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Molecular characterization and phylogenetic analysis of human influenza A viruses isolated in Iran during the 2014-2015 season

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Abstract

Influenza A viruses are an important cause of severe infectious diseases in humans and are characterized by their fast evolution rate. Global monitoring of these viruses is critical to detect newly emerging variants during annual epidemics. Here, we sought to genetically characterize influenza A/H1N1pdm09 and A/H3N2 viruses collected in Iran during the 2014–2015 influenza season. A total of 200 nasopharyngeal swabs were collected from patients with influenza-like illnesses. Swabs were screened for influenza A and B using real-time PCR. Furthermore, positive specimens with high virus load underwent virus isolation and genetic characterization of their hemagglutinin (HA) and M genes. Of the 200 specimens, 80 were influenza A-positive, including 44 A/H1N1pdm09 and 36 A/H3N2, while 18 were influenza B-positive. Phylogenetic analysis of the HA genes of the A/H1N1pdm09 viruses revealed the circulation of clade 6C, characterized by amino acid substitutions D97N, V234I and K283E. Analysis of the A/H3N2 viruses showed a genetic drift from the vaccine strain A/Texas/50/2012 with 5 mutations (T128A, R142G, N145S, P198S and S219F) belonging to the antigenic sites A, B, and D of the HA protein. The A/H3N2 viruses belonged to phylogenetic clades 3C.2 and 3C.3. The M gene trees of the Iranian A/H1N1pdm09 and A/H3N2 mirrored the clustering patterns of their corresponding HA trees. Our results reveal co-circulation of several influenza A virus strains in Iran during the 2014-2015 influenza season.

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References

  1. Medina RA, García-Sastre A (2011) Influenza A viruses: new research developments. Nat Rev Microbiol 9:590–603

    Article  CAS  PubMed  Google Scholar 

  2. World Health Organization Influenza (seasonal) (2015) Fact sheet N 211. April 2009. http://www.who.int/mediacentre/factsheets/fs211/en. Accessed 23 Apr 2015

  3. Nguyen-Van-Tam JS, Hampson AW (2003) The epidemiology and clinical impact of pandemic influenza. Vaccine 21:1762–1768

    Article  PubMed  Google Scholar 

  4. World Health Organization Influenza (seasonal) (2016) Fact sheet. March 2014. http://www.who.int/mediacentre/factsheets/fs211/en. Accessed 23 June 2016

  5. Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y (1992) Evolution and ecology of influenza A viruses. Microbiol Rev 56:152–179

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Wright PF, Webster RG (2001) Orthomyxoviruses. Fields Virol 1:1533–1579

    Google Scholar 

  7. Tong S, Zhu X, Li Y, Shi M, Zhang J, Bourgeois M, Yang H (2013) New world bats harbor diverse influenza A viruses. PLoS Pathog 9:e1003657

    Article  PubMed  PubMed Central  Google Scholar 

  8. Yoon S-W, Webby RJ, Webster RG (2014) Evolution and ecology of influenza A viruses. In: Influenza pathogenesis and control, vol I. Springer, New York, pp 359–375

  9. Holmes EC (2010) Helping the resistance. Science 328:1243–1244

    Article  CAS  PubMed  Google Scholar 

  10. Gu R, Liu LA, Wei D (2014) Drug inhibition and proton conduction mechanisms of the influenza A M2 proton channel. Adv Exp Med Biol 205–226

  11. Bouvier NM, Palese P (2008) The biology of influenza viruses. Vaccine 26:D49–D53

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Dong G, Peng C, Luo J, Wang C, Han L, Wu B, Ji G (2015) Adamantane-resistant influenza A viruses in the world (1902–2013): frequency and distribution of M2 gene mutations. PLoS One 10:e0119115

