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Abstract

Background

In the Netherlands, echovirus type 6 (E6) is identified through clinical and environmental enterovirus surveillance (CEVS and EEVS).

Aim

We aimed to identify E6 transmission clusters and to assess the role of EEVS in surveillance and early warning of E6.

Methods

We included all E6 strains from CEVS and EEVS from 2007 through 2016. CEVS samples were from patients with enterovirus illness. EEVS samples came from sewage water at pre-specified sampling points. E6 strains were defined by partial VP1 sequence, month and 4-digit postcode. Phylogenetic E6 clusters were detected using pairwise genetic distances. We identified transmission clusters using a combined pairwise distance in time, place and phylogeny dimensions.

Results

E6 was identified in 157 of 3,506 CEVS clinical episodes and 92 of 1,067 EEVS samples. Increased E6 circulation was observed in 2009 and from 2014 onwards. Eight phylogenetic clusters were identified; five included both CEVS and EEVS strains. Among these, identification in EEVS did not consistently precede CEVS. One phylogenetic cluster was dominant until 2014, but genetic diversity increased thereafter. Of 14 identified transmission clusters, six included both EEVS and CEVS; in two of them, EEVS identification preceded CEVS identification. Transmission clusters were consistent with phylogenetic clusters, and with previous outbreak reports.

Conclusion

Algorithms using combined time–place–phylogeny data allowed identification of clusters not detected by any of these variables alone. EEVS identified strains circulating in the population, but EEVS samples did not systematically precede clinical case surveillance, limiting EEVS usefulness for early warning in a context where E6 is endemic.

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/content/10.2807/1560-7917.ES.2018.23.45.1800288
2018-11-08
2018-11-19
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2018.23.45.1800288
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References

