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Abstract

Background

Understanding enterovirus D68 (EV-D68) circulation patterns as well as risk factors for severe respiratory and neurological illness is important for developing preventive strategies. : Between 2010 and 2016, 11,132 respiratory specimens from hospitalised patients in Lyon, France, were screened for EV-D68 by PCR. Phylogenetic relationships of the viral-protein-1 sequences were reconstructed using maximum-likelihood and Bayesian-Markov-Chain-Monte-Carlo approaches. Overall, 171 infections with a biennial pattern were detected, including seven, one, 55, none, 42, one and 65 cases annually during 2010–16. Children (< 16 years-old; n = 150) were mostly affected and 71% (n = 121) of the total patients were under 5 years-old. In 146 patients with medical reviews, 73% (n = 107) presented with acute respiratory distress. Among paediatric patients with medical reviews (n = 133), 55% (n=73) had an asthma/wheezing history, while among adults (n = 13), 11 had underlying diseases. In total, 45 patients had severe infections and 28 patients needed intensive care unit stays. No acute flaccid myelitis (AFM) was detected. We found genotypes A, B1, B2 B3 and D circulating, and no associations between these and clinical presentations. During the study, new genotypes continuously emerged, being replaced over time. We estimated that ancestors of currently circulating genotypes emerged in the late-1990s to 2010. Rises of the EV-D68 effective population size in Lyon coincided with infection upsurges. Phylogenetic analyses showed ongoing diversification of EV-D68 worldwide, coinciding with more infections in recent years and increases of reported AFM paediatric cases. Reinforcement of diagnostic capacities and clinical-based surveillance of EV-D68 infections is needed in Europe to assess the EV-D68 burden.

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2018-09-13
2024-12-23
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References

  1. Schieble JH, Fox VL, Lennette EH. A probable new human picornavirus associated with respiratory diseases. Am J Epidemiol. 1967;85(2):297-310.  https://doi.org/10.1093/oxfordjournals.aje.a120693  PMID: 4960233 
  2. Khetsuriani N, Lamonte-Fowlkes A, Oberst S, Pallansch MACenters for Disease Control and Prevention. Enterovirus surveillance--United States, 1970-2005. MMWR Surveill Summ. 2006;55(8):1-20. PMID: 16971890 
  3. Tokarz R, Firth C, Madhi SA, Howie SRC, Wu W, Sall AA, et al. Worldwide emergence of multiple clades of enterovirus 68. J Gen Virol. 2012;93(Pt 9):1952-8.  https://doi.org/10.1099/vir.0.043935-0  PMID: 22694903 
  4. Midgley CM, Jackson MA, Selvarangan R, Turabelidze G, Obringer E, Johnson D, et al. Severe respiratory illness associated with enterovirus D68 - Missouri and Illinois, 2014. MMWR Morb Mortal Wkly Rep. 2014;63(36):798-9. PMID: 25211545 
  5. Oermann CM, Schuster JE, Conners GP, Newland JG, Selvarangan R, Jackson MA. Enterovirus d68. A focused review and clinical highlights from the 2014 U.S. Outbreak. Ann Am Thorac Soc. 2015;12(5):775-81.  https://doi.org/10.1513/AnnalsATS.201412-592FR  PMID: 25714788 
  6. Aliabadi N, Messacar K, Pastula DM, Robinson CC, Leshem E, Sejvar JJ, et al. Enterovirus D68 Infection in Children with Acute Flaccid Myelitis, Colorado, USA, 2014. Emerg Infect Dis. 2016;22(8):1387-94.  https://doi.org/10.3201/eid2208.151949  PMID: 27434186 
  7. Midgley SE, Christiansen CB, Poulsen MW, Hansen CH, Fischer TK. Emergence of enterovirus D68 in Denmark, June 2014 to February 2015. Euro Surveill. 2015;20(17):21105.  https://doi.org/10.2807/1560-7917.ES2015.20.17.21105  PMID: 25955773 
  8. Antona D, Kossorotoff M, Schuffenecker I, Mirand A, Leruez-Ville M, Bassi C, et al. Severe paediatric conditions linked with EV-A71 and EV-D68, France, May to October 2016. Euro Surveill. 2016;21(46):30402.  https://doi.org/10.2807/1560-7917.ES.2016.21.46.30402  PMID: 27918268 
  9. Dyrdak R, Grabbe M, Hammas B, Ekwall J, Hansson KE, Luthander J, et al. Outbreak of enterovirus D68 of the new B3 lineage in Stockholm, Sweden, August to September 2016. Euro Surveill. 2016;21(46):30403.  https://doi.org/10.2807/1560-7917.ES.2016.21.46.30403  PMID: 27918255 
