Risk of Guillain-Barré syndrome after 2010-2011 influenza vaccination

Francesca Galeotti, Marco Massari, Roberto D'Alessandro, Ettore Beghi, Adriano Chiò, Giancarlo Logroscino, Graziella Filippini, Maria Donata Benedetti, Maura Pugliatti, Carmela Santuccio, Roberto Raschetti, ITANG study group, Roberto Michelucci, Patrizia Riguzzi, Tommaso Sacquegna, Anna Maria Borghi, Scienze Neurologiche, Vittoria Mussuto, Patrizia De Massis, Fabio Cirignotta, Rita Rinaldi, Walter Neri, Carlo Guidi, Maria Rosaria, Enrico Granieri, Valentina Simioni, Paolo Nichelli, Jessica Mandrioli, Donata Guidetti, Emilio Terlizzi, Mario Giovanni Terzano, Giovanni Pavesi, Fabrizio Rasi, Claudio Callegarini, Norina Marcello, Massimo Bondavalli, Alessandro Ravasio, Marco Curro'Dossi, Annamaria Mauro, Chiara Minardi, Gabriele Greco, Stefano Amidei, Enrico Montanari, Doriana Medici, Tommaso Riccardi, Elisabetta D'Adda, Luigi Bettoni, Luciano Abruzzi, Elio Agostoni, Francesco Basso, Andrea Magnoni, Vittorio Crespi, Maria Repaci, Antonella Cheldi, Mariagrazia Bellotti, Carlo Ferrarese, Natale Augusto Curto, Giovanni Meola, Giuseppe Rotondo, Eduardo Nobile-Orazio, Fabrizia Terenghi, Franco Sasanelli, Alessio Galbussera, Marco Mattioli, Marco Tiriticco Azienda, Caterina Nascimbene, Alessandra Vanotti, Stefano Jann, Luisa De Toni Franceschini, Vincenzo Silani, Nicola Ticozzi, Giancarlo Comi, Raffaella Fazio, Patrizia Perrone, Andrea Giorgetti, Alessandro Romorini, Pietro Bassi, Domenico Santoro, Nereo Bresolin, Simone Tonietti, Massimo Suardelli, Giacomo Bezzi, Daria Baldini, Angelo Maurizio Clerici, Giuseppina Cafazzo, Daniele Porazzi, Isidoro La Spina, Giampiero Grampa, Davide Zarcone, Michele Perini, Marco Poloni, Emanuela Agazzi, Massimiliano Filosto, Alessandro Padovani, Renato Besana, Edoardo Donati, Eugenio Magni, Marco Arnaboldi, Vincenzo Belcastro, Mario Guidotti, Maurizio Riva, Eugenio Vitelli, Paolo Previdi, Giuseppe Micieli, Elisa Candeloro, Carlo Dallocchio, Carla Arbasino, Andrea Calvo, Cristina Moglia, Marco Vercellino, Bruno Ferrero, Pietro Pignatta, Enrico Oddenino, Daniele Imperiale, Daniela Leotta, Maurizio Gionco, Carlo Ravetti, Roberto Cavallo, Nicoletta Di Vito, Claudio Geda, Simona Bortolotto, Emilio Luda di Cortemiglia, Giovanna Liotta, Emilio Ursino, Mario Palermo, Luca Ambrogio, Piero Meineri, Michele Dotta, Paolo Ghiglione, Joseph Maistrelli, Susana Onorato, Maurizio Leone, Diego Maria Papurello, Angelo Villani, Roberto Conti, Franco Coppo, Fabiana Tesser, Lucia Testa, Silvia Isabella Cattaneo, Maria Teresa Penza, Graziano Gusmaroli, Katia Savio, Franco Perla, Ceva Mondovı, Fabrizio Pisano, Fabio Poglio, Luca Pradotto, Edo Fausto Bottacchi, Paolo Livrea, Francesco Federico, Maria Trojano, Vito Covelli, Bruno Maggio, Vito Santamato, Bruno Passarella, Giovanni Zimatore, Giorgio Trianni, Gerardo Ciardo, Salvatore Interno, Corrado Marchini, Sandro Zambito Marsala, Giorgio Michieli, Carlo Borsato, Giuseppe Didone, Emma Frasson, Alberto Polo, Vincenza Argentiero, Vincenzo Romeo, Novenia Perlotto, Roberto L'Erario, Gianfranco Micaglio, Tiziana Rosso, Sandro Bruno, Bruno Giometto, Mirco Serena, Rocco Quatrale, Ernesto Gastaldo, Francesco Perini, Michele DiLeone, Alessandro Casano, Lauretta Silvestri, Alessandro Burlina, Virginia Munerati, Sebastiano D'Anna, Flavio Sanson, Valeria Sartori, Giuseppe Moretto, Giovanna Squintani, Salvatore Monaco, Maria Donata Benedetti, Simone Fusina, Claudio Bianconi, Fabiana Pimazzoni, Angela Bonometti, Giampietro Zanette, Marco Turatti, Stefania Leoni, Giuseppe Mura, Anna