Guillain-Barré syndrome associated with SARS-CoV-2 infection: A systematic review and individual participant data meta-analysis
Imran Hasan
Laboratory of Gut-Brain Signaling, Laboratory Sciences and Services Division, icddr,b, Dhaka, Bangladesh
Search for more papers by this authorKM Saif-Ur-Rahman
Health Systems and Population Studies Division, icddr,b, Dhaka, Bangladesh
Department of Public Health and Health Systems, Graduate School of Medicine, Nagoya University, Nagoya, Japan
Search for more papers by this authorShoma Hayat
Laboratory of Gut-Brain Signaling, Laboratory Sciences and Services Division, icddr,b, Dhaka, Bangladesh
Search for more papers by this authorNowshin Papri
Laboratory of Gut-Brain Signaling, Laboratory Sciences and Services Division, icddr,b, Dhaka, Bangladesh
Department of Neurology, Erasmus MC, University Medical Center, Rotterdam, The Netherlands
Search for more papers by this authorIsrat Jahan
Laboratory of Gut-Brain Signaling, Laboratory Sciences and Services Division, icddr,b, Dhaka, Bangladesh
Search for more papers by this authorRufydha Azam
Laboratory of Gut-Brain Signaling, Laboratory Sciences and Services Division, icddr,b, Dhaka, Bangladesh
Search for more papers by this authorGulshan Ara
Nutrition and Clinical Services Division, icddr,b, Dhaka, Bangladesh
Search for more papers by this authorCorresponding Author
Zhahirul Islam
Laboratory of Gut-Brain Signaling, Laboratory Sciences and Services Division, icddr,b, Dhaka, Bangladesh
Correspondence
Dr. Zhahirul Islam, PhD, Laboratory of Gut-Brain Signaling, Laboratory Sciences and Services Division, icddr,b, 68, Shaheed Tajuddin Ahmad Sarani, Mohakhali, Dhaka 1212, Bangladesh.
Email: [email protected]
Search for more papers by this authorImran Hasan
Laboratory of Gut-Brain Signaling, Laboratory Sciences and Services Division, icddr,b, Dhaka, Bangladesh
Search for more papers by this authorKM Saif-Ur-Rahman
Health Systems and Population Studies Division, icddr,b, Dhaka, Bangladesh
Department of Public Health and Health Systems, Graduate School of Medicine, Nagoya University, Nagoya, Japan
Search for more papers by this authorShoma Hayat
Laboratory of Gut-Brain Signaling, Laboratory Sciences and Services Division, icddr,b, Dhaka, Bangladesh
Search for more papers by this authorNowshin Papri
Laboratory of Gut-Brain Signaling, Laboratory Sciences and Services Division, icddr,b, Dhaka, Bangladesh
Department of Neurology, Erasmus MC, University Medical Center, Rotterdam, The Netherlands
Search for more papers by this authorIsrat Jahan
Laboratory of Gut-Brain Signaling, Laboratory Sciences and Services Division, icddr,b, Dhaka, Bangladesh
Search for more papers by this authorRufydha Azam
Laboratory of Gut-Brain Signaling, Laboratory Sciences and Services Division, icddr,b, Dhaka, Bangladesh
Search for more papers by this authorGulshan Ara
Nutrition and Clinical Services Division, icddr,b, Dhaka, Bangladesh
Search for more papers by this authorCorresponding Author
Zhahirul Islam
Laboratory of Gut-Brain Signaling, Laboratory Sciences and Services Division, icddr,b, Dhaka, Bangladesh
Correspondence
Dr. Zhahirul Islam, PhD, Laboratory of Gut-Brain Signaling, Laboratory Sciences and Services Division, icddr,b, 68, Shaheed Tajuddin Ahmad Sarani, Mohakhali, Dhaka 1212, Bangladesh.
