1887
  1. Home
  2. Eurosurveillance
  3. Volume 24, Issue 35, 29/Aug/2019
  4. Article
Research Open Access
Like 0
Download

Abstract

Background

Enterovirus D68 (EV-D68) has caused major outbreaks of severe respiratory illness worldwide since 2010.

Aim

Our aim was to evaluate EV-D68 circulation in the Netherlands by conducting a serosurvey of EV-D68 neutralising antibodies (nAb) among the Dutch general population.

Methods

We screened 280 sera from children and adults in the Netherlands and used two independent sets of samples collected in the years 2006 and 2007 and in the years 2015 and 2016, time points before and after the first EV-D68 upsurge in 2010. Neutralisation capacity of the sera was tested against the prototype Fermon EV-D68 strain isolated in 1962 and against a recent EV-D68 strain (genotype B3) isolated in France in 2016.

Results

Regardless of the time of serum collection, we found remarkably high overall seropositivity (94.3–98.3%) for nAb against both EV-D68 strains. Geometric mean titres increased in an age-dependent manner.

Conclusions

Our data suggest that EV-D68 has been circulating in the Netherlands for decades and that the enterovirus surveillance does not accurately capture the prevalence of this clinically relevant pathogen.

© Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.
Loading

Article metrics loading...

/content/10.2807/1560-7917.ES.2019.24.35.1800671
2019-08-29
2024-11-24
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2019.24.35.1800671
Loading
Loading full text...

Full text loading...

/deliver/fulltext/eurosurveillance/24/35/eurosurv-24-35-3.html?itemId=/content/10.2807/1560-7917.ES.2019.24.35.1800671&mimeType=html&fmt=ahah