Ticca, Piernicola Marchi, Davide Manca, Francesca Galeotti, Marco Massari, Roberto D'Alessandro, Ettore Beghi, Adriano Chiò, Giancarlo Logroscino, Graziella Filippini, Maria Donata Benedetti, Maura Pugliatti, Carmela Santuccio, Roberto Raschetti, ITANG study group, Roberto Michelucci, Patrizia Riguzzi, Tommaso Sacquegna, Anna Maria Borghi, Scienze Neurologiche, Vittoria Mussuto, Patrizia De Massis, Fabio Cirignotta, Rita Rinaldi, Walter Neri, Carlo Guidi, Maria Rosaria, Enrico Granieri, Valentina Simioni, Paolo Nichelli, Jessica Mandrioli, Donata Guidetti, Emilio Terlizzi, Mario Giovanni Terzano, Giovanni Pavesi, Fabrizio Rasi, Claudio Callegarini, Norina Marcello, Massimo Bondavalli, Alessandro Ravasio, Marco Curro'Dossi, Annamaria Mauro, Chiara Minardi, Gabriele Greco, Stefano Amidei, Enrico Montanari, Doriana Medici, Tommaso Riccardi, Elisabetta D'Adda, Luigi Bettoni, Luciano Abruzzi, Elio Agostoni, Francesco Basso, Andrea Magnoni, Vittorio Crespi, Maria Repaci, Antonella Cheldi, Mariagrazia Bellotti, Carlo Ferrarese, Natale Augusto Curto, Giovanni Meola, Giuseppe Rotondo, Eduardo Nobile-Orazio, Fabrizia Terenghi, Franco Sasanelli, Alessio Galbussera, Marco Mattioli, Marco Tiriticco Azienda, Caterina Nascimbene, Alessandra Vanotti, Stefano Jann, Luisa De Toni Franceschini, Vincenzo Silani, Nicola Ticozzi, Giancarlo Comi, Raffaella Fazio, Patrizia Perrone, Andrea Giorgetti, Alessandro Romorini, Pietro Bassi, Domenico Santoro, Nereo Bresolin, Simone Tonietti, Massimo Suardelli, Giacomo Bezzi, Daria Baldini, Angelo Maurizio Clerici, Giuseppina Cafazzo, Daniele Porazzi, Isidoro La Spina, Giampiero Grampa, Davide Zarcone, Michele Perini, Marco Poloni, Emanuela Agazzi, Massimiliano Filosto, Alessandro Padovani, Renato Besana, Edoardo Donati, Eugenio Magni, Marco Arnaboldi, Vincenzo Belcastro, Mario Guidotti, Maurizio Riva, Eugenio Vitelli, Paolo Previdi, Giuseppe Micieli, Elisa Candeloro, Carlo Dallocchio, Carla Arbasino, Andrea Calvo, Cristina Moglia, Marco Vercellino, Bruno Ferrero, Pietro Pignatta, Enrico Oddenino, Daniele Imperiale, Daniela Leotta, Maurizio Gionco, Carlo Ravetti, Roberto Cavallo, Nicoletta Di Vito, Claudio Geda, Simona Bortolotto, Emilio Luda di Cortemiglia, Giovanna Liotta, Emilio Ursino, Mario Palermo, Luca Ambrogio, Piero Meineri, Michele Dotta, Paolo Ghiglione, Joseph Maistrelli, Susana Onorato, Maurizio Leone, Diego Maria Papurello, Angelo Villani, Roberto Conti, Franco Coppo, Fabiana Tesser, Lucia Testa, Silvia Isabella Cattaneo, Maria Teresa Penza, Graziano Gusmaroli, Katia Savio, Franco Perla, Ceva Mondovı, Fabrizio Pisano, Fabio Poglio, Luca Pradotto, Edo Fausto Bottacchi, Paolo Livrea, Francesco Federico, Maria Trojano, Vito Covelli, Bruno Maggio, Vito Santamato, Bruno Passarella, Giovanni Zimatore, Giorgio Trianni, Gerardo Ciardo, Salvatore Interno, Corrado Marchini, Sandro Zambito Marsala, Giorgio Michieli, Carlo Borsato, Giuseppe Didone, Emma Frasson, Alberto Polo, Vincenza Argentiero, Vincenzo Romeo, Novenia Perlotto, Roberto L'Erario, Gianfranco Micaglio, Tiziana Rosso, Sandro Bruno, Bruno Giometto, Mirco Serena, Rocco Quatrale, Ernesto Gastaldo, Francesco Perini, Michele DiLeone, Alessandro Casano, Lauretta Silvestri, Alessandro Burlina, Virginia Munerati, Sebastiano D'Anna, Flavio Sanson, Valeria Sartori, Giuseppe Moretto, Giovanna Squintani, Salvatore Monaco, Maria Donata Benedetti, Simone Fusina, Claudio Bianconi, Fabiana Pimazzoni, Angela Bonometti, Giampietro Zanette, Marco Turatti, Stefania Leoni, Giuseppe Mura, Anna Ticca, Piernicola Marchi, Davide Manca

