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An electrophysiological classification associated with Guillain–Barré syndrome outcomes

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Abstract

Guillain–Barré syndrome (GBS) is an acute, post-infectious, inflammatory, autoimmune peripheral neuropathy with a highly diverse clinical course and outcome. We classified GBS on the basis of patients’ first nerve conduction and validated this system to be associated with outcome on the basis of electrophysiological characteristics during the acute phase of GBS. We retrospectively evaluated 40 GBS patients who underwent their first electrophysiological study within 14 days of onset and classified GBS into four patterns: (1) acute inflammatory demyelinating polyneuropathy (AIDP) pattern with sensory nerve conduction abnormalities (motor–sensory AIDP: MS-AIDP), (2) AIDP pattern without sensory nerve conduction abnormalities (motor AIDP: M-AIDP), (3) acute motor axonal neuropathy (AMAN) pattern, and (4) minor abnormalities pattern. We compared the clinical, electrophysiological, and laboratory findings between groups and determined subgroups associated with poor outcome. The MS-AIDP and AMAN patterns more frequently exhibited prolonged recovery compared with the M-AIDP and minor abnormalities patterns and were associated with prolonged recovery (specificity, 100 %; sensitivity, 73 %; P < 0.001). The period of inability to walk independently was significantly longer in the MS-AIDP and AMAN patterns than in the M-AIDP and minor abnormalities patterns (median 85 vs. 10 days; P < 0.001). In conclusion, our classification of GBS using a single nerve conduction study in the early phase of disease is associated with outcomes. This classification can be used to counsel individual patients and guide decision-making with respect to treatment.

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References

  1. Ho TW, Mishu B, Li CY, Gao CY, Cornblath DR, Griffin JW, Asbury AK, Blaser MJ, McKhann GM (1995) Guillain–Barré syndrome in northern China. Relationship to Campylobacter jejuni infection and anti-glycolipid antibodies. Brain 118(Pt 3):597–605

    Article  PubMed  Google Scholar 

  2. Feasby TE, Gilbert JJ, Brown WF, Bolton CF, Hahn AF, Koopman WF, Zochodne DW (1986) An acute axonal form of Guillain–Barré polyneuropathy. Brain 109(Pt 6):1115–1126

    Article  PubMed  Google Scholar 

  3. McKhann GM, Cornblath DR, Griffin JW, Ho TW, Li CY, Jiang Z, Wu HS, Zhaori G, Liu Y, Jou LP et al (1993) Acute motor axonal neuropathy: a frequent cause of acute flaccid paralysis in China. Ann Neurol 33:333–342

    Article  CAS  PubMed  Google Scholar 

  4. Yuki N, Hartung HP (2012) Guillain–Barré syndrome. N Engl J Med 366:2294–2304

    Article  CAS  PubMed  Google Scholar 

  5. Kuwabara S, Yuki N (2013) Axonal Guillain–Barré syndrome: concepts and controversies. Lancet Neurol 12:1180–1188

    Article  PubMed  Google Scholar 

  6. Kuwabara S, Yuki N, Koga M, Hattori T, Matsuura D, Miyake M, Noda M (1998) IgG anti-GM1 antibody is associated with reversible conduction failure and axonal degeneration in Guillain–Barré syndrome. Ann Neurol 44:202–208

    Article  CAS  PubMed  Google Scholar 

  7. Capasso M, Caporale CM, Pomilio F, Gandolfi P, Lugaresi A, Uncini A (2003) Acute motor conduction block neuropathy Another Guillain–Barré syndrome variant. Neurology 61:617–622

    Article  CAS  PubMed  Google Scholar 

  8. Hiraga A, Kuwabara S, Ogawara K, Misawa S, Kanesaka T, Koga M, Yuki N, Hattori T, Mori M (2005) Patterns and serial changes in electrodiagnostic abnormalities of axonal Guillain–Barré syndrome. Neurology 64:856–860

    Article  CAS  PubMed  Google Scholar 

  9. Kokubun N, Nishibayashi M, Uncini A, Odaka M, Hirata K, Yuki N (2010) Conduction block in acute motor axonal neuropathy. Brain 133:2897–2908

    Article  PubMed  Google Scholar 

  10. Kuwabara S, Asahina M, Koga M, Mori M, Yuki N, Hattori T (1998) Two patterns of clinical recovery in Guillain–Barré syndrome with IgG anti-GM1 antibody. Neurology 51:1656–1660

    Article  CAS  PubMed  Google Scholar 

  11. Uncini A, Manzoli C, Notturno F, Capasso M (2010) Pitfalls in electrodiagnosis of Guillain–Barré syndrome subtypes. J Neurol Neurosurg Psychiatry 81:1157–1163

    Article  PubMed  Google Scholar 

  12. Kuwabara S, Ogawara K, Misawa S, Koga M, Mori M, Hiraga A, Kanesaka T, Hattori T, Yuki N (2004) Does Campylobacter jejuni infection elicit “demyelinating” Guillain–Barré syndrome? Neurology 63:529–533