Email: [email protected]
Search for more papers by this authorAbstract
Several published reports have described a possible association between Guillain-Barré syndrome (GBS) and severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2) infection. This systematic review aimed to summarize and meta-analyze the salient features and prognosis of SARS-CoV-2-associated GBS. We searched the PubMed (Medline), Web of Science and Cochrane databases for articles published between 01 January 2020 and 05 August 2020 using SARS-CoV-2 and GBS-related keywords. Data on sociodemographic characteristics, antecedent symptoms, clinical, serological and electrophysiological features, and hospital outcomes were recorded. We included 45 articles from 16 countries reporting 61 patients with SARS-CoV-2-associated GBS. Most (97.7%) articles were from high- and upper-middle-income countries. Forty-two (68.9%) of the patients were male; median (interquartile range) age was 57 (49-70) years. Reverse transcriptase polymerase chain reaction for SARS-CoV-2 was positive in 90.2% of patients. One report of SARS-CoV-2-associated familial GBS was found which affected a father and daughter of a family. Albuminocytological dissociation in cerebrospinal fluid was found in 80.8% of patients. The majority of patients (75.5%) had a demyelinating subtype of GBS. Intravenous immunoglobulin and plasmapheresis were given to 92.7% and 7.3% of patients, respectively. Around two-thirds (65.3%) of patients had a good outcome (GBS-disability score ≤ 2) on discharge from hospital. Two patients died in hospital. SARS-CoV-2-associated GBS mostly resembles the classical presentations of GBS that respond to standard treatments. Extensive surveillance is required in low- and lower-middle-income countries to identify and report similar cases/series. Further large-scale case-control studies are warranted to strengthen the current evidence. PROSPERO Registration Number CRD42020201673.
CONFLICT OF INTERESTS
Zhahirul Islam received grants from the Fogarty International Center, National Institute of Neurological Disorders and Stroke of the National Institutes of Health, USA under Award Number K43 TW011447 and Annexon Biosciences (South San Francisco, CA 94080, USA). The other authors do not have any conflict of interests.
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REFERENCES
- 1 Coronavirus Resource Center - Johns Hopkins University. Accessed 8 October 2020. https://coronavirus.jhu.edu/map.html.
- 2Huang C, Wang Y, Li X, et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet. 2020; 395(10223): 497-506.
- 3Mao L, Jin H, Wang M, et al. Neurologic manifestations of hospitalized patients with coronavirus disease 2019 in Wuhan, China. JAMA Neurol. 2020; 77(6): 683-690.
- 4Helms J, Kremer S, Merdji H, et al. Neurologic features in severe SARS-CoV-2 infection. N Engl J Med. 2020; 382(23): 2268-2270.
- 5Cao-Lormeau V-M, Blake A, Mons S, et al. Guillain-Barré syndrome outbreak associated with Zika virus infection in French Polynesia: a case-control study. Lancet. 2016; 387(10027): 1531-1539.
- 6Kim JE, Heo JH, Kim HO, et al. Neurological complications during treatment of Middle East respiratory syndrome. J Clin Neurol. 2017; 13(3): 227-233.
- 7Carrillo-Larco R, Altez-Fernandez C, Ravaglia S, Vizcarra J. COVID-19 and Guillain-Barre syndrome: a systematic review of case reports. Wellcome Open Res. 2020; 5(107).
- 8De Sanctis P, Doneddu PE, Viganò L, Selmi C, Nobile-Orazio E. Guillain Barré syndrome associated with SARS-CoV-2 infection. A systematic review. Eur J Neurol. 2020; 27: 2361–2370.
- 9Abu-Rumeileh S, Abdelhak A, Foschi M, Tumani H, Otto M. Guillain-Barré syndrome spectrum associated with COVID-19: an up-to-date systematic review of 73 cases. J Neurol. 2020.
- 10Uncini A, Vallat J-M, Jacobs BC. Guillain-Barré syndrome in SARS-CoV-2 infection: an instant systematic review of the first six months of pandemic. J Neurol Neurosurg Psychiatry Res. 2020; 91: 1105–1110.
10.1136/jnnp-2020-324491 Google Scholar
- 11Moher D, Shamseer L, Clarke M, et al. Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015 statement. Syst Rev. 2015; 4(1): 1.
- 12Shamseer L, Moher D, Clarke M, et al. Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015: elaboration and explanation. Br Med J. 2015; g7647: 349.
- 13Asbury AK, Cornblath DR. Assessment of current diagnostic criteria for Guillain-Barré syndrome. Ann Neurol. 1990; 27(S1): S21-S24.
- 14Sejvar 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.