    Article  PubMed  PubMed Central  Google Scholar 

  13. Li W, Shi W, Qiao H, Ho SYW, Luo A, Zhang Y, Zhu C (2011) Positive selection on hemagglutinin and neuraminidase genes of H1N1 influenza viruses. Virol J. doi:10.1186/1743-422x-8-183

    Google Scholar 

  14. Hay AJ, Gregory V, Douglas AR, Lin YP (2001) The evolution of human influenza viruses. Philos Trans R Soc Lond B Biol Sci 356:1861–1870

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Mir MA, Lal RB, Sullender W, Singh Y, Garten R, Krishnan A, Broor S (2012) Genetic diversity of HA1 domain of hemagglutinin gene of pandemic influenza H1N1pdm09 viruses in New Delhi, India. J Med Virol 84:386–393

    Article  CAS  PubMed  Google Scholar 

  16. Scalera NM, Mossad SB (2009) The first pandemic of the 21st century: review of the 2009 pandemic variant influenza A (H1N1) virus. Postgrad Med 121:43–47

    Article  PubMed  Google Scholar 

  17. World Health Organization (2013) Global epidemiological surveillance standards for influenza. Edited by Influenza WHOWGESSf. World Health Organization, Geneva. http://www.who.int/influenza/resources/documents/WHO_Epidemiological_Influenza_Surveillance_Standards_2014.pdf

  18. Centers for Disease Control and Prevention (2009) CDC protocol of realtime RTPCR for influenza A (H1N1). http://www.who.int/csr/resources/publications/swineflu/CDCRealtimeRTPCR_SwineH1Assay-2009_20090430.pdf

  19. Han Y, Sun N, Lv Q-Y, Liu D-H, Liu D-P (2016) Molecular epidemiology and phylogenetic analysis of HA gene of influenza A (H1N1) pdm09 strain during 2010–2014 in Dalian, North China. Virus Genes 1–7

  20. Burke DF, Smith DJ (2014) A recommended numbering scheme for influenza A HA subtypes. PLoS One 9:e112302

    Article  PubMed  PubMed Central  Google Scholar 

  21. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evolut 30:2725–2729

    Article  CAS  Google Scholar 

  22. Nelson M, Spiro D, Wentworth D, Fan J, Beck E, George KS, Hine E et al (2009) The early diversification of influenza A/H1N1pdm. PLoS Curr Influenza

  23. European Centre for Disease Prevention and Control (ECDC) (2014) Influenza virus characterisation, summary Europe, November 2014. ECDC, Stockholm. http://www.ecdc.europa.eu/en/publications/Publications/ERLI-Net-report-November-2014.pdf

  24. European Centre for Disease Prevention and Control (2013) Influenza virus characterisation, summary Europe, December 2013. ECDC, Stockholm. http://ecdc.europa.eu/en/publications/publications/influenza-virus-characterisation-dec-2013.pdf

  25. Broberg E, Melidou A, Prosenc K, Bragstad K, Hungnes O (2016) Predominance of influenza A (H1N1) pdm09 virus genetic subclade 6B. 1 and influenza B/Victoria lineage viruses at the start of the 2015/16 influenza season in Europe. Eurosurveillance 21

  26. European Centre for Disease Prevention and Control (ECDC) (2012) Influenza virus characterization, summary Europe, March 2012. In: Technical document. Community network of reference laboratories for human influenza in Europe. http://ecdc.europa.eu/en/publications/Publications/1204-TED-CNRL-report.pdf. Accessed 7 Dec 2013

  27. European Centre for Disease Prevention and Control (ECDC) (2012) Influenza virus characterization, summary Europe, June 2012. In: Technical document. Community network of reference laboratories for human influenza in Europe. http://www.ecdc.europa.eu/en/publications/Publications/Influenza-visus-characterisation-June-2012.pdf Accessed 7 Dec 2013

  28. Broberg E, Snacken R, Adlhoch C, Beauté J, Galinska M, Pereyaslov D (2015) Start of the 2014/15 influenza season in Europe: drifted influenza A (H3N2) viruses circulate as dominant subtype. Eurosurveillance 20