Abstract

Influenza vaccination has been implicated in Guillain Barré Syndrome (GBS) although the evidence for this link is controversial. A case-control study was conducted between October 2010 and May 2011 in seven Italian Regions to explore the relation between influenza vaccination and GBS. The study included 176 GBS incident cases aged ≥18 years from 86 neurological centers. Controls were selected among patients admitted for acute conditions to the Emergency Department of the same hospital as cases. Each control was matched to a case by sex, age, Region and admission date. Two different analyses were conducted: a matched case-control analysis and a self-controlled case series analysis (SCCS). Case-control analysis included 140 cases matched to 308 controls. The adjusted matched odds ratio (OR) for GBS occurrence within 6 weeks after influenza vaccination was 3.8 (95 % CI: 1.3, 10.5). A much stronger association with gastrointestinal infections (OR = 23.8; 95 % CI 7.3, 77.6) and influenza-like illness or upper respiratory tract infections (OR = 11.5; 95 % CI 5.6, 23.5) was highlighted. The SCCS analysis included all 176 GBS cases. Influenza vaccination was associated with GBS, with a relative risk of 2.1 (95 % CI 1.1, 3.9). According to these results the attributable risk in adults ranges from two to five GBS cases per 1,000,000 vaccinations.

Figures

Fig. 1
Fig. 1
Diagram of the observation period for the self-controlled case-series (SCSS) method
Fig. 2
Fig. 2
Recruitment of participants in the study. The reasons for exclusion from the Brighton criteria were: alternative explanation of symptoms (11 cases), course not monophasic (11), nadir of symptoms not reached between 12 h and 28 days after symptoms onset (5), absence of bilateral limbs weakness (18), conservation of tendon stretching reflexes (4); missing data (4 patients)
Fig. 3
Fig. 3
Forest plot showing the results of the final conditional regression analysis. a ILI = Influenza-like illness; URI = Upper respiratory tract infections, b Any occurrence of chronic comorbidities among: malignancies, immunocompromised states (e.g. transplantation, use of immunosuppressants, HIV infection), autoimmune disorders (e.g. thyroiditis, diabetes type I, rheumatoid arthritis, vasculitis) and past surgical intervention

