1887

Abstract

Besides the influenza virus (IV), several other viruses are responsible for influenza-like illness (ILI). Although human parechoviruses (HPeVs) and enteroviruses (EVs) may impact on ILI, limited data on their epidemiological characteristics are available. During seven consecutive winter seasons (from 2010–2011 to 2016–2017), within the framework of an influenza surveillance system (InfluNet), 593 respiratory swabs were collected from children ≤5 years of age with ILIs. Molecular detection showed that 58.3 % of swabs were positive for at least one of the viruses under study: 46 % for IV, 13 % for EV and 5.4 % for HPeV. A single virus was identified in 51.3 % of samples while more than one virus was detected in 7 % of the samples. The risk of contracting IV was higher than the risk associated with EV, which in turn was higher than the risk of contracting HPeV. The risk of developing an IV infection was twofold greater in children >3 years than in those ≤3 years, who had higher risk of EV/HPeV infection. The frequency of EV/HPeV-positive swabs increased significantly during the 2016–2017 winter season compared to the previous six seasons. Sixteen EV genotypes were identified belonging to species A and B. HPeV-1 was the most frequently detected genotype, followed by -6 and -3. In this study, IV was mainly responsible for ILI, however EV and HPeV were also involved and particularly affected children ≤3 years of age. Influenza surveillance samples could provide us with valuable insight into the epidemiological features of viruses involved in ILI.

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2017-11-07
2019-10-16
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References

  1. Liu L, Oza S, Hogan D, Perin J, Rudan I et al. Global, regional, and national causes of child mortality in 2000–13, with projections to inform post-2015 priorities: an updated systematic analysis. Lancet 2015; 385: 430– 440 [CrossRef] [PubMed]
    [Google Scholar]
  2. Turner D, Wailoo A, Nicholson K, Cooper N, Sutton A et al. Systematic review and economic decision modelling for the prevention and treatment of influenza A and B. Health Technol Assess 2003; 7: iiixi1– ivxiii170 [CrossRef] [PubMed]
    [Google Scholar]
  3. Nicoll A, Ciancio BC, Lopez Chavarrias V, Mølbak K, Pebody R et al. Influenza-related deaths-available methods for estimating numbers and detecting patterns for seasonal and pandemic influenza in Europe. Euro Surveill 2012; 17: [PubMed] [Crossref]
    [Google Scholar]
  4. Brottet E, Jaffar-Bandjee MC, Li-Pat-Yuen G, Filleul L. Etiology of influenza-like illnesses from sentinel network practitioners in réunion Island, 2011–2012. PLoS One 2016; 11: e0163377 [CrossRef] [PubMed]
    [Google Scholar]
  5. Kelly H, Birch C. The causes and diagnosis of influenza-like illness. Aust Fam Physician 2004; 33: 305– 309 [PubMed]
    [Google Scholar]
  6. Taylor S, Lopez P, Weckx L, Borja-Tabora C, Ulloa-Gutierrez R et al. Respiratory viruses and influenza-like illness: epidemiology and outcomes in children aged 6 months to 10 years in a multi-country population sample. J Infect 2017; 74: 29– 41 [CrossRef] [PubMed]
    [Google Scholar]
  7. Lekana-Douki SE, Nkoghe D, Drosten C, Ngoungou EB, Drexler JF et al. Viral etiology and seasonality of influenza-like illness in Gabon, March 2010 to June 2011. BMC Infect Dis 2014; 14: 373 [CrossRef] [PubMed]
    [Google Scholar]
  8. Ljubin-Sternak S, Marijan T, Ivković-Jureković I, Čepin-Bogović J, Gagro A et al. Etiology and clinical characteristics of single and multiple respiratory virus infections diagnosed in croatian children in two respiratory seasons. J Pathog 2016; 2016: 1– 8 [CrossRef] [PubMed]
