-
VIRO-TypeNed, systematic molecular surveillance of enteroviruses in the Netherlands between 2010 and 2014
- Kimberley S M Benschop1 , Janette C Rahamat-Langendoen2,3 , Harrie G A M van der Avoort1 , Eric C J Claas4 , Suzan D Pas5 , Rob Schuurman6 , Jaco J Verweij7 , Katja C Wolthers8 , Hubert G M Niesters2 , Marion P G Koopmans1,5 , on behalf of VIRO-TypeNed9
-
View Affiliations Hide AffiliationsAffiliations: 1 Center for Infectious Disease Control, National Institute for Public Health and the Environment, Bilthoven, the Netherlands 2 Department of Medical Microbiology, University Medical Center Groningen, Groningen, the Netherlands 3 Current address: Department of Medical Microbiology, Radboud University Medical Center, Nijmegen, the Netherlands 4 Department of Medical Microbiology, Leiden University Medical Center, Leiden, the Netherlands 5 Department of Viroscience, Erasmus Medical Center, Rotterdam, the Netherlands 6 Department of Virology, University Medical Center Utrecht, Utrecht, the Netherlands 7 Laboratory of Medical Microbiology and Immunology, St Elisabeth Hospital, Tilburg, the Netherlands 8 Department of Medical Microbiology, Academic Medical Center, Amsterdam, the Netherlands 9 http://www.rivm.nl/Onderwerpen/T/Type_Ned/Type_Ned_VirologieKimberley S.M. Benschopk.s.m.benschop gmail.com
-
View Citation Hide Citation
Citation style for this article: Benschop Kimberley S M, Rahamat-Langendoen Janette C, van der Avoort Harrie G A M, Claas Eric C J, Pas Suzan D, Schuurman Rob, Verweij Jaco J, Wolthers Katja C, Niesters Hubert G M, Koopmans Marion P G, on behalf of VIRO-TypeNed. VIRO-TypeNed, systematic molecular surveillance of enteroviruses in the Netherlands between 2010 and 2014. Euro Surveill. 2016;21(39):pii=30352. https://doi.org/10.2807/1560-7917.ES.2016.21.39.30352 Received: 22 Oct 2015; Accepted: 23 May 2016
Abstract
VIRO-TypeNed is a collaborative molecular surveillance platform facilitated through a web-based database. Genetic data in combination with epidemiological, clinical and patient data are shared between clinical and public health laboratories, as part of the surveillance underpinning poliovirus eradication. We analysed the combination of data submitted from 2010 to 2014 to understand circulation patterns of non-polio enteroviruses (NPEV) of public health relevance. Two epidemiological patterns were observed based on VIRO-TypeNed data and classical surveillance data dating back to 1996: (i) endemic cyclic, characterised by predictable upsurges/outbreaks every two to four years, and (ii) epidemic, where rare virus types caused upsurges/outbreaks. Genetic analysis suggests continuous temporal displacement of virus lineages due to the accumulation of (silent) genetic changes. Non-synonymous changes in the antigenic B/C loop suggest antigenic diversification, which may affect population susceptibility. Infections were frequently detected at an age under three months and at an older, parenting age (25–49 years) pointing to a distinct role of immunity in the circulation patterns. Upsurges were detected in the summer and winter which can promote increased transmissibility underlying new (cyclic) upsurges and requires close monitoring. The combination of data provide a better understanding of NPEV circulation required to control and curtail upsurges and outbreaks.
Article metrics loading...
Full text loading...
