Skip to main content

Advertisement

Log in

Detection of human enteroviruses and parechoviruses as part of the national enterovirus surveillance in the Netherlands, 1996–2011

  • Published:
European Journal of Clinical Microbiology & Infectious Diseases Aims and scope Submit manuscript

Abstract

Laboratories of the Dutch Working Group on Clinical Virology have routinely performed enterovirus diagnostics in the Netherlands since the early 1960s, with country-wide coverage. Enterovirus-positive samples are typed for clinical and epidemiological purposes, as well as to document the absence of poliovirus circulation. Human parechoviruses 1 and 2, initially recognized as enteroviruses, and since 2006 also the higher numbered human parechovirus types, have been detected as part of this surveillance. The purpose of this report is to describe the national enterovirus surveillance data from stool specimens collected in the Netherlands between 1996 and 2011 by all the participating laboratories. Since 2007, the average annual percentage of human enterovirus- and parechovirus-positive specimens increased from 6.5 to 10.8 % and from 0.3 to 2.5 % of the total numbers of specimens tested, respectively, following a gradual implementation of molecular diagnostics directly on clinical samples. Increased detection rates were observed for human enterovirus species A coxsackieviruses (from 0.1 to 0.5 %). Human enteroviruses of species B, C, and D were detected at average rates of 4.7, 0.04, and 0.005 %, respectively. The introduction of molecular diagnostics also resulted in an increase in the number of untyped enterovirus-positive specimens for which the presence of poliovirus was not excluded (from 1.3 to 3.1 % since 2007). To increase knowledge on human entero- and parechovirus epidemiology and type-specific pathogenesis, as well as to warrant the quality of the poliovirus surveillance in the Netherlands, it is of importance to continue the typing of enterovirus- and parechovirus-positive samples.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Hyypiä T, Hovi T, Knowles NJ, Stanway G (1997) Classification of enteroviruses based on molecular and biological properties. J Gen Virol 78(Pt 1):1–11

    PubMed  Google Scholar 

  2. Oberste MS, Maher K, Michele SM, Belliot G, Uddin M, Pallansch MA (2005) Enteroviruses 76, 89, 90 and 91 represent a novel group within the species Human enterovirus A. J Gen Virol 86(Pt 2):445–451

    Article  PubMed  CAS  Google Scholar 

  3. Oberste MS, Michele SM, Maher K, Schnurr D, Cisterna D, Junttila N, Uddin M, Chomel JJ, Lau CS, Ridha W, al-Busaidy S, Norder H, Magnius LO, Pallansch MA (2004) Molecular identification and characterization of two proposed new enterovirus serotypes, EV74 and EV75. J Gen Virol 85(Pt 11):3205–3212

    Article  PubMed  CAS  Google Scholar 

  4. Oberste MS, Maher K, Nix WA, Michele SM, Uddin M, Schnurr D, Al-Busaidy S, Akoua-Koffi C, Pallansch MA (2007) Molecular identification of 13 new enterovirus types, EV79-88, EV97, and EV100-101, members of the species Human Enterovirus B. Virus Res 128(1–2):34–42

    Article  PubMed  CAS  Google Scholar 

  5. van der Sanden S, de Bruin E, Vennema H, Swanink C, Koopmans M, van der Avoort H (2008) Prevalence of human parechovirus in the Netherlands in 2000 to 2007. J Clin Microbiol 46(9):2884–2889

    Article  PubMed  Google Scholar 

  6. Nix WA, Oberste MS, Pallansch MA (2006) Sensitive, seminested PCR amplification of VP1 sequences for direct identification of all enterovirus serotypes from original clinical specimens. J Clin Microbiol 44(8):2698–2704

    Article  PubMed  CAS  Google Scholar 

  7. Oberste MS, Maher K, Kilpatrick DR, Flemister MR, Brown BA, Pallansch MA (1999) Typing of human enteroviruses by partial sequencing of VP1. J Clin Microbiol 37(5):1288–1293

    PubMed  CAS  Google Scholar 

  8. Noordhoek GT, Weel JFL, Poelstra E, Hooghiemstra M, Brandenburg AH (2008) Clinical validation of a new real-time PCR assay for detection of enteroviruses and parechoviruses, and implications for diagnostic procedures. J Clin Virol 41(2):75–80. doi:10.1016/j.jcv.2007.09.011

    Article  PubMed  CAS  Google Scholar 

  9. Antona D, Lévêque N, Chomel JJ, Dubrou S, Lévy-Bruhl D, Lina B (2007) Surveillance of enteroviruses in France, 2000–2004. Eur J Clin Microbiol Infect Dis 26:403–412

    Article  PubMed  CAS  Google Scholar 

  10. Khetsuriani N, Lamonte-Fowlkes A, Oberst S, Pallansch MA; Centers for Disease Control and Prevention (2006) Enterovirus surveillance—United States, 1970–2005. MMWR Surveill Summ 55(8):1–20