    [Google Scholar]
  9. Harvala H, Robertson I, Mcwilliam Leitch EC, Benschop K, Wolthers KC et al. Epidemiology and clinical associations of human parechovirus respiratory infections. J Clin Microbiol 2008; 46: 3446– 3453 [CrossRef] [PubMed]
    [Google Scholar]
  10. Pallansch MA OM, Whitton JL. Enteroviruses: polioviruses, coxsackieviruses, echoviruses, and newer enteroviruses. In Knipe DM, Howley PM, Cohen JI, Griffen DG, Lamb RA. et al. (editors) Fields Virology, 6th ed.vol. 1 Philadelphia, PA: Lippincott Williams & Wilkins; 2013; pp. 490
    [Google Scholar]
  11. Dunn JJ. Enteroviruses and Parechoviruses. Microbiol Spectr 2016; 4: 273– 296 [CrossRef] [PubMed]
    [Google Scholar]
  12. Harvala H, Wolthers KC, Simmonds P. Parechoviruses in children: understanding a new infection. Curr Opin Infect Dis 2010; 23: 224– 230 [CrossRef] [PubMed]
    [Google Scholar]
  13. Rittichier KR, Bryan PA, Bassett KE, Taggart EW, Enriquez FR et al. Diagnosis and outcomes of enterovirus infections in young infants. Pediatr Infect Dis J 2005; 24: 546– 550 [CrossRef] [PubMed]
    [Google Scholar]
  14. Picornaviridae 2017; Parechovirus. www.picornaviridae.com/parechovirus/parechovirus.htm (Accessed 28-07-17)
  15. Xu Y, Sun Y, Ma J, Zhou S, Fang W et al. A novel Enterovirus 96 circulating in China causes hand, foot, and mouth disease. Virus Genes 2017; 53: 352– 356 [CrossRef] [PubMed]
    [Google Scholar]
  16. Piralla A, Daleno C, Scala A, Greenberg D, Usonis V CAP-PRI Study Group et al. Genome characterisation of enteroviruses 117 and 118: a new group within human enterovirus species C. PLoS One 2013; 8: e60641 [CrossRef] [PubMed]
    [Google Scholar]
  17. Sun G, Wang Y, Tao G, Shen Q, Cao W et al. Complete genome sequence of a novel type of human parechovirus strain reveals natural recombination events. J Virol 2012; 86: 8892– 8893 [CrossRef] [PubMed]
    [Google Scholar]
  18. Holm-Hansen CC, Midgley SE, Fischer TK. Global emergence of enterovirus D68: a systematic review. Lancet Infect Dis 2016; 16: e64 e75 [CrossRef] [PubMed]
    [Google Scholar]
  19. The Lancet Infectious Diseases Enterovirus D68: the unexpected guest. Lancet Infect Dis 2014; 14: 1023 [CrossRef] [PubMed]
    [Google Scholar]
  20. Fowlkes A, Giorgi A, Erdman D, Temte J, Goodin K IISP Working Group et al. Viruses associated with acute respiratory infections and influenza-like illness among outpatients from the Influenza Incidence surveillance project, 2010– 2011. J Infect Dis 2014; 209: 1715– 1725 [CrossRef] [PubMed]
    [Google Scholar]
  21. Druce J, Tran T, Kelly H, Kaye M, Chibo D et al. Laboratory diagnosis and surveillance of human respiratory viruses by PCR in Victoria, Australia, 2002-2003. J Med Virol 2005; 75: 122– 129 [CrossRef] [PubMed]
    [Google Scholar]
  22. Pierangeli A, Gentile M, di Marco P, Pagnotti P, Scagnolari C et al. Detection and typing by molecular techniques of respiratory viruses in children hospitalized for acute respiratory infection in Rome, Italy. J Med Virol 2007; 79: 463– 468 [CrossRef] [PubMed]
    [Google Scholar]
  23. Landes MB, Neil RB, Mccool SS, Mason BP, Woron AM et al. The frequency and seasonality of influenza and other respiratory viruses in Tennessee: two influenza seasons of surveillance data, 2010-2012. Influenza Other Respir Viruses 2013; 7: 1122– 1127 [CrossRef] [PubMed]
    [Google Scholar]
  24. Fu Y, Pan L, Sun Q, Zhu W, Zhu L et al. The clinical and etiological characteristics of influenza-like illness (ILI) in outpatients in Shanghai, China, 2011 to 2013. PLoS One 2015; 10: e0119513 [CrossRef] [PubMed]