References
-
The picornavirus pages. Enterovirus. Pirbright; The Pirbright Institute. [Accessed: 14 Sep 2016]. Available from: http://www.picornaviridae.com/enterovirus/enterovirus.htm
-
Abzug MJ. Presentation, diagnosis, and management of enterovirus infections in neonates. Paediatr Drugs. 2004;6(1):1-10. https://doi.org/10.2165/00148581-200406010-00001 PMID: 14969566
-
Grist NR, Bell EJ, Assaad F. Enteroviruses in human disease. Prog Med Virol. 1978;24:114-57. PMID: 360295
-
Mohle-Boetani JC, Matkin C, Pallansch M, Helfand R, Fenstersheib M, Blanding JA, et al. Viral meningitis in child care center staff and parents: an outbreak of echovirus 30 infections. Public Health Rep. 1999;114(3):249-56. https://doi.org/10.1093/phr/114.3.249 PMID: 10476994
-
Hawkes MT, Vaudry W. Nonpolio enterovirus infection in the neonate and young infant. Paediatr Child Health. 2005;10(7):383-8. PMID: 19668644
-
Fuchs I, Golan A, Borer A, Shemer-Avni Y, Dagan R, Greenberg D. Proactive approach to containment of enterovirus infection in the nursery. Clin Pediatr (Phila). 2013;52(7):639-44. https://doi.org/10.1177/0009922813484087 PMID: 23572447
-
Verma NA, Zheng XT, Harris MU, Cadichon SB, Melin-Aldana H, Khetsuriani N, et al. Outbreak of life-threatening coxsackievirus B1 myocarditis in neonates. Clin Infect Dis. 2009;49(5):759-63. https://doi.org/10.1086/605089 PMID: 19622042
-
Modlin JF. Fatal echovirus 11 disease in premature neonates. Pediatrics. 1980;66(5):775-80. PMID: 7432883
-
Gear JH, Measroch V. Coxsackievirus infections of the newborn. Prog Med Virol. 1973;15:42-62. PMID: 4572439
-
Freund MW, Kleinveld G, Krediet TG, van Loon AM, Verboon-Maciolek MA. Prognosis for neonates with enterovirus myocarditis. Arch Dis Child Fetal Neonatal Ed. 2010;95(3):F206-12. https://doi.org/10.1136/adc.2009.165183 PMID: 20444813
-
Kaplan MH, Klein SW, McPhee J, Harper RG. Group B coxsackievirus infections in infants younger than three months of age: a serious childhood illness. Rev Infect Dis. 1983;5(6):1019-32. https://doi.org/10.1093/clinids/5.6.1019 PMID: 6318288
-
Wildenbeest JG, van den Broek PJ, Benschop KS, Koen G, Wierenga PC, Vossen AC, et al. Pleconaril revisited: clinical course of chronic enteroviral meningoencephalitis after treatment correlates with in vitro susceptibility. Antivir Ther. 2012;17(3):459-66. https://doi.org/10.3851/IMP1936 PMID: 22293148
-
Benschop KS, van der Avoort HG, Duizer E, Koopmans MP. Antivirals against enteroviruses: a critical review from a public-health perspective. Antivir Ther. 2015;20(2):121-30. https://doi.org/10.3851/IMP2939 PMID: 25643052
-
Simmonds P, Welch J. Frequency and dynamics of recombination within different species of human enteroviruses. J Virol. 2006;80(1):483-93. https://doi.org/10.1128/JVI.80.1.483-493.2006 PMID: 16352572
-
Lukashev AN, Lashkevich VA, Ivanova OE, Koroleva GA, Hinkkanen AE, Ilonen J. Recombination in circulating enteroviruses. J Virol. 2003;77(19):10423-31. https://doi.org/10.1128/JVI.77.19.10423-10431.2003 PMID: 12970427
-
Lukashev AN. Role of recombination in evolution of enteroviruses. Rev Med Virol. 2005;15(3):157-67. https://doi.org/10.1002/rmv.457 PMID: 15578739
-
McWilliam Leitch EC, Cabrerizo M, Cardosa J, Harvala H, Ivanova OE, Kroes AC, et al. Evolutionary dynamics and temporal/geographical correlates of recombination in the human enterovirus echovirus types 9, 11, and 30. J Virol. 2010;84(18):9292-300. https://doi.org/10.1128/JVI.00783-10 PMID: 20610722
-