  1. Centers for Disease Control and Prevention (CDC). Non-polio enterovrius. Atlanta: CDC. [Accessed: 20 Mar 2018]. Available from: www.cdc.gov/non-polio-enterovirus/about/overview.html
  2. European Centre for Disease Prevention and Control (ECDC). Enterovirus detections associated with severe neurological symptoms in children and adults in European countries, 8 August 2016. Rapid risk assessment. Stockholm: ECDC; 2016. Available from: https://ecdc.europa.eu/en/publications-data/rapid-risk-assessment-enterovirus-detections-associated-severe-neurological
  3. European Centre for Disease Prevention and Control (ECDC). Outbreak of enterovirus A71 with severe neurological symptoms among children in Catalonia, Spain, 16 June 2016. Rapid risk assessment. Stockholm: ECDC; 2016. Available from: https://ecdc.europa.eu/en/publications-data/rapid-risk-assessment-outbreak-enterovirus-a71-severe-neurological-symptoms-among
  4. Grist NR, Bell EJ, Assaad F. Enteroviruses in human disease. Prog Med Virol. 1978;24:114-57. PMID: 360295 
  5. Khetsuriani N, Lamonte A, Oberste MS, Pallansch M. Neonatal enterovirus infections reported to the national enterovirus surveillance system in the United States, 1983-2003. Pediatr Infect Dis J. 2006;25(10):889-93.  https://doi.org/10.1097/01.inf.0000237798.07462.32  PMID: 17006282 
  6. de Ory F, Avellón A, Echevarría JE, Sánchez-Seco MP, Trallero G, Cabrerizo M, et al. Viral infections of the central nervous system in Spain: a prospective study. J Med Virol. 2013;85(3):554-62.  https://doi.org/10.1002/jmv.23470  PMID: 23239485 
  7. Lee HY, Chen CJ, Huang YC, Li WC, Chiu CH, Huang CG, et al. Clinical features of echovirus 6 and 9 infections in children. J Clin Virol. 2010;49(3):175-9.  https://doi.org/10.1016/j.jcv.2010.07.010  PMID: 20729140 
  8. Papa A, Skoura L, Dumaidi K, Spiliopoulou A, Antoniadis A, Frantzidou F. Molecular epidemiology of Echovirus 6 in Greece. Eur J Clin Microbiol Infect Dis. 2009;28(6):683-7.  https://doi.org/10.1007/s10096-008-0685-1  PMID: 19130106 
  9. van der Sanden SM, Koopmans MP, van der Avoort HG. Detection of human enteroviruses and parechoviruses as part of the national enterovirus surveillance in the Netherlands, 1996-2011. Eur J Clin Microbiol Infect Dis. 2013;32(12):1525-31.  https://doi.org/10.1007/s10096-013-1906-9  PMID: 23780695 
  10. Benschop KS, Geeraedts F, Beuvink B, Spit SA, Fanoy EB, Claas EC, et al. Increase in ECHOvirus 6 infections associated with neurological symptoms in the Netherlands, June to August 2016. Euro Surveill. 2016;21(39):30351.  https://doi.org/10.2807/1560-7917.ES.2016.21.39.30351  PMID: 27719751 
  11. Harvala H, Jasir A, Penttinen P, Pastore Celentano L, Greco D, Broberg E. Surveillance and laboratory detection for non-polio enteroviruses in the European Union/European Economic Area, 2016. Euro Surveill. 2017;22(45):16-00807.  https://doi.org/10.2807/1560-7917.ES.2017.22.45.16-00807  PMID: 29162204 
  12. Cabrerizo M, Trallero G, Echevarría JE, Moreno-Docón A, Pena MJ, Pérez-Ruiz M, et al. Molecular characterization of enteroviruses associated with neurological infections in Spain, 2008. J Med Virol. 2013;85(11):1975-7.  https://doi.org/10.1002/jmv.23693  PMID: 23893817 
  13. Harvala H, Calvert J, Van Nguyen D, Clasper L, Gadsby N, Molyneaux P, et al. Comparison of diagnostic clinical samples and environmental sampling for enterovirus and parechovirus surveillance in Scotland, 2010 to 2012. Euro Surveill. 2014;19(15):20772.  https://doi.org/10.2807/1560-7917.ES2014.19.15.20772  PMID: 24762664 
  14. Wang H, Tao Z, Li Y, Lin X, Yoshida H, Song L, et al. Environmental surveillance of human enteroviruses in Shandong Province, China, 2008 to 2012: serotypes, temporal fluctuation, and molecular epidemiology. Appl Environ Microbiol. 2014;80(15):4683-91.  https://doi.org/10.1128/AEM.00851-14  PMID: 24837389 