    Article  CAS  PubMed  Google Scholar 

  13. Kuwabara S, Ogawara K, Misawa S, Mizobuchi K, Sung JY, Kitano Y, Mori M, Hattori T (2004) Sensory nerve conduction in demyelinating and axonal Guillain–Barré syndromes. Eur Neurol 51:196–198

    Article  PubMed  Google Scholar 

  14. Sekiguchi Y, Uncini A, Yuki N, Misawa S, Notturno F, Nasu S, Kanai K, Noto Y, Fujimaki Y, Shibuya K, Ohmori S, Sato Y, Kuwabara S (2012) Antiganglioside antibodies are associated with axonal Guillain–Barré syndrome: a Japanese-Italian collaborative study. J Neurol Neurosurg Psychiatry 83:23–28

    Article  PubMed  Google Scholar 

  15. The Italian Guillain-Barré Study Group (1996) The prognosis and main prognostic indicators of Guillain–Barré syndrome. A multicentre prospective study of 297 patients. Brain 119 (Pt 6):2053–2061

  16. The Emilia-Romagna Study group on Clinical and Epidemiological Problems in Neurology (1997) A prospective study on the incidence and prognosis of Guillain–Barré syndrome in Emilia-Romagna region, Italy (1992-1993). Neurology 48:214–221

  17. Chio A, Cocito D, Leone M, Giordana MT, Mora G, Mutani R (2003) Guillain–Barré syndrome: a prospective, population-based incidence and outcome survey. Neurology 60:1146–1150

    Article  CAS  PubMed  Google Scholar 

  18. McKhann GM, Griffin JW, Cornblath DR, Mellits ED, Fisher RS, Quaskey SA (1988) Plasmapheresis and Guillain–Barré syndrome: analysis of prognostic factors and the effect of plasmapheresis. Ann Neurol 23:347–353

    Article  CAS  PubMed  Google Scholar 

  19. Visser LH, Schmitz PI, Meulstee J, van Doorn PA, van der Meche FG (1999) Prognostic factors of Guillain–Barré syndrome after intravenous immunoglobulin or plasma exchange. Dutch Guillain–Barré Study Group. Neurology 53:598–604

    Article  CAS  PubMed  Google Scholar 

  20. Asbury AK, Cornblath DR (1990) Assessment of current diagnostic criteria for Guillain–Barré syndrome. Ann Neurol 27(Suppl):S21–S24

    Article  PubMed  Google Scholar 

  21. Yuki N, Kokubun N, Kuwabara S, Sekiguchi Y, Ito M, Odaka M, Hirata K, Notturno F, Uncini A (2012) Guillain–Barré syndrome associated with normal or exaggerated tendon reflexes. J Neurol 259:1181–1190

    Article  PubMed  Google Scholar 

  22. Hughes RA, Newsom-Davis JM, Perkin GD, Pierce JM (1978) Controlled trial prednisolone in acute polyneuropathy. Lancet 2:750–753

    Article  CAS  PubMed  Google Scholar 

  23. Kimura J (1989) electrodiagnosis in diseases of nerve and muscle: principles and practice. F.A Davis, Philadelphia

    Google Scholar 

  24. Isose S, Kuwabara S, Kokubun N, Sato Y, Mori M, Shibuya K, Sekiguchi Y, Nasu S, Fujimaki Y, Noto Y, Sawai S, Kanai K, Hirata K, Misawa S (2009) Utility of the distal compound muscle action potential duration for diagnosis of demyelinating neuropathies. J Peripher Nerv Syst 14:151–158

    Article  PubMed  Google Scholar 

  25. Kalita J, Misra UK, Das M (2008) Neurophysiological criteria in the diagnosis of different clinical types of Guillain–Barré syndrome. J Neurol Neurosurg Psychiatry 79:289–293

    Article  CAS  PubMed  Google Scholar 

  26. American Association of Electrodiagnostic M, Olney RK (1999) Guidelines in electrodiagnostic medicine. Consensus criteria for the diagnosis of partial conduction block. Muscle Nerve Suppl 8:S225–S229

    Google Scholar 

  27. Feasby TE, Hahn AF, Brown WF, Bolton CF, Gilbert JJ, Koopman WJ (1993) Severe axonal degeneration in acute Guillain–Barré syndrome: evidence of two different mechanisms? J Neurol Sci 116:185–192

    Article  CAS  PubMed  Google Scholar 

  28. Griffin JW, Li CY, Ho TW, Tian M, Gao CY, Xue P, Mishu B, Cornblath DR, Macko C, McKhann GM, Asbury AK (1996) Pathology of the motor-sensory axonal Guillain–Barré syndrome. Ann Neurol 39:17–28

    Article  CAS  PubMed  Google Scholar 

  29. Yuki N (2001) Infectious origins of, and molecular mimicry in, Guillain–Barré and Fisher syndromes. Lancet Infect Dis 1:29–37