Savolainen C, Hovi T, Mulders MN. Molecular epidemiology of echovirus 30 in Europe: succession of dominant sublineages within a single major genotype. Arch Virol. 2001;146(3):521-37. https://doi.org/10.1007/s007050170160 PMID: 11338388
-
Harvala H, Kalimo H, Bergelson J, Stanway G, Hyypiä T. Tissue tropism of recombinant coxsackieviruses in an adult mouse model. J Gen Virol. 2005;86(Pt 7):1897-907. https://doi.org/10.1099/vir.0.80603-0 PMID: 15958668
-
Harvala H, Kalimo H, Dahllund L, Santti J, Hughes P, Hyypiä T, et al. Mapping of tissue tropism determinants in coxsackievirus genomes. J Gen Virol. 2002;83(Pt 7):1697-706. https://doi.org/10.1099/0022-1317-83-7-1697 PMID: 12075089
-
Harvala H, Kalimo H, Stanway G, Hyypiä T. Pathogenesis of coxsackievirus A9 in mice: role of the viral arginine-glycine-aspartic acid motif. J Gen Virol. 2003;84(Pt 9):2375-9. https://doi.org/10.1099/vir.0.19246-0 PMID: 12917458
-
Ooi MH, Wong SC, Lewthwaite P, Cardosa MJ, Solomon T. Clinical features, diagnosis, and management of enterovirus 71. Lancet Neurol. 2010;9(11):1097-105. https://doi.org/10.1016/S1474-4422(10)70209-X PMID: 20965438
-
Sun LM, Zheng HY, Zheng HZ, Guo X, He JF, Guan DW, et al. An enterovirus 71 epidemic in Guangdong Province of China, 2008: epidemiological, clinical, and virogenic manifestations. Jpn J Infect Dis. 2011;64(1):13-8. PMID: 21266750
-
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
-
Esposito S, Zampiero A, Ruggiero L, Madini B, Niesters H, Principi N. Enterovirus D68-associated community-acquired pneumonia in children living in Milan, Italy. J Clin Virol. 2015;68:94-6. https://doi.org/10.1016/j.jcv.2015.05.017 PMID: 26071345
-
Farrell JJ, Ikladios O, Wylie KM, O’Rourke LM, Lowery KS, Cromwell JS, et al. Enterovirus D68-associated acute respiratory distress syndrome in adult, United States, 2014. Emerg Infect Dis. 2015;21(5):914-6. https://doi.org/10.3201/eid2105.142033 PMID: 25897542
-
Lang M, Mirand A, Savy N, Henquell C, Maridet S, Perignon R, et al. Acute flaccid paralysis following enterovirus D68 associated pneumonia, France, 2014. Euro Surveill. 2014;19(44):20952. https://doi.org/10.2807/1560-7917.ES2014.19.44.20952 PMID: 25394254
-
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
-
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
-
Poelman R, Schuffenecker I, Van Leer-Buter C, Josset L, Niesters HG, Lina B, et al. 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
-
Janes VA, Minnaar R, Koen G, van Eijk H, Dijkman-de Haan K, Pajkrt D, et al. Presence of human non-polio enterovirus and parechovirus genotypes in an Amsterdam hospital in 2007 to 2011 compared to national and international published surveillance data: a comprehensive review. Euro Surveill. 2014;19(46):20964. https://doi.org/10.2807/1560-7917.ES2014.19.46.20964 PMID: 25425513
-
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
-
Niesters HG, Rossen JW, van der Avoort H, Baas D, Benschop K, Claas EC, et al. Laboratory-based surveillance in the molecular era: the TYPENED model, a joint data-sharing platform for clinical and public health laboratories. Euro Surveill. 2013;18(4):20387. PMID: 23369392
-
Benschop K, Molenkamp R, van der Ham A, Wolthers K, Beld M. Rapid detection of human parechoviruses in clinical samples by real-time PCR. J Clin Virol. 2008;41(2):69-74. https://doi.org/10.1016/j.jcv.2007.10.004 PMID: 18354819
-
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
-