  10. Knoester M, Schölvinck EH, Poelman R, Smit S, Vermont CL, Niesters HGM, et al. Upsurge of Enterovirus D68, the Netherlands, 2016. Emerg Infect Dis. 2017;23(1):140-3.  https://doi.org/10.3201/eid2301.161313  PMID: 27660916 
  11. Bragstad K, Jakobsen K, Rojahn AE, Skram MK, Vainio K, Holberg-Petersen M, et al. High frequency of enterovirus D68 in children hospitalised with respiratory illness in Norway, autumn 2014. Influenza Other Respi Viruses. 2015;9(2):59-63.  https://doi.org/10.1111/irv.12300  PMID: 25534826 
  12. Schuffenecker I, Mirand A, Josset L, Henquell C, Hecquet D, Pilorgé L, et al. Epidemiological and clinical characteristics of patients infected with enterovirus D68, France, July to December 2014. Euro Surveill. 2016;21(19):30226.  https://doi.org/10.2807/1560-7917.ES.2016.21.19.30226  PMID: 27195770 
  13. Levy A, Roberts J, Lang J, Tempone S, Kesson A, Dofai A, et al. Enterovirus D68 disease and molecular epidemiology in Australia. J Clin Virol. 2015;69:117-21.  https://doi.org/10.1016/j.jcv.2015.06.079  PMID: 26209392 
  14. Huang Y-P, Lin T-L, Lin T-H, Wu H-S. Molecular and epidemiological study of enterovirus D68 in Taiwan. J Microbiol Immunol Infect. 2017;50(4):411-417. PMID: 26458357 
  15. Messacar K, Robinson CC, Pretty K, Yuan J, Dominguez SR. Surveillance for enterovirus D68 in colorado children reveals continued circulation. J Clin Virol. 2017;92:39-41.  https://doi.org/10.1016/j.jcv.2017.05.009  PMID: 28521212 
  16. Meijer A, Benschop KS, Donker GA, van der Avoort HG. Continued seasonal circulation of enterovirus D68 in the Netherlands, 2011-2014. Euro Surveill. 2014;19(42):20935.  https://doi.org/10.2807/1560-7917.ES2014.19.42.20935  PMID: 25358039 
  17. Poelman R, Schuffenecker I, Van Leer-Buter C, Josset L, Niesters HGM, Lina B. European surveillance for enterovirus D68 during the emerging North-American outbreak in 2014. J Clin Virol. 2015;71:1-9.  https://doi.org/10.1016/j.jcv.2015.07.296  PMID: 26364237 
  18. Nix WA, Oberste MS, Pallansch MA. Sensitive, seminested PCR amplification of VP1 sequences for direct identification of all enterovirus serotypes from original clinical specimens. J Clin Microbiol. 2006;44(8):2698-704.  https://doi.org/10.1128/JCM.00542-06  PMID: 16891480 
  19. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30(4):772-80.  https://doi.org/10.1093/molbev/mst010  PMID: 23329690 
  20. Darriba D, Taboada GL, Doallo R, Posada D. jModelTest 2: more models, new heuristics and parallel computing. Nat Methods. 2012;9(8):772.  https://doi.org/10.1038/nmeth.2109  PMID: 22847109 
  21. Guindon S, Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol. 2003;52(5):696-704.  https://doi.org/10.1080/10635150390235520  PMID: 14530136 
  22. Trifinopoulos J, Nguyen L-T, von Haeseler A, Minh BQ. W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Res. 2016;44(W1):W232-5.  https://doi.org/10.1093/nar/gkw256  PMID: 27084950 
  23. Rambaut A, Lam TT, Max Carvalho L, Pybus OG. Exploring the temporal structure of heterochronous sequences using TempEst (formerly Path-O-Gen). Virus Evol. 2016;2(1):vew007.  https://doi.org/10.1093/ve/vew007  PMID: 27774300 
  24. Drummond AJ, Suchard MA, Xie D, Rambaut A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol. 2012;29(8):1969-73.  https://doi.org/10.1093/molbev/mss075  PMID: 22367748 
  25. Bruen TC, Philippe H, Bryant D. A simple and robust statistical test for detecting the presence of recombination. Genetics. 2006;172(4):2665-81.  https://doi.org/10.1534/genetics.105.048975  PMID: 16489234 
  26. Gong Y-N, Yang S-L, Shih S-R, Huang Y-C, Chang P-Y, Huang C-G, et al. Molecular evolution and the global reemergence of enterovirus D68 by genome-wide analysis. Medicine (Baltimore). 2016;95(31):e4416.  https://doi.org/10.1097/MD.0000000000004416  PMID: 27495059 
  27. Meijer A, van der Sanden S, Snijders BEP, Jaramillo-Gutierrez G, Bont L, van der Ent CK, et al. Emergence and epidemic occurrence of enterovirus 68 respiratory infections in The Netherlands in 2010. Virology. 2012;423(1):49-57.  https://doi.org/10.1016/j.virol.2011.11.021  PMID: 22177700 