- 15Hughes RA, Newsom-Davis JM, Perkin GD, Pierce JM. Controlled trial prednisolone in acute polyneuropathy. Lancet. 1978; 2(8093): 750-753.
- 16Ouzzani M, Hammady H, Fedorowicz Z, Elmagarmid A. Rayyan—a web and mobile app for systematic reviews. Syst Rev. 2016; 5(1):210.
- 17 JBI Critical Appraisal Tools. Accessed 27 July 2020. https://joannabriggs.org/critical-appraisal-tools.
- 18Gigli GL, Bax F, Marini A, et al. Guillain-Barré syndrome in the COVID-19 era: just an occasional cluster? J Neurol. 2020; 1-3.
- 19Paterson RW, Brown RL, Benjamin L, et al. The emerging spectrum of COVID-19 neurology: clinical, radiological and laboratory findings. Brain. 2020; 143(10): 3104–3120.
- 20Abrams RMC, Kim BD, Markantone DM, et al. Severe rapidly progressive Guillain-Barré syndrome in the setting of acute COVID-19 disease. J Neurovirol. 2020; 26: 797-799.
- 21Agosti E, Giorgianni A, D'Amore F, Vinacci G, Balbi S, Locatelli D. Is Guillain-Barrè syndrome triggered by SARS-CoV-2? Case report and literature review. Neurol Sci. 2020.
- 22Alberti P, Beretta S, Piatti M, et al. Guillain-Barré syndrome related to COVID-19 infection. Neurol Neuroimmunol Neruroinflamm. 2020; 7(4): e741.
- 23Arnaud S, Budowski C, Ng Wing Tin S, Degos B. Post SARS-CoV-2 Guillain-Barré syndrome. Clin Neurophysiol. 2020; 131(7): 1652-1654.
- 24Assini A, Benedetti L, Di Maio S, Schirinzi E, Del Sette M. New clinical manifestation of COVID-19 related Guillain-Barrè syndrome highly responsive to intravenous immunoglobulins: two Italian cases. Neurol Sci. 2020; 41(7): 1657–1658.
- 25Bigaut K, Mallaret M, Baloglu S, et al. Guillain-Barré syndrome related to SARS-CoV-2 infection. Neurol Neuroimmunol Neuroinflamm. 2020; 7(5): e785
- 26Camdessanche JP, Morel J, Pozzetto B, Paul S, Tholance Y, Botelho-Nevers E. COVID-19 may induce Guillain-Barré syndrome. Rev Neurol. 2020; 176(6): 516-518.
- 27Chan JL, Ebadi H, Sarna JR. Guillain-Barré syndrome with facial diplegia related to SARS-CoV-2 infection. Can J Neurol Sci. 2020;-.
- 28Coen M, Jeanson G, Culebras Almeida LA, et al. Guillain-Barré syndrome as a complication of SARS-CoV-2 infection. Brain Behav Immun. 2020; 87: 111-112.
- 29El Otmani H, El Moutawakil B, Rafai MA, et al. Covid-19 and Guillain-Barré syndrome: more than a coincidence! Rev Neurol. 2020; 176(6): 518-519.
- 30Elkhouly A, Kaplan AC. Noteworthy neurological manifestations associated with COVID-19 infection. Cureus. 2020; 12(7):e8992.
- 31Esteban Molina A, Mata Martínez M, Sánchez Chueca P, Carrillo López A, Sancho Val I, Sanjuan-Villarreal TA. Guillain-Barré syndrome associated with SARS-CoV-2 infection. Medicina Intensiva. 2020; S0210-5691(20): 30154–30156.
- 32Farzi MA, Ayromlou H, Jahanbakhsh N, Bavil PH, Janzadeh A, Shayan FK. Guillain-Barré syndrome in a patient infected with SARS-CoV-2, a case report. J Neuroimmunol. 2020; 346:577294.
- 33Fernández-Domínguez J, Ameijide-Sanluis E, García-Cabo C, García-Rodríguez R, Mateos V. Miller-fisher-like syndrome related to SARS-CoV-2 infection (COVID 19). J Neurol. 2020; 267(9): 2495-2496.
- 34Frank CHM, Almeida TVR, Marques EA, et al. Guillain-Barré syndrome associated with SARS-CoV-2 infection in a pediatric patient. J Trop Pediatr. 2020.