Benschop K, Minnaar R, Koen G, van Eijk H, Dijkman K, Westerhuis B, et al. Detection of human enterovirus and human parechovirus (HPeV) genotypes from clinical stool samples: polymerase chain reaction and direct molecular typing, culture characteristics, and serotyping. Diagn Microbiol Infect Dis. 2010;68(2):166-73. https://doi.org/10.1016/j.diagmicrobio.2010.05.016 PMID: 20846590
-
Beld M, Minnaar R, Weel J, Sol C, Damen M, van der Avoort H, et al. Highly sensitive assay for detection of enterovirus in clinical specimens by reverse transcription-PCR with an armored RNA internal control. J Clin Microbiol. 2004;42(7):3059-64. https://doi.org/10.1128/JCM.42.7.3059-3064.2004 PMID: 15243060
-
Benschop K, Thomas X, Serpenti C, Molenkamp R, Wolthers K. High prevalence of human Parechovirus (HPeV) genotypes in the Amsterdam region and identification of specific HPeV variants by direct genotyping of stool samples. J Clin Microbiol. 2008;46(12):3965-70. https://doi.org/10.1128/JCM.01379-08 PMID: 18945833
-
Oberste MS, Maher K, Flemister MR, Marchetti G, Kilpatrick DR, Pallansch MA. Comparison of classic and molecular approaches for the identification of untypeable enteroviruses. J Clin Microbiol. 2000;38(3):1170-4. PMID: 10699015
-
Oberste MS, Maher K, Kilpatrick DR, Flemister MR, Brown BA, Pallansch MA. Typing of human enteroviruses by partial sequencing of VP1. J Clin Microbiol. 1999;37(5):1288-93. PMID: 10203472
-
Kroneman A, Vennema H, Deforche K, van der 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
-
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
-
Harvala H, McLeish N, Kondracka J, McIntyre CL, McWilliam Leitch EC, Templeton K, et al. Comparison of human parechovirus and enterovirus detection frequencies in cerebrospinal fluid samples collected over a 5-year period in edinburgh: HPeV type 3 identified as the most common picornavirus type. J Med Virol. 2011;83(5):889-96. https://doi.org/10.1002/jmv.22023 PMID: 21412796
-
Page GS, Mosser AG, Hogle JM, Filman DJ, Rueckert RR, Chow M. Three-dimensional structure of poliovirus serotype 1 neutralizing determinants. J Virol. 1988;62(5):1781-94. PMID: 2451757
-
Simmonds P. SSE: a nucleotide and amino acid sequence analysis platform. BMC Res Notes. 2012;5(1):50. https://doi.org/10.1186/1756-0500-5-50 PMID: 22264264
-
Kumar S, Tamura K, Nei M. MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform. 2004;5(2):150-63. https://doi.org/10.1093/bib/5.2.150 PMID: 15260895
-
Benschop KS, Williams CH, Wolthers KC, Stanway G, Simmonds P. Widespread recombination within human parechoviruses: analysis of temporal dynamics and constraints. J Gen Virol. 2008;89(Pt 4):1030-5. https://doi.org/10.1099/vir.0.83498-0 PMID: 18343846
-
McWilliam Leitch EC, Bendig J, Cabrerizo M, Cardosa J, Hyypiä T, Ivanova OE, et al. Transmission networks and population turnover of echovirus 30. J Virol. 2009;83(5):2109-18. https://doi.org/10.1128/JVI.02109-08 PMID: 19091869
-
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
-
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
-
Cordey S, Petty TJ, Schibler M, Martinez Y, Gerlach D, van Belle S, et al. Identification of site-specific adaptations conferring increased neural cell tropism during human enterovirus 71 infection. PLoS Pathog. 2012;8(7):e1002826. https://doi.org/10.1371/journal.ppat.1002826 PMID: 22910880
-
Baek K, Yeo S, Lee B, Park K, Song J, Yu J, et al. Epidemics of enterovirus infection in Chungnam Korea, 2008 and 2009. Virol J. 2011;8(1):297. https://doi.org/10.1186/1743-422X-8-297 PMID: 21668960
-
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
-
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
-