    PubMed  Google Scholar 

  11. Witsø E, Palacios G, Cinek O, Stene LC, Grinde B, Janowitz D, Lipkin WI, Rønningen KS (2006) High prevalence of human enterovirus a infections in natural circulation of human enteroviruses. J Clin Microbiol 44(11):4095–4100

    Article  PubMed  Google Scholar 

  12. Tan DS, Lam SK (1978) Enterovirus survey before and after poliomyelitis vaccination in Kuala Lumpur, Malaysia. Southeast Asian J Trop Med Public Health 9(3):301–307

    PubMed  CAS  Google Scholar 

  13. Gamble DR (1962) Isolation of Coxsackie viruses from normal children aged 0–5 years. Br Med J 1(5270):16–18

    Article  PubMed  CAS  Google Scholar 

  14. Galbraith NS (1965) A survey of enteroviruses and adenoviruses in the faeces of normal children aged 0–4 years. A report of the Public Health Laboratory Service and the Society of Medical Officers of Health. J Hyg (Lond) 63(4):441–455

    Article  CAS  Google Scholar 

  15. Cole RM, Bell JA, Beeman EA, Huebner RJ (1951) Studies of Coxsackie viruses: observations on epidemiological aspects of Group A viruses. Am J Public Health Nations Health 41(11 Pt 1):1342–1358

    Article  PubMed  CAS  Google Scholar 

  16. Blomqvist S, Paananen A, Savolainen-Kopra C, Hovi T, Roivainen M (2008) Eight years of experience with molecular identification of human enteroviruses. J Clin Microbiol 46(7):2410–2413

    Article  PubMed  Google Scholar 

  17. Druyts-Voets E (1997) Epidemiological features of entero non-poliovirus isolations in Belgium 1980–94. Epidemiol Infect 119(1):71–77

    Article  PubMed  CAS  Google Scholar 

  18. Zaoutis T, Klein JD (1998) Enterovirus infections. Pediatr Rev 19(6):183–191

    Article  PubMed  CAS  Google Scholar 

  19. Yen FB, Chang LY, Kao CL, Lee PI, Chen CM, Lee CY, Shao PL, Wang SC, Lu CY, Huang LM (2009) Coxsackieviruses infection in northern Taiwan—epidemiology and clinical characteristics. J Microbiol Immunol Infect 42(1):38–46

    PubMed  Google Scholar 

  20. van der Sanden S, Koopmans M, Uslu G, van der Avoort H; Dutch Working Group for Clinical Virology (2009) Epidemiology of enterovirus 71 in the Netherlands, 1963 to 2008. J Clin Microbiol 47(9):2826–2833

    Article  PubMed  Google Scholar 

  21. van der Sanden S, van der Avoort H, Lemey P, Uslu G, Koopmans M (2010) Evolutionary trajectory of the VP1 gene of human enterovirus 71 genogroup B and C viruses. J Gen Virol 91:1949–1958

    Article  PubMed  Google Scholar 

  22. Meijer A, van der Sanden S, Snijders BE, Jaramillo-Gutierrez G, Bont L, van der Ent CK, Overduin P, Jenny SL, Jusic E, van der Avoort HG, Smith GJ, Donker GA, Koopmans MP (2012) Emergence and epidemic occurrence of enterovirus 68 respiratory infections in The Netherlands in 2010. Virology 423(1):49–57

    Article  PubMed  CAS  Google Scholar 

  23. McWilliam Leitch EC, Cabrerizo M, Cardosa J, Harvala H, Ivanova OE, Koike S, Kroes AC, Lukashev A, Perera D, Roivainen M, Susi P, Trallero G, Evans DJ, Simmonds P (2012) The association of recombination events in the founding and emergence of subgenogroup evolutionary lineages of human enterovirus 71. J Virol 86(5):2676–2685

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We want to thank all the virologists participating in the Weekly Sentinel Surveillance System of the Dutch Working Group for Clinical Virology for collecting and providing positive diagnostic results over the whole period of study. For participating in the enterovirus surveillance activities, we acknowledge the contribution of the laboratory staff of the RIVM (Gökhan Uslu, Ron Altena, and Edin Jusic). We want to thank Erwin Duizer and Kimberley Benschop for critically reading the manuscript.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to H. G. A. M. van der Avoort.

Rights and permissions

Reprints and permissions

About this article

Cite this article

van der Sanden, S.M.G., Koopmans, M.P.G. & van der Avoort, H.G.A.M. Detection of human enteroviruses and parechoviruses as part of the national enterovirus surveillance in the Netherlands, 1996–2011. Eur J Clin Microbiol Infect Dis 32, 1525–1531 (2013). https://doi.org/10.1007/s10096-013-1906-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10096-013-1906-9

Keywords

Navigation