    [Google Scholar]
  25. Piralla A, Mariani B, Rovida F, Baldanti F. Frequency of respiratory viruses among patients admitted to 26 Intensive Care Units in seven consecutive winter-spring seasons (2009-2016) in Northern Italy. J Clin Virol 2017; 92: 48– 51 [CrossRef] [PubMed]
    [Google Scholar]
  26. Wang W, Cavailler P, Ren P, Zhang J, Dong W et al. Molecular monitoring of causative viruses in child acute respiratory infection in endemo-epidemic situations in Shanghai. J Clin Virol 2010; 49: 211– 218 [CrossRef] [PubMed]
    [Google Scholar]
  27. WHO 2017; Recommended composition of influenza virus vaccines for use in the 2015-2016 northern hemisphere influenza season. www.who.int/influenza/vaccines/virus/recommendations/201502_recommendation.pdf (Accessed 28-07-17)
  28. Puenpa J, Mauleekoonphairoj J, Linsuwanon P, Suwannakarn K, Chieochansin T et al. Prevalence and characterization of enterovirus infections among pediatric patients with hand foot mouth disease, herpangina and influenza like illness in Thailand, 2012. PLoS One 2014; 9: e98888 [CrossRef] [PubMed]
    [Google Scholar]
  29. Nguyen DNT, Mai LQ, Bryant JE, Hang NLK, Hoa LNM et al. Epidemiology and etiology of influenza-like-illness in households in Vietnam; it's not all about the kids!. J Clin Virol 2016; 82: 126– 132 [CrossRef] [PubMed]
    [Google Scholar]
  30. Khetsuriani N, Lamonte-Fowlkes A, Oberst S, Pallansch MA. Centers for Disease Control and Prevention Enterovirus surveillance-United States, 1970–2005. MMWR Surveill Summ 2006; 55: 1– 20 [PubMed]
    [Google Scholar]
  31. Pallansch M, Roos R. Enteroviruses: polioviruses, coxsackieviruses, echoviruses, and newer enteroviruses. In Knipe DM, Howley PM. (editors) Fields' Virology, 5th ed. Philadelphia, PA 19106, USA: Lippincott Williams & Wilkins; 2007
    [Google Scholar]
  32. ECDC 2017; Rapid risk assessment. Enterovirus detections associated with severe neurological symptoms in children and adults in European countries. http://ecdc.europa.eu/en/publications/Publications/01-08-2016-RRA-Enterovirus%2071-Spain,%20France,%20Netherlands.pdf (Accessed 28-07-17)
  33. Centers for Disease Control and Prevention (CDC) Enterovirus surveillance-United States, 2002–2004. MMWR Morb Mortal Wkly Rep 2006; 55: 153– 156 [PubMed]
    [Google Scholar]
  34. Pariani E, Pellegrinelli L, Merlone ADC, Piralla A, Baldanti F et al. Letter to the editor: need for a European network for enterovirus D68 surveillance after detections of EV-D68 of the new B3 lineage in Sweden and Italy, 2016. Euro Surveill 2017; 22: pii: 30440 [CrossRef]
    [Google Scholar]
  35. Eurosurveillance Editorial Team A note from the editors: enterovirus D68 epidemiology in France and Germany-food for thought. 2016;21 pii=30229
  36. Sharp J, Bell J, Harrison CJ, Nix WA, Oberste MS et al. Human parechovirus in respiratory specimens from children in Kansas city, Missouri. J Clin Microbiol 2012; 50: 4111– 4113 [CrossRef] [PubMed]
    [Google Scholar]
  37. Harvala H, Robertson I, Chieochansin T, Mcwilliam Leitch EC, Templeton K et al. Specific association of human parechovirus type 3 with sepsis and fever in young infants, as identified by direct typing of cerebrospinal fluid samples. J Infect Dis 2009; 199: 1753– 1760 [CrossRef] [PubMed]
    [Google Scholar]
  38. Fischer TK, Midgley S, Dalgaard C, Nielsen AY. Human parechovirus infection, Denmark. Emerg Infect Dis 2014; 20: 83– 87 [CrossRef] [PubMed]
    [Google Scholar]
  39. Pariani E, Pellegrinelli L, Pugni L, Bini P, Perniciaro S et al. Two cases of neonatal human parechovirus 3 encephalitis. Pediatr Infect Dis J 2014; 33: 1191– 1193 [CrossRef] [PubMed]