References

  1. Holm-Hansen CC, Midgley SE, Fischer TK. Global emergence of enterovirus D68: a systematic review. Lancet Infect Dis. 2016;16(5):e64-75.  https://doi.org/10.1016/S1473-3099(15)00543-5  PMID: 26929196 
  2. Messacar K, Abzug MJ, Dominguez SR. The emergence of enterovirus-D68. Microbiol Spectr. 2016;4(3). PMID: 27337448 
  3. Tokarz R, Firth C, Madhi SA, Howie SR, 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. Meijer A, van der Sanden S, Snijders BE, 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 
  5. Rahamat-Langendoen J, Riezebos-Brilman A, Borger R, van der Heide R, Brandenburg A, Schölvinck E, et al. Upsurge of human enterovirus 68 infections in patients with severe respiratory tract infections. J Clin Virol. 2011;52(2):103-6.  https://doi.org/10.1016/j.jcv.2011.06.019  PMID: 21802981 
  6. Oberste MS, Maher K, Schnurr D, Flemister MR, Lovchik JC, Peters H, et al. Enterovirus 68 is associated with respiratory illness and shares biological features with both the enteroviruses and the rhinoviruses. J Gen Virol. 2004;85(Pt 9):2577-84.  https://doi.org/10.1099/vir.0.79925-0  PMID: 15302951 
  7. Sejvar JJ, Lopez AS, Cortese MM, Leshem E, Pastula DM, Miller L, et al. Acute flaccid myelitis in the United States, August-December 2014: results of nationwide surveillance. Clin Infect Dis. 2016;63(6):737-45.  https://doi.org/10.1093/cid/ciw372  PMID: 27318332 
  8. 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 
  9. 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 
  10. Dyda A, Stelzer-Braid S, Adam D, Chughtai AA, MacIntyre CR. The association between acute flaccid myelitis (AFM) and Enterovirus D68 (EV-D68) - what is the evidence for causation? Euro Surveill. 2018;23(3):17-00310.  https://doi.org/10.2807/1560-7917.ES.2018.23.3.17-00310  PMID: 29386095 
  11. Cabrerizo M, García-Iñiguez JP, Munell F, Amado A, Madurga-Revilla P, Rodrigo C, et al. First cases of severe flaccid paralysis associated with enterovirus D68 infection in Spain, 2015-2016. Pediatr Infect Dis J. 2017;36(12):1214-6.  https://doi.org/10.1097/INF.0000000000001668  PMID: 28661963 
  12. Pfeiffer HC, Bragstad K, Skram MK, Dahl H, Knudsen PK, Chawla MS, et al. Two cases of acute severe flaccid myelitis associated with enterovirus D68 infection in children, Norway, autumn 2014. Euro Surveill. 2015;20(10):21062.  https://doi.org/10.2807/1560-7917.ES2015.20.10.21062  PMID: 25788251 
  13. Knoester M, Schölvinck EH, Poelman R, Smit S, Vermont CL, Niesters HG, 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 
  14. 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 
  15. Poelman R, Schölvinck EH, Borger R, Niesters HG, van Leer-Buter C. The emergence of enterovirus D68 in a Dutch University Medical Center and the necessity for routinely screening for respiratory viruses. J Clin Virol. 2015;62:1-5.  https://doi.org/10.1016/j.jcv.2014.11.011  PMID: 25542461 
  16. 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 
  17. McAllister SC, Schleiss MR, Arbefeville S, Steiner ME, Hanson RS, Pollock C, et al. Epidemic 2014 enterovirus D68 cross-reacts with human rhinovirus on a respiratory molecular diagnostic platform. PLoS One. 2015;10(3):e0118529.  https://doi.org/10.1371/journal.pone.0118529  PMID: 25799541 
  18. Ehrenfeld E, Domingo E, Roos PR. The Picornaviruses. Washington, DC: ASM Press; 2010.
  19. 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 
  20. Xiang Z, Li L, Ren L, Guo L, Xie Z, Liu C, et al. Seroepidemiology of enterovirus D68 infection in China. Emerg Microbes Infect. 2017;6(5):e32.  https://doi.org/10.1038/emi.2017.14  PMID: 28487560 
  21. World Health Organization (WHO). Polio laboratory manual 2004. 4th edition. Geneva: WHO; 2004. Available from: https://apps.who.int/iris/bitstream/handle/10665/68762/WHO_IVB_04.10.pdf?sequence=1&isAllowed=y
  22. Reed LJ, Muench H. A simple method of estimating fifty percent endpoints. Am J Hyg. 1938;27:493-7.
  23. Mollema L, de Melker HE, Hahné SJM, van Weert JWM, Berbers GAM, van der Klis FRM. PIENTER 2-project: second research project on the protection against infectious diseases offered by the national immunization programme in the Netherlands. Bilthoven: National Institute for Public Health and the Environment; 2010. Available from: https://www.rivm.nl/publicaties/pienter-2-project-second-research-project-on-protection-against-infectious-diseases
  24. Karelehto E, van der Sanden S, Geraets JA, Domanska A, van der Linden L, Hoogendoorn D, et al. Strain-dependent neutralization reveals antigenic variation of human parechovirus 3. Sci Rep. 2017;7(1):12075.  https://doi.org/10.1038/s41598-017-12458-5  PMID: 28935894 
  25. van der Klis FR, Mollema L, Berbers GA, de Melker HE, Coutinho RA. Second national serum bank for population-based seroprevalence studies in the Netherlands. Neth J Med. 2009;67(7):301-8. PMID: 19687529 
  26. 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 
  27. Smura T, Ylipaasto P, Klemola P, Kaijalainen S, Kyllönen L, Sordi V, et al. Cellular tropism of human enterovirus D species serotypes EV-94, EV-70, and EV-68 in vitro: implications for pathogenesis. J Med Virol. 2010;82(11):1940-9.  https://doi.org/10.1002/jmv.21894  PMID: 20872722 
  28. Imamura T, Okamoto M, Nakakita S, Suzuki A, Saito M, Tamaki R, et al. Antigenic and receptor binding properties of enterovirus 68. J Virol. 2014;88(5):2374-84.  https://doi.org/10.1128/JVI.03070-13  PMID: 24371050 
  29. Zhang Y, Moore DD, Nix WA, Oberste MS, Weldon WC. Neutralization of Enterovirus D68 isolated from the 2014 US outbreak by commercial intravenous immune globulin products. J Clin Virol. 2015;69:172-5.  https://doi.org/10.1016/j.jcv.2015.06.086  PMID: 26209401 
  30. Pons-Salort M, Grassly NC. Serotype-specific immunity explains the incidence of diseases caused by human enteroviruses. Science. 2018;361(6404):800-3.  https://doi.org/10.1126/science.aat6777  PMID: 30139872 
Enterovirus D68 serosurvey: evidence for endemic circulation in the Netherlands, 2006 to 2016
<p class="citation"> <span>Citation style for this article:</span> <span class="meta-value authors"> <a href="/search?value1=Eveliina+Karelehto&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Karelehto Eveliina</a>, <a href="/search?value1=Gerrit+Koen&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Koen Gerrit</a>, <a href="/search?value1=Kimberley+Benschop&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Benschop Kimberley</a>, <a href="/search?value1=Fiona+van+der+Klis&option1=author&noRedirect=true" class="nonDisambigAuthorLink">van der Klis Fiona</a>, <a href="/search?value1=Dasja+Pajkrt&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Pajkrt Dasja</a>, <a href="/search?value1=Katja+Wolthers&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Wolthers Katja</a></span>. Enterovirus D68 serosurvey: evidence for endemic circulation in the Netherlands, 2006 to 2016. <a href="/content/ecdc">Euro Surveill.</a> 2019;24(35):pii=1800671. <a href="https://doi.org/10.2807/1560-7917.ES.2019.24.35.1800671" title="doi link" target="_blank">https://doi.org/10.2807/1560-7917.ES.2019.24.35.1800671</a> <span class="ES_Article_citation"> <span class="generated">Received</span>: 12 Dec 2018;&nbsp;&nbsp; <span class="generated">Accepted</span>: 05 Jun 2019 </span> </p>
/content/10.2807/1560-7917.ES.2019.24.35.1800671
/content/10.2807/1560-7917.ES.2019.24.35.1800671
Loading

Data & Media loading...

Supplementary data

Submit comment
Close
Comment moderation successfully completed
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error