Ayscue P, Van Haren K, Sheriff H, Waubant E, Waldron P, Yagi S, et al. Acute flaccid paralysis with anterior myelitis - California, June 2012-June 2014. MMWR Morb Mortal Wkly Rep. 2014;63(40):903-6. PMID: 25299608
-
Khan F. Enterovirus D68: acute respiratory illness and the 2014 outbreak. Emerg Med Clin North Am. 2015;33(2):e19-32. https://doi.org/10.1016/j.emc.2014.12.011 PMID: 26065305
-
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
-
Nougairede A, Bessaud M, Thiberville SD, Piorkowski G, Ninove L, Zandotti C, et al. Widespread circulation of a new echovirus 30 variant causing aseptic meningitis and non-specific viral illness, South-East France, 2013. J Clin Virol. 2014;61(1):118-24. https://doi.org/10.1016/j.jcv.2014.05.022 PMID: 24973284
-
Milia MG, Cerutti F, Gregori G, Burdino E, Allice T, Ruggiero T, et al. Recent outbreak of aseptic meningitis in Italy due to Echovirus 30 and phylogenetic relationship with other European circulating strains. J Clin Virol. 2013;58(3):579-83. https://doi.org/10.1016/j.jcv.2013.08.023 PMID: 24051044
-
Ramirez-Fort MK, Downing C, Doan HQ, Benoist F, Oberste MS, Khan F, et al. Coxsackievirus A6 associated hand, foot and mouth disease in adults: clinical presentation and review of the literature. J Clin Virol. 2014;60(4):381-6. https://doi.org/10.1016/j.jcv.2014.04.023 PMID: 24932735
-
Rabenau HF, Richter M, Doerr HW. Hand, foot and mouth disease: seroprevalence of Coxsackie A16 and Enterovirus 71 in Germany. Med Microbiol Immunol (Berl). 2010;199(1):45-51. https://doi.org/10.1007/s00430-009-0133-6 PMID: 19941005
-
McPhee F, Zell R, Reimann BY, Hofschneider PH, Kandolf R. Characterization of the N-terminal part of the neutralizing antigenic site I of coxsackievirus B4 by mutation analysis of antigen chimeras. Virus Res. 1994;34(2):139-51. https://doi.org/10.1016/0168-1702(94)90096-5 PMID: 7531922
-
Westerhuis BM, Koen G, Wildenbeest JG, Pajkrt D, de Jong MD, Benschop KS, et al. Specific cell tropism and neutralization of human parechovirus types 1 and 3: implications for pathogenesis and therapy development. J Gen Virol. 2012;93(Pt 11):2363-70. https://doi.org/10.1099/vir.0.043323-0 PMID: 22837420
-
Yarmolskaya MS, Shumilina EY, Ivanova OE, Drexler JF, Lukashev AN. Molecular epidemiology of echoviruses 11 and 30 in Russia: different properties of genotypes within an enterovirus serotype. Infect Genet Evol. 2015;30:244-8. https://doi.org/10.1016/j.meegid.2014.12.033 PMID: 25562123
-
Moeller JL. Aseptic meningitis: a seasonal concern. Phys Sportsmed. 1997;25(7):34-42. https://doi.org/10.3810/psm.1997.07.1472 PMID: 20086919
-
David JM, Ravel A, Nesbitt A, Pintar K, Pollari F. Assessing multiple foodborne, waterborne and environmental exposures of healthy people to potential enteric pathogen sources: effect of age, gender, season, and recall period. Epidemiol Infect. 2014;142(1):28-39. PMID: 23731678
-
Pallansch MA, Oberste MS. Enterovirus 71 encephalitis: a new vaccine on the horizon? Lancet. 2013;381(9871):976-7. https://doi.org/10.1016/S0140-6736(13)60286-X PMID: 23668563
-
Oberste MS, Moore D, Anderson B, Pallansch MA, Pevear DC, Collett MS. In vitro antiviral activity of V-073 against polioviruses. Antimicrob Agents Chemother. 2009;53(10):4501-3. https://doi.org/10.1128/AAC.00671-09 PMID: 19635956
-
Thibaut HJ, De Palma AM, Neyts J. Combating enterovirus replication: state-of-the-art on antiviral research. Biochem Pharmacol. 2012;83(2):185-92. https://doi.org/10.1016/j.bcp.2011.08.016 PMID: 21889497
Data & Media loading...