  29. Cox N (2012) Seasonal influenza and zoonotic influenza. In: Information for the vaccine and related biological products advisory committee meeting. Silver Spring, Maryland, 28 Feb 2012

  30. Stucker K, Schobel S, Olsen R, Hodges H, Lin X, Halpin R, Das S et al (2015) Haemagglutinin mutations and glycosylation changes shaped the 2012/13 influenza A (H3N2) epidemic, Houston, Texas. Euro Surveill 20:21122

    Article  PubMed  Google Scholar 

  31. McCauley John DR, Lin YP, Zheng X (2015) Report prepared for the WHO annual consultation on the composition of influenza vaccine for the Southern Hemisphere. MRC National Institute for Medical Research, London

    Google Scholar 

  32. World Health Organization (2015) Review of the 2014–2015 influenza season in the northern hemisphere. Wkly Epidemiol Rec 90:281–296

    Google Scholar 

  33. Saito R, Akinobu H, Shaker R, Akel I, Assaf-Casals A, Lteif M, Odagiri T (2016) Characterization of influenza outbreaks in Lebanon during the 2013/14 and 2014/15 seasons. East Mediterr Health J 22:547

    CAS  PubMed  Google Scholar 

  34. Ferguson NM, Galvani AP, Bush RM (2003) Ecological and immunological determinants of influenza evolution. Nature 422:428–433

    Article  CAS  PubMed  Google Scholar 

  35. World Health Organization (2015) Recommended composition of influenza virus vaccines for use in the 2015–2016 northern hemisphere influenza season. Wkly Epidemiol Rec 90:97–108

    Google Scholar 

  36. Caton AJ, Brownlee GG, Yewdell JW, Gerhard W (1982) The antigenic structure of the influenza virus A/PR/8/34 hemagglutinin (H1 subtype). Cell 31:417–427

    Article  CAS  PubMed  Google Scholar 

  37. Sriwilaijaroen N, Suzuki Y (2012) Molecular basis of the structure and function of H1 hemagglutinin of influenza virus. Proc Jpn Acad Ser B 88:226–249

    Article  CAS  Google Scholar 

  38. Koel BF, Mögling R, Chutinimitkul S, Fraaij PL, Burke DF, van der Vliet S, Osterhaus AD et al (2015) Identification of amino acid substitutions supporting antigenic change of influenza A (H1N1) pdm09 viruses. J Virol 89:3763–3775

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Pan C, Cheung B, Tan S, Li C, Li L, Liu S, Jiang S (2010) Genomic signature and mutation trend analysis of pandemic (H1N1) 2009 influenza A virus. PLoS One 5:e9549

    Article  PubMed  PubMed Central  Google Scholar 

  40. Chambers BS, Parkhouse K, Ross TM, Alby K, Hensley SE (2015) Identification of hemagglutinin residues responsible for H3N2 antigenic drift during the 2014–2015 influenza season. Cell Rep 12:1–6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Webster R, Laver W (1980) Determination of the number of nonoverlapping antigenic areas on Hong Kong (H3N2) influenza virus hemagglutinin with monoclonal antibodies and the selection of variants with potential epidemiological significance. Virology 104:139–148

    Article  CAS  PubMed  Google Scholar 

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All authors contributed extensively to the work presented in this paper.

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Correspondence to Farida Behzadian.

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The authors declare that they have no conflict of interest.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the Pasteur’s institutional research committee of Iran and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

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Informed consent was obtained from all individual participants included in the study.

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Moasser, E., Behzadian, F., Moattari, A. et al. Molecular characterization and phylogenetic analysis of human influenza A viruses isolated in Iran during the 2014-2015 season. Arch Virol 162, 1975–1984 (2017). https://doi.org/10.1007/s00705-017-3323-3

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  • DOI: https://doi.org/10.1007/s00705-017-3323-3

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