  15. Tao Z, Song Y, Wang H, Zhang Y, Yoshida H, Ji S, et al. Intercity spread of echovirus 6 in Shandong Province, China: application of environmental surveillance in tracing circulating enteroviruses. Appl Environ Microbiol. 2012;78(19):6946-53.  https://doi.org/10.1128/AEM.01861-12  PMID: 22843520 
  16. Abedi GR, Watson JT, Pham H, Nix WA, Oberste MS, Gerber SI. Enterovirus and human parechovirus surveillance - United States, 2009-2013. MMWR Morb Mortal Wkly Rep. 2015;64(34):940-3.  https://doi.org/10.15585/mmwr.mm6434a3  PMID: 26334674 
  17. Papadakis G, Chibo D, Druce J, Catton M, Birch C. Detection and genotyping of enteroviruses in cerebrospinal fluid in patients in Victoria, Australia, 2007-2013. J Med Virol. 2014;86(9):1609-13.  https://doi.org/10.1002/jmv.23885  PMID: 24474149 
  18. Thoelen I, Lemey P, Van Der Donck I, Beuselinck K, Lindberg AM, Van Ranst M. Molecular typing and epidemiology of enteroviruses identified from an outbreak of aseptic meningitis in Belgium during the summer of 2000. J Med Virol. 2003;70(3):420-9.  https://doi.org/10.1002/jmv.10412  PMID: 12767006 
  19. Luchs A, Russo DH, Cilli A, Costa FF, Morillo SG, Machado BC, et al. Echovirus 6 associated to aseptic meningitis outbreak, in São Joaquim da Barra, São Paulo, Brazil. Braz J Microbiol. 2008;39(1):28-31.  https://doi.org/10.1590/S1517-83822008000100007  PMID: 24031172 
  20. Siafakas N, Goudesidou M, Gaitana K, Gounaris A, Velegraki A, Pantelidi K, et al. Successful control of an echovirus 6 meningitis outbreak in a neonatal intensive care unit in central Greece. Am J Infect Control. 2013;41(11):1125-8.  https://doi.org/10.1016/j.ajic.2013.02.014  PMID: 23706831 
  21. Kim HJ, Kang B, Hwang S, Hong J, Kim K, Cheon DS. Epidemics of viral meningitis caused by echovirus 6 and 30 in Korea in 2008. Virol J. 2012;9(1):38.  https://doi.org/10.1186/1743-422X-9-38  PMID: 22336050 
  22. World Health Organization Regional Office for Europe (WHO Europe). Enterovirus surveillance guidelines: Guidelines for enterovirus surveillance in support of the Polio Eradication Initiative. Copenhagen: WHO Europe; 2015. Available from: http://www.euro.who.int/en/publications/abstracts/enterovirus-surveillance-guidelines.-guidelines-for-enterovirus-surveillance-in-support-of-the-polio-eradication-initiative
  23. Harvala H, Broberg E, Benschop K, Berginc N, Ladhani S, Susi P, et al. Recommendations for enterovirus diagnostics and characterisation within and beyond Europe. J Clin Virol. 2018;101:11-7.  https://doi.org/10.1016/j.jcv.2018.01.008  PMID: 29414181 
  24. Benschop KSM, van der Avoort HG, Jusic E, Vennema H, van Binnendijk R, Duizer E. Polio and measles down the drain: Environmental enterovirus surveillance in the Netherlands, 2005 to 2015. Appl Environ Microbiol. 2017;83(13):e00558-17.  https://doi.org/10.1128/AEM.00558-17  PMID: 28432101 
  25. Hovi T, Shulman LM, van der Avoort H, Deshpande J, Roivainen M, DE Gourville EM. Role of environmental poliovirus surveillance in global polio eradication and beyond. Epidemiol Infect. 2012;140(1):1-13.  https://doi.org/10.1017/S095026881000316X  PMID: 21849095 
  26. Bisseux M, Colombet J, Mirand A, Roque-Afonso AM, Abravanel F, Izopet J, et al. Monitoring human enteric viruses in wastewater and relevance to infections encountered in the clinical setting: a one-year experiment in central France, 2014 to 2015. Euro Surveill. 2018;23(7):17-00237. . Available from: http://dx.ddoi.org/10.2807/1560-7917.ES.2018.23.7.17-00237 https://doi.org/10.2807/1560-7917.ES.2018.23.7.17-00237  PMID: 29471623 
  27. Wieczorek M, Ciąćka A, Witek A, Kuryk Ł, Żuk-Wasek A. Environmental surveillance of non-polio enteroviruses in Poland, 2011. Food Environ Virol. 2015;7(3):224-31.  https://doi.org/10.1007/s12560-015-9195-3  PMID: 25862480 