References

    1. Sejvar JJ, Baughman AL, Wise M, et al. Population incidence of Guillain-Barré syndrome: a systematic review and meta-analysis. Neuroepidemiology. 2011;36(2):123–133. doi: 10.1159/000324710.
    1. van Doorn PA, Ruts L, Jacobs BC. Clinical features, pathogenesis, and treatment of Guillain-Barré syndrome. Lancet Neurol. 2008;7(10):939–950. doi: 10.1016/S1474-4422(08)70215-1.
    1. Schonberger LB, Bregman DJ, Sullivan-Bolyai JZ, et al. Guillain-Barré syndrome following vaccination in the national influenza immunization program, United States, 1976–1977. Am J Epidemiol. 1979;110(2):105–123.
    1. Hurwitz ES, Schonberger LB, Nelson DB, et al. Guillain-Barré syndrome and the 1978–1979 influenza vaccine. N Engl J Med. 1981;304(26):1557–1561. doi: 10.1056/NEJM198106253042601.
    1. Kaplan JE, Katona P, Hurwitz ES, et al. Guillain-Barré syndrome in the United States, 1979–1980 and 1980–1981. Lack of an association with influenza vaccination. JAMA. 1982;248(6):698–700. doi: 10.1001/jama.1982.03330060038030.
    1. Roscelli JD, Bass JW, Pang L. Guillain-Barré syndrome and influenza vaccination in the US Army, 1980–1988. Am J Epidemiol. 1991;133(9):952–955.
    1. Chen R, Kent J, Rhodes P. Investigation of a possible association between influenza vaccination and Guillain-Barré syndrome in the United States, 1990–1991. Post Mark Surveill. 1992;6:5–6.
    1. Lasky T, Terracciano GJ, Magder L, et al. The Guillain-Barré syndrome and the 1992–1993 and 1993–1994 influenza vaccines. N Engl J Med. 1998;339(25):1797–1802. doi: 10.1056/NEJM199812173392501.
    1. Haber P, DeStefano F, Angulo FJ, et al. Guillain-Barré syndrome following influenza vaccination. JAMA. 2004;292(20):2478–2481. doi: 10.1001/jama.292.20.2478.
    1. Juurlink DN, Stukel TA, Kwong J, et al. Guillain-Barré syndrome after influenza vaccination in adults: a population-based study. Arch Intern Med. 2006;166(20):2217–2221. doi: 10.1001/archinte.166.20.2217.
    1. Stowe J, Andrews N, Wise L, et al. Investigation of the temporal association of Guillain-Barré syndrome with influenza vaccine and influenzalike illness using the United Kingdom general practice research database. Am J Epidemiol. 2009;169(3):382–388. doi: 10.1093/aje/kwn310.
    1. Burwen DR, Ball R, Bryan WW, et al. Evaluation of Guillain-Barré syndrome among recipients of influenza vaccine in 2000 and 2001. Am J Prev Med. 2010;39(4):296–304. doi: 10.1016/j.amepre.2010.05.022.
    1. Sejvar JJ, Pfeifer D, Schonberger LB. Guillain-Barré syndrome following influenza vaccination: causal or coincidental? Curr Infect Dis Rep. 2011;13(4):387–398. doi: 10.1007/s11908-011-0194-8.
    1. Nachamkin I, Shadomy SV, Moran AP, et al. Anti-ganglioside antibody induction by swine (A/NJ/1976/H1N1) and other influenza vaccines: insights into vaccine-associated Guillain-Barré syndrome. J Infect Dis. 2008;198(2):226–233. doi: 10.1086/589624.
    1. Italian National Institute of Statistics—ISTAT. (2011). Accessed 7 Aug 2012.
    1. The Brighton Collaboration. Automatic Brighton case classification Tool. ) (2011). Accessed 7 Aug 2012.
    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. doi: 10.1016/j.vaccine.2010.06.003.
    1. Whitaker HJ, Farrington CP, Spiessens B, et al. Tutorial in biostatistics: the self-controlled case series method. Stat Med. 2006;25(10):1768–1797. doi: 10.1002/sim.2302.