- 35García-Manzanedo S, López de la Oliva Calvo L, Ruiz Álvarez L. Guillain-barré syndrome after covid-19 infection. Med Clin. 2020; 155: 366.
- 36Gutiérrez-Ortiz C, Méndez-Guerrero A, Rodrigo-Rey S, et al. Miller fisher syndrome and polyneuritis cranialis in COVID-19. Neurology. 2020; 95(5):e601.
- 37Helbok R, Beer R, Löscher W, et al. Guillain-Barré syndrome in a patient with antibodies against SARS-COV-2. Eur J Neurol. 2020; 27: 1754-1756.
- 38Hutchins KL, Jansen JH, Comer AD, et al. COVID-19-associated bifacial weakness with Paresthesia subtype of Guillain-Barré syndrome. Am J Neuroradiol. 2020; 41(9): 1707–1711.
- 39Khalifa M, Zakaria F, Ragab Y, et al. Guillain-Barre syndrome associated with SARS-CoV-2 detection and a COVID-19 infection in a child. J Pediatric Infect Dis Soc. 2020; 9(4): 510–513.
- 40Kilinc D, van de Pasch S, Doets AY, Jacobs BC, van Vliet J, Garssen MPJ. Guillain-Barré syndrome after SARS-CoV-2 infection. Eur J Neurol. 2020; 27: 1757-1758.
- 41Lantos JE, Strauss SB, Lin E. COVID-19-associated miller fisher syndrome: MRI findings. Am J Neuroradiol. 2020; 41(7): 1184-1186.
- 42Lascano AM, Epiney JB, Coen M, et al. SARS-CoV-2 and Guillain-Barré syndrome: AIDP variant with favorable outcome. Eur J Neurol. 2020; 27: 1751-1753.
- 43Manganotti P, Bellavita G, D'Acunto L, et al. Clinical neurophysiology and cerebrospinal liquor analysis to detect Guillain-Barré syndrome and polyneuritis cranialis in COVID-19 patients: a case series. J Med Virol. 2020.
- 44Manganotti P, Pesavento V, Buoite Stella A, et al. Miller fisher syndrome diagnosis and treatment in a patient with SARS-CoV-2. J Neurovirol. 2020; 26: 605-606.
- 45Marta-Enguita J, Rubio-Baines I, Gastón-Zubimendi I. Fatal Guillain-Barre syndrome after infection with SARS-CoV-2. Neurologia. 2020; 35(4): 265-267.
- 46Oguz-Akarsu E, Ozpar R, Mirzayev H, et al. Guillain-Barré syndrome in a patient with minimal symptoms of COVID-19 infection. Muscle Nerve. 2020; 62(3): E54–E57.
- 47Ottaviani D, Boso F, Tranquillini E, et al. Early Guillain-Barré syndrome in coronavirus disease 2019 (COVID-19): a case report from an Italian COVID-hospital. Neurol Sci. 2020; 41(6): 1351-1354.
- 48Padroni M, Mastrangelo V, Asioli GM, et al. Guillain-Barré syndrome following COVID-19: new infection, old complication? J Neurol. 2020; 267(7): 1877-1879.
- 49Rana S, Lima AA, Chandra R, et al. Novel coronavirus (COVID-19)-associated Guillain-Barré syndrome: case report. J Clin Neuromuscul Dis. 2020; 21(4): 240-242.
- 50Reyes-Bueno JA, García-Trujillo L, Urbaneja P, et al. Miller-fisher syndrome after SARS-CoV-2 infection. Eur J Neurol. 2020; 27: 1759-1761.
- 51Riva N, Russo T, Falzone YM, et al. Post-infectious Guillain-Barré syndrome related to SARS-CoV-2 infection: a case report. J Neurol. 2020; 267(9): 2492-2494.
- 52Paybast S, Gorji R, Mavandadi S. Guillain-Barré syndrome as a neurological complication of novel COVID-19 infection: a case report and review of the literature. Neurologist. 2020; 25(4): 101-103.
- 53Sancho-Saldaña A, Lambea-Gil Á, Liesa JLC, et al. Guillain-Barré syndrome associated with leptomeningeal enhancement following SARS-CoV-2 infection. Clin Med. 2020; 20: e93-e94.