  28. Piralla A, Girello A, Grignani M, Gozalo-Margüello M, Marchi A, Marseglia G, et al. Phylogenetic characterization of enterovirus 68 strains in patients with respiratory syndromes in Italy. J Med Virol. 2014;86(9):1590-3.  https://doi.org/10.1002/jmv.23821  PMID: 24155220 
  29. NikNadia N, Sam IC, Rampal S, WanNorAmalina W, NurAtifah G, Verasahib K, et al. Cyclical Patterns of Hand, Foot and Mouth Disease Caused by Enterovirus A71 in Malaysia. PLoS Negl Trop Dis. 2016;10(3):e0004562.  https://doi.org/10.1371/journal.pntd.0004562  PMID: 27010319 
  30. Renois F, Bouin A, Andreoletti L. Enterovirus 68 in pediatric patients hospitalized for acute airway diseases. J Clin Microbiol. 2013;51(2):640-3.  https://doi.org/10.1128/JCM.02640-12  PMID: 23224095 
  31. Midgley CM, Watson JT, Nix WA, Curns AT, Rogers SL, Brown BA, et al. EV-D68 Working Group. Severe respiratory illness associated with a nationwide outbreak of enterovirus D68 in the USA (2014): a descriptive epidemiological investigation. Lancet Respir Med. 2015;3(11):879-87.  https://doi.org/10.1016/S2213-2600(15)00335-5  PMID: 26482320 
  32. Hixon AM, Yu G, Leser JS, Yagi S, Clarke P, Chiu CY, et al. A mouse model of paralytic myelitis caused by enterovirus D68. PLoS Pathog. 2017;13(2):e1006199.  https://doi.org/10.1371/journal.ppat.1006199  PMID: 28231269 
  33. Esposito S, Chidini G, Cinnante C, Napolitano L, Giannini A, Terranova L, et al. Acute flaccid myelitis associated with enterovirus-D68 infection in an otherwise healthy child. Virol J. 2017;14(1):4.  https://doi.org/10.1186/s12985-016-0678-0  PMID: 28081720 
  34. Rambaut A, Pybus OG, Nelson MI, Viboud C, Taubenberger JK, Holmes EC. The genomic and epidemiological dynamics of human influenza A virus. Nature. 2008;453(7195):615-9.  https://doi.org/10.1038/nature06945  PMID: 18418375 
  35. Tee KK, Lam TT-Y, Chan YF, Bible JM, Kamarulzaman A, Tong CYW, et al. Evolutionary genetics of human enterovirus 71: origin, population dynamics, natural selection, and seasonal periodicity of the VP1 gene. J Virol. 2010;84(7):3339-50.  https://doi.org/10.1128/JVI.01019-09  PMID: 20089660 
  36. Richter J, Tryfonos C, Christodoulou C. Circulation of enteroviruses in Cyprus assessed by molecular analysis of clinical specimens and sewage isolates. J Appl Microbiol. 2011;111(2):491-8.  https://doi.org/10.1111/j.1365-2672.2011.05061.x  PMID: 21615636 
  37. Zhang Y, Cao J, Zhang S, Lee AJ, Sun G, Larsen CN, et al. Genetic changes found in a distinct clade of Enterovirus D68 associated with paralysis during the 2014 outbreak. Virus Evol. 2016;2(1):vew015.  https://doi.org/10.1093/ve/vew015  PMID: 28512577 
Molecular diversity and biennial circulation of enterovirus D68: a systematic screening study in Lyon, France, 2010 to 2016
<p class="citation"> <span>Citation style for this article:</span> <span class="meta-value authors"> <a href="/search?value1=Rolf+Kramer&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Kramer Rolf</a>, <a href="/search?value1=Marina+Sabatier&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Sabatier Marina</a>, <a href="/search?value1=Thierry+Wirth&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Wirth Thierry</a>, <a href="/search?value1=Maxime+Pichon&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Pichon Maxime</a>, <a href="/search?value1=Bruno+Lina&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Lina Bruno</a>, <a href="/search?value1=Isabelle+Schuffenecker&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Schuffenecker Isabelle</a>, <a href="/search?value1=Laurence+Josset&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Josset Laurence</a></span>. Molecular diversity and biennial circulation of enterovirus D68: a systematic screening study in Lyon, France, 2010 to 2016. <a href="/content/ecdc">Euro Surveill.</a> 2018;23(37):pii=1700711. <a href="https://doi.org/10.2807/1560-7917.ES.2018.23.37.1700711" title="doi link" target="_blank">https://doi.org/10.2807/1560-7917.ES.2018.23.37.1700711</a> <span class="ES_Article_citation"> <span class="generated">Received</span>: 20 Oct 2017;&nbsp;&nbsp; <span class="generated">Accepted</span>: 06 May 2018 </span> </p>
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