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
Medina RA, García-Sastre A (2011) Influenza A viruses: new research developments. Nat Rev Microbiol 9:590–603
World Health Organization Influenza (seasonal) (2015) Fact sheet N 211. April 2009. http://www.who.int/mediacentre/factsheets/fs211/en. Accessed 23 Apr 2015
Nguyen-Van-Tam JS, Hampson AW (2003) The epidemiology and clinical impact of pandemic influenza. Vaccine 21:1762–1768
World Health Organization Influenza (seasonal) (2016) Fact sheet. March 2014. http://www.who.int/mediacentre/factsheets/fs211/en. Accessed 23 June 2016
Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y (1992) Evolution and ecology of influenza A viruses. Microbiol Rev 56:152–179
Wright PF, Webster RG (2001) Orthomyxoviruses. Fields Virol 1:1533–1579
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
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
Holmes EC (2010) Helping the resistance. Science 328:1243–1244
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
Bouvier NM, Palese P (2008) The biology of influenza viruses. Vaccine 26:D49–D53
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
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
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
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
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
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
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
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
Burke DF, Smith DJ (2014) A recommended numbering scheme for influenza A HA subtypes. PLoS One 9:e112302
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
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
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
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
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
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
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
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
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
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
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
World Health Organization (2015) Review of the 2014–2015 influenza season in the northern hemisphere. Wkly Epidemiol Rec 90:281–296
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
Ferguson NM, Galvani AP, Bush RM (2003) Ecological and immunological determinants of influenza evolution. Nature 422:428–433
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
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
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
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
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
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
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
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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