    1. Weldeselassie YG, Whitaker HJ, Farrington CP. Use of the self-controlled case-series method in vaccine safety studies: review and recommendations for best practice. Epidemiol Infect. 2011;139(12):1805–1817. doi: 10.1017/S0950268811001531.
    1. Farrington CP, Whitaker HJ, Hocine MN. Case series analysis for censored, perturbed, or curtailed post-event exposures. Biostatistics. 2009;10(1):3–16. doi: 10.1093/biostatistics/kxn013.
    1. R Development Core Team. R: a language and environment for statistical computing. Vienna, Austria. (2011).
    1. Kuhner R, Whitaker H. Package “adSCCS.” (2011). Accessed 7 Aug 2012.
    1. Efron B, Tibshirani R. An introduction to the bootstrap. Chapman & Hall: New York; 1993. p. 456.
    1. Italian Ministry of Health. Official data influenza vaccination coverage: season 2010–2011. (2011). Accessed 7 Aug 2012.
    1. Centers for Disease Control and Prevention (CDC). Preliminary results: surveillance for Guillain-Barré syndrome after receipt of influenza A (H1N1) 2009 monovalent vaccine—United States, 2009–2010. MMWR Morb Mortal Wkly Rep. 2010;59(21):657–661.
    1. Tokars JI, Lewis P, DeStefano F, et al. The risk of Guillain-Barré syndrome associated with influenza A (H1N1) 2009 monovalent vaccine and 2009–2010 seasonal influenza vaccines: results from self-controlled analyses. Pharmacoepidemiol Drug Saf. 2012;21(5):546–552. doi: 10.1002/pds.3220.
    1. Greene SK, Rett M, Weintraub ES, et al. Risk of confirmed Guillain-Barré syndrome following receipt of monovalent inactivated influenza A (H1N1) and seasonal influenza vaccines in the vaccine safety datalink project, 2009–2010. Am J Epidemiol. 2012;175(11):1100–1109. doi: 10.1093/aje/kws195.
    1. Wise ME, Viray M, Sejvar JJ, et al. Guillain-Barré syndrome during the 2009–2010 H1N1 influenza vaccination campaign: population-based surveillance among 45 million Americans. Am J Epidemiol. 2012;175(11):1110–1119. doi: 10.1093/aje/kws196.
    1. Yih WK, Lee GM, Lieu TA, et al. Surveillance for adverse events following receipt of pandemic 2009 H1N1 vaccine in the post-licensure rapid immunization safety monitoring (PRISM) system, 2009–2010. Am J Epidemiol. 2012;175(11):1120–1128. doi: 10.1093/aje/kws197.
    1. Dieleman J, Romio S, Johansen K, et al. Guillain-Barré syndrome adjuvanted pandemic influenza A (H1N1), vaccine: multinational case–control study in Europe. BMJ. 2009;2011:343.
    1. Grimaldi-Bensouda L, Alpérovitch A, Besson G, et al. Guillain-Barre syndrome, influenzalike illnesses, and influenza vaccination during seasons with and without circulating A/H1N1 viruses. Am J Epidemiol. 2011;174(3):326–335. doi: 10.1093/aje/kwr072.
    1. De Wals P, Deceuninck G, Toth E, et al. Risk of Guillain-Barré syndrome following H1N1 influenza vaccination in Quebec. JAMA. 2012;308(2):175–181. doi: 10.1001/jama.2012.7342.
    1. Rizzo C, Bella A, Viboud C, et al. Trends for influenza-related deaths during pandemic and epidemic seasons, Italy, 1969–2001. Emerging Infect Dis. 2007;13(5):694–699. doi: 10.3201/eid1305.061309.
    1. Lambert LC, Fauci AS. Influenza vaccines for the future. N Engl J Med. 2010;363(21):2036–2044. doi: 10.1056/NEJMra1002842.
    1. World Health Organization. Influenza vaccines. (2011). Accessed 7 Aug 2012.

Source: PubMed

Sponsorer och medarbetare

Medicinska tillstånd

Läkemedelsinterventioner

3
Prenumerera