  28. van der Avoort HG, Reimerink JH, Ras A, Mulders MN, van Loon AM. Isolation of epidemic poliovirus from sewage during the 1992-3 type 3 outbreak in The Netherlands. Epidemiol Infect. 1995;114(3):481-91.  https://doi.org/10.1017/S0950268800052195  PMID: 7781736 
  29. Savolainen-Kopra C, Paananen A, Blomqvist S, Klemola P, Simonen ML, Lappalainen M, et al. A large Finnish echovirus 30 outbreak was preceded by silent circulation of the same genotype. Virus Genes. 2011;42(1):28-36.  https://doi.org/10.1007/s11262-010-0536-x  PMID: 20960045 
  30. Kyriakopoulou Z, Dedepsidis E, Pliaka V, Tsakogiannis D, Ruether IG, Krikelis A, et al. Complete nucleotide sequence analysis of the VP1 genomic region of Echoviruses 6 isolated from sewage in Greece revealed 98% similarity with Echoviruses 6 that were characterized from an aseptic meningitis outbreak 1 year later. Clin Microbiol Infect. 2011;17(8):1170-3.  https://doi.org/10.1111/j.1469-0691.2010.03381.x  PMID: 21489045 
  31. Benschop KS, Rahamat-Langendoen JC, van der Avoort HG, Claas EC, Pas SD, Schuurman R, et al. VIRO-TypeNed, systematic molecular surveillance of enteroviruses in the Netherlands between 2010 and 2014. Euro Surveill. 2016;21(39):30352.  https://doi.org/10.2807/1560-7917.ES.2016.21.39.30352  PMID: 27719752 
  32. Ruijs WL, Hautvast JL, van der Velden K, de Vos S, Knippenberg H, Hulscher ME. Religious subgroups influencing vaccination coverage in the Dutch Bible belt: an ecological study. BMC Public Health. 2011;11(1):102.  https://doi.org/10.1186/1471-2458-11-102  PMID: 21320348 
  33. Duizer E, Rutjes S, de Roda Husman AM, Schijven J. Risk assessment, risk management and risk-based monitoring following a reported accidental release of poliovirus in Belgium, September to November 2014. Euro Surveill. 2016;21(11):30169.  https://doi.org/10.2807/1560-7917.ES.2016.21.11.30169  PMID: 27020766 
  34. Duizer E, Ruijs WL, van der Weijden CP, Timen A. Response to a wild poliovirus type 2 (WPV2)-shedding event following accidental exposure to WPV2, the Netherlands, April 2017. Euro Surveill. 2017;22(21):30542.  https://doi.org/10.2807/1560-7917.ES.2017.22.21.30542  PMID: 28597830 
  35. 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 
  36. Kroneman A, Vennema H, Deforche K, v d Avoort H, Peñaranda S, Oberste MS, et al. An automated genotyping tool for enteroviruses and noroviruses. J Clin Virol. 2011;51(2):121-5.  https://doi.org/10.1016/j.jcv.2011.03.006  PMID: 21514213 
  37. Benschop KS, de Vries M, Minnaar RP, Stanway G, van der Hoek L, Wolthers KC, et al. Comprehensive full-length sequence analyses of human parechoviruses: diversity and recombination. J Gen Virol. 2010;91(Pt 1):145-54.  https://doi.org/10.1099/vir.0.014670-0  PMID: 19759239 
  38. Ragonnet-Cronin M, Hodcroft E, Hué S, Fearnhill E, Delpech V, Brown AJ, et al. Automated analysis of phylogenetic clusters. BMC Bioinformatics. 2013;14(1):317.  https://doi.org/10.1186/1471-2105-14-317  PMID: 24191891 
  39. Ypma RJ, Donker T, van Ballegooijen WM, Wallinga J. Finding evidence for local transmission of contagious disease in molecular epidemiological datasets. PLoS One. 2013;8(7):e69875.  https://doi.org/10.1371/journal.pone.0069875  PMID: 23922835 
  40. Cabrerizo M, Trallero G, Simmonds P. Recombination and evolutionary dynamics of human echovirus 6. J Med Virol. 2014;86(5):857-64.  https://doi.org/10.1002/jmv.23741  PMID: 24114692 
  41. Wieczorek M, Krzysztoszek A, Ciąćka A, Figas A. Molecular characterization of environmental and clinical echovirus 6 isolates from Poland, 2006-2014. J Med Virol. 2017;89(5):936-40.  https://doi.org/10.1002/jmv.24709  PMID: 27736044 
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