- 54Scheidl E, Canseco DD, Hadji-Naumov A, Bereznai B. Guillain-Barré syndrome during SARS-CoV-2 pandemic: a case report and review of recent literature. J Peripher Nerv Syst. 2020; 25(2): 204-207.
- 55Sedaghat Z, Karimi N. Guillain Barre syndrome associated with COVID-19 infection: a case report. J Clin Neurosci. 2020; 76: 233-235.
- 56Su XW, Palka SV, Rao RR, Chen FS, Brackney CR, Cambi F. SARS-CoV-2-associated Guillain-Barré syndrome with dysautonomia. Muscle Nerve. 2020; 62: E48-E49.
- 57Tiet MY, AlShaikh N. Guillain-Barré syndrome associated with COVID-19 infection: a case from the UK. BMJ Case Rep. 2020; 13(7):e236536.
- 58Toscano G, Palmerini F, Ravaglia S, et al. Guillain-Barré syndrome associated with SARS-CoV-2. New Engl J Med. 2020; 382(26): 2574-2576.
- 59Velayos Galán A, Del Saz Saucedo P, Peinado Postigo F, Botia Paniagua E. Guillain-Barré syndrome associated with SARS-CoV-2 infection. Neurologia. 2020; 35(4): 268-269.
- 60Virani A, Rabold E, Hanson T, et al. Guillain-Barré syndrome associated with SARS-CoV-2 infection. IDCases. 2020; 20:e00771.
- 61Webb S, Wallace VC, Martin-Lopez D, Yogarajah M. Guillain-Barré syndrome following COVID-19: a newly emerging post-infectious complication. BMJ Case Rep. 2020; 13(6):e236182.
- 62Zhao H, Shen D, Zhou H, Liu J, Chen S. Guillain-Barré syndrome associated with SARS-CoV-2 infection: causality or coincidence? Lancet Neurol. 2020; 19(5): 383-384.
- 63Willison HJ, Jacobs BC, van Doorn PA. Guillain-Barré syndrome. Lancet. 2016; 388(10045): 717-727.
- 64Islam Z, Jacobs BC, van Belkum A, et al. Axonal variant of Guillain-Barre syndrome associated with campylobacter infection in Bangladesh. Neurology. 2010; 74(7): 581-587.
- 65Dalakas MC. Guillain-Barré syndrome: the first documented COVID-19-triggered autoimmune neurologic disease: more to come with myositis in the offing. Neurol Neuroimmunol Neuroinflamm. 2020; 7(5): e781.
- 66Islam Z, Hasan I, Mohammad QD. Guillain-Barré syndrome in developing countries in the COVID-19 era. J Neurol Neurosurg Psychiatry. 2020. https://jnnp.bmj.com/content/91/10/1105.responses.
- 67O'Donnell O. Access to health care in developing countries: breaking down demand side barriers. Cad Saúde Pública. 2007; 23: 2820-2834.
- 68Fritzen SA. Strategic management of the health workforce in developing countries: what have we learned? Hum Resour Health. 2007; 5(1):4.
- 69Kannampallil TG, Goss CW, Evanoff BA, Strickland JR, McAlister RP, Duncan J. Exposure to COVID-19 patients increases physician trainee stress and burnout. PLoS One. 2020; 15(8):e0237301.
- 70Tatu L, Nono S, Grácio S, Koçer S. Guillain-Barré syndrome in the COVID-19 era: another occasional cluster? J Neurol. 2020.
- 71Brizzi KT, Lyons JL. Peripheral nervous system manifestations of infectious diseases. Neurohospitalist. 2014; 4(4): 230-240.
- 72Uncini A, Shahrizaila N, Kuwabara S. Zika virus infection and Guillain-Barré syndrome: a review focused on clinical and electrophysiological subtypes. J Neurol Neurosurg Psychiatry. 2017; 88(3): 266-271.
- 73Qin J, You C, Lin Q, Hu T, Yu S, Zhou XH. Estimation of incubation period distribution of COVID-19 using disease onset forward time: a novel cross-sectional and forward follow-up study. Science Advances. 2020; 6(33): eabc1202.