    Article  CAS  PubMed  Google Scholar 

  30. Ogawara K, Kuwabara S, Mori M, Hattori T, Koga M, Yuki N (2000) Axonal Guillain–Barré syndrome: relation to anti-ganglioside antibodies and Campylobacter jejuni infection in Japan. Ann Neurol 48:624–631

    Article  CAS  PubMed  Google Scholar 

  31. Yuki N, Taki T, Inagaki F, Kasama T, Takahashi M, Saito K, Handa S, Miyatake T (1993) A bacterium lipopolysaccharide that elicits Guillain–Barré syndrome has a GM1 ganglioside-like structure. J Exp Med 178:1771–1775

    Article  CAS  PubMed  Google Scholar 

  32. Yuki N, Susuki K, Koga M, Nishimoto Y, Odaka M, Hirata K, Taguchi K, Miyatake T, Furukawa K, Kobata T, Yamada M (2004) Carbohydrate mimicry between human ganglioside GM1 and Campylobacter jejuni lipooligosaccharide causes Guillain–Barré syndrome. Proc Natl Acad Sci USA 101:11404–11409

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  33. Clouston PD, Kiers L, Zuniga G, Cros D (1994) Quantitative analysis of the compound muscle action potential in early acute inflammatory demyelinating polyneuropathy. Electroencephalogr Clin Neurophysiol 93:245–254

    Article  CAS  PubMed  Google Scholar 

  34. Baba M, Matsunaga M (1984) Recovery from acute demyelinating conduction block in the presence of prolonged distal conduction delay due to peripheral nerve constriction. Electromyogr Clin Neurophysiol 24:611–617

    CAS  PubMed  Google Scholar 

  35. Susuki K, Rasband MN, Tohyama K, Koibuchi K, Okamoto S, Funakoshi K, Hirata K, Baba H, Yuki N (2007) Anti-GM1 antibodies cause complement-mediated disruption of sodium channel clusters in peripheral motor nerve fibers. J Neurosci 27:3956–3967

    Article  CAS  PubMed  Google Scholar 

  36. Griffin JW, Li CY, Macko C, Ho TW, Hsieh ST, Xue P, Wang FA, Cornblath DR, McKhann GM, Asbury AK (1996) Early nodal changes in the acute motor axonal neuropathy pattern of the Guillain–Barré syndrome. J Neurocytol 25:33–51

    Article  CAS  PubMed  Google Scholar 

  37. Susuki K, Yuki N, Schafer DP, Hirata K, Zhang G, Funakoshi K, Rasband MN (2012) Dysfunction of nodes of Ranvier: a mechanism for anti-ganglioside antibody-mediated neuropathies. Exp Neurol 233:534–542

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  38. Kaida K, Sonoo M, Ogawa G, Kamakura K, Ueda-Sada M, Arita M, Motoyoshi K, Kusunoki S (2008) GM1/GalNAc-GD1a complex: a target for pure motor Guillain–Barré syndrome. Neurology 71:1683–1690

    Article  CAS  PubMed  Google Scholar 

  39. Kusunoki S, Kaida K (2011) Antibodies against ganglioside complexes in Guillain–Barré syndrome and related disorders. J Neurochem 116:828–832

    Article  CAS  PubMed  Google Scholar 

  40. Hiraga A, Mori M, Ogawara K, Hattori T, Kuwabara S (2003) Differences in patterns of progression in demyelinating and axonal Guillain–Barré syndromes. Neurology 61:471–474

    Article  CAS  PubMed  Google Scholar 

  41. van Koningsveld R, Steyerberg EW, Hughes RA, Swan AV, van Doorn PA, Jacobs BC (2007) A clinical prognostic scoring system for Guillain–Barré syndrome. Lancet Neurol 6:589–594

    Article  PubMed  Google Scholar 

  42. Walgaard C, Lingsma HF, Ruts L, van Doorn PA, Steyerberg EW, Jacobs BC (2011) Early recognition of poor prognosis in Guillain–Barré syndrome. Neurology 76:968–975

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Department of Internal Medicine I, Osaka Medical College, Daigakumachi 2-7, Takatsuki, Osaka, 569-8686, Japan

    Takafumi Hosokawa, Hideto Nakajima, Kiichi Unoda, Kazushi Yamane, Yoshimitsu Doi, Shimon Ishida, Fumiharu Kimura & Toshiaki Hanafusa

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  1. Takafumi Hosokawa
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  2. Hideto Nakajima
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  3. Kiichi Unoda
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  4. Kazushi Yamane
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Correspondence to Takafumi Hosokawa.

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Hosokawa, T., Nakajima, H., Unoda, K. et al. An electrophysiological classification associated with Guillain–Barré syndrome outcomes. J Neurol 261, 1986–1993 (2014). https://doi.org/10.1007/s00415-014-7452-2

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  • DOI: https://doi.org/10.1007/s00415-014-7452-2

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