    [Google Scholar]
  40. Ehrnst A, Eriksson M. Epidemiological features of type 22 echovirus infection. Scand J Infect Dis 1993; 25: 275– 281 [CrossRef] [PubMed]
    [Google Scholar]
  41. Chieochansin T, Vichiwattana P, Korkong S, Theamboonlers A, Poovorawan Y. Molecular epidemiology, genome characterization, and recombination event of human parechovirus. Virology 2011; 421: 159– 166 [CrossRef] [PubMed]
    [Google Scholar]
  42. Tregoning JS, Schwarze J. Respiratory viral infections in infants: causes, clinical symptoms, virology, and immunology. Clin Microbiol Rev 2010; 23: 74– 98 [CrossRef] [PubMed]
    [Google Scholar]
  43. Tang JW, Lam TT, Zaraket H, Lipkin WI, Drews SJ et al. Global epidemiology of non-influenza RNA respiratory viruses: data gaps and a growing need for surveillance. Lancet Infect Dis 2017; 17: e320 e326 [CrossRef]
    [Google Scholar]
  44. InfluNet 2017; InfluNet: sorveglianza epidemiologica. www.iss.it/flue/index.php?lang=1&id=159&tipo=11 (Accessed 28-07-17)
  45. Shephard DA. The 1975 Declaration of Helsinki and consent. Can Med Assoc J 1976; 115: 1191– 1192 [PubMed]
    [Google Scholar]
  46. WHO 2017; Global influenza surveillance network. Manual for the laboratory diagnosis and virological surveillance of influenza. http://whqlibdoc.who.int/publications/2011/9789241548090_eng.pdf (Accessed 28-07-17)
  47. CDC Guidance for clinicians on the use of rt-pcr and other molecular assays for diagnosis of influenza virus infection. https://www.cdc.gov/flu/professionals/diagnosis/molecular-assays.htm (Accessed 06-09-17)
  48. Bubba L, Pellegrinelli L, Pariani E, Primache V, Amendola A et al. A novel multiplex one-step real-time RT-PCR assay for the simultaneous identification of enterovirus and parechovirus in clinical fecal samples. J Prev Med Hyg 2015; 56: E57 60 [PubMed]
    [Google Scholar]
  49. Poelman R, Schuffenecker I, Van Leer-Buter C, Josset L, Niesters HG et al. European surveillance for enterovirus D68 during the emerging North-American outbreak in 2014. J Clin Virol 2015; 71: 1– 9 [CrossRef] [PubMed]
    [Google Scholar]
  50. Ellis JS, Alvarez-Aguero A, Gregory V, Lin YP, Hay A et al. Influenza AH1N2 viruses, United Kingdom, 2001-02 influenza season. Emerg Infect Dis 2003; 9: 304– 310 [CrossRef] [PubMed]
    [Google Scholar]
  51. Ellis JS, Chakraverty P, Clewley JP. Genetic and antigenic variation in the haemagglutinin of recently circulating human influenza A (H3N2) viruses in the United Kingdom. Arch Virol 1995; 140: 1889– 1904 [CrossRef] [PubMed]
    [Google Scholar]
  52. Ansaldi F, D'Agaro P, de Florentiis D, Puzelli S, Lin YP et al. Molecular characterization of influenza B viruses circulating in northern Italy during the 2001-2002 epidemic season. J Med Virol 2003; 70: 463– 469 [CrossRef] [PubMed]
    [Google Scholar]
  53. 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: 2698– 2704 [CrossRef] [PubMed]
    [Google Scholar]
  54. Hall T. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/ NT. Nucleic Acids Symp. Ser 1999; 95– 98
    [Google Scholar]
  55. Basic Local Alignment Search Tool 2017; BLAST. NCBI - NIH. https://blast.ncbi.nlm.nih.gov (Accessed 06-09-17)
  56. GenBank 2017; NCBI - NIH. https://www.ncbi.nlm.nih.gov/genbank/ (Accessed 28-07-17)
  57. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 2013; 30: 2725– 2729 [CrossRef] [PubMed]
    [Google Scholar]
  58. Dean Ag SK, Soe MM. 2003; Open source software for public health epidemiology. www.openepi.com (Accessed 28-07-17)
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