral neuropathies. Ann NY Acad Sci 1109:256–264
Johannis W, Renno JH, Klatt AR, Wielckens K (2014) Anti-glycolipid antibodies in patients with neuropathy: a diagnostic assessment. J Clin Neurosci Off J Neurosurg Soc Australas 21(3):488–492
Acknowledgements
The authors thank Dr Anne-Sophie DELEPLANCQUE, MD, for her help in identifying patients from Lille University Hospital.
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MC, DA, SA, FB, JPC, GC, CC, JBC, PC, AC, ED, GF, SF, TG, TK, CL, TM, MMi, MMo, GN, JBN, YP, AP, GS, FT, CT, MT, ST, LV & AEL participated in data collection. AEL&MC designed research, performed research, and participated in data collection. MC & AEL wrote the manuscript. DA, SA, FB, JPC, GC, CC, JBC, PC, AC, ED, GF, SF, TG, TK, CL, TM, MMi, MMo, GN, JBN, YP, AP, GS, FT, CT, MT, ST & LV revised the manuscript for intellectual content. All authors have read and agreed to the published version of the manuscript.
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MC, DA, SA, FB, JPC, GC, CC, JBC, PC, AC, ED, GF, SF, TG, TK, CL, TM, MMi, MMo, GN, JBN, YP, AP, GS, FT, CT, MT, ST, LV & AEL disclose all competing interests. Dr M. Coly, Pr D. Adams, Pr S. Attarian, Dr F. Bouhour, Pr JP. Camdessanche, Dr G. Carey, Dr C. Cauquil, Dr P. Chretien, Dr E. Delmont, Dr G. Fargeot, Dr S. Frachet, Dr T. Gendre, Dr T. Kuntzer, Dr C. Labeyrie, Dr T. Maisonobe, Dr M. Michaud, Dr M. Moulin, Pr G. Nicolas, Dr JB. Noury, Pr Y. Pereon, Dr A. Puma, Dr G. Sole, Dr F. Taithe, Dr C. Tard, Dr M. Theaudin, Pr S. Timsit, Dr L. Venditti: declares no disclosures, Dr JB. Chanson declares consultancy fees from Alnylam. Pr A. Creange received grants from Octapharma. Pr A. Echaniz-Laguna received consulting fees from LFB, Alnylam, and Pfizer.
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Coly, M., Adams, D., Attarian, S. et al. Clinical, paraclinical and outcome features of 166 patients with acute anti-GQ1b antibody syndrome. J Neurol (2024). https://doi.org/10.1007/s00415-024-12410-4
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DOI: https://doi.org/10.1007/s00415-024-12410-4