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Erschienen in: Archives of Virology 5/2018

02.02.2018 | Original Article

Genetic characterization and diversity of circulating influenza A/H1N1pdm09 viruses isolated in Jeddah, Saudi Arabia between 2014 and 2015

verfasst von: Anwar M. Hashem, Esam I. Azhar, Sarah Shalhoub, Turki S. Abujamel, Norah A. Othman, Abdulwahab B. Al Zahrani, Hanan M. Abdullah, Maha M. Al-Alawi, Anees A. Sindi

Erschienen in: Archives of Virology | Ausgabe 5/2018

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Abstract

The emerged influenza A/H1N1pdm09 viruses have replaced the previously circulating seasonal H1N1 viruses. The close antigenic properties of these viruses to the 1918 H1N1 pandemic viruses and their post-pandemic evolution pattern could further enhance their adaptation and pathogenicity in humans representing a major public health threat. Given that data on the dynamics and evolution of these viruses in Saudi Arabia is sparse we investigated the genetic diversity of circulating influenza A/H1N1pdm09 viruses from Jeddah, Saudi Arabia, by analyzing 39 full genomes from isolates obtained between 2014-2015, from patients with varying symptoms. Phylogenetic analysis of all gene segments and concatenated genomes showed similar topologies and co-circulation of clades 6b, 6b.1 and 6b.2, with clade 6b.1 being the most predominate since 2015. Most viruses were more closely related to the vaccine strain (Michigan/45/2015) recommended for the 2017/2018 season, than to the California/07/2009 strain. Low sequence variability was observed in the haemagglutinin protein compared to the neuraminidase protein. Resistance to neuraminidase inhibitors was limited as only one isolate had the H275Y substitution. Interestingly, two isolates had short PA-X proteins of 206 amino acids compared to the 232 amino acid protein found in most influenza A/H1N1pdm09 viruses. Together, the co-circulation of several clades and the predominance of clade 6b.1, despite its low circulation in Asia in 2015, suggests multiple introductions most probably during the mass gathering events of Hajj and Umrah. Jeddah represents the main port of entry to the holy cities of Makkah and Al-Madinah, emphasizing the need for vigilant surveillance in the kingdom.
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Literatur
1.
Zurück zum Zitat Medina RA, García-Sastre A (2011) Influenza A viruses: new research developments. Nat Rev Microbiol 9:590–603CrossRefPubMed Medina RA, García-Sastre A (2011) Influenza A viruses: new research developments. Nat Rev Microbiol 9:590–603CrossRefPubMed
2.
Zurück zum Zitat Nguyen-Van-Tam JS, Hampson AW (2003) The epidemiology and clinical impact of pandemic influenza. Vaccine 21:1762–1768CrossRefPubMed Nguyen-Van-Tam JS, Hampson AW (2003) The epidemiology and clinical impact of pandemic influenza. Vaccine 21:1762–1768CrossRefPubMed
4.
Zurück zum Zitat Lui KJ, Kendal AP (1987) Impact of influenza epidemics on mortality in the United States from October 1972 to May 1985. Am J Public Health 77:712–716CrossRefPubMedPubMedCentral Lui KJ, Kendal AP (1987) Impact of influenza epidemics on mortality in the United States from October 1972 to May 1985. Am J Public Health 77:712–716CrossRefPubMedPubMedCentral
7.
Zurück zum Zitat Martinez O, Tsibane T, Basler CF (2009) Neutralizing anti-influenza virus monoclonal antibodies: therapeutics and tools for discovery. Int Rev Immunol 28:69–92CrossRefPubMed Martinez O, Tsibane T, Basler CF (2009) Neutralizing anti-influenza virus monoclonal antibodies: therapeutics and tools for discovery. Int Rev Immunol 28:69–92CrossRefPubMed
8.
Zurück zum Zitat Schäfer JR, Kawaoka Y, Bean WJ et al (1993) Origin of the pandemic 1957 H2 influenza A virus and the persistence of its possible progenitors in the avian reservoir. Virology 194:781–788CrossRefPubMed Schäfer JR, Kawaoka Y, Bean WJ et al (1993) Origin of the pandemic 1957 H2 influenza A virus and the persistence of its possible progenitors in the avian reservoir. Virology 194:781–788CrossRefPubMed
10.
Zurück zum Zitat Garten RJ, Davis CT, Russell CA et al (2009) Antigenic and genetic characteristics of swine-origin 2009 A(H1N1) influenza viruses circulating in humans. Science 325:197–201CrossRefPubMedPubMedCentral Garten RJ, Davis CT, Russell CA et al (2009) Antigenic and genetic characteristics of swine-origin 2009 A(H1N1) influenza viruses circulating in humans. Science 325:197–201CrossRefPubMedPubMedCentral
11.
12.
Zurück zum Zitat Miller MA, Viboud C, Balinska M et al (2009) The signature features of influenza pandemics—implications for policy. N Engl J Med 360:2595–2598CrossRefPubMed Miller MA, Viboud C, Balinska M et al (2009) The signature features of influenza pandemics—implications for policy. N Engl J Med 360:2595–2598CrossRefPubMed
13.
Zurück zum Zitat Smith GJ, Vijaykrishna D, Bahl J et al (2009) Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic. Nature 459:1122–1125CrossRefPubMed Smith GJ, Vijaykrishna D, Bahl J et al (2009) Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic. Nature 459:1122–1125CrossRefPubMed
14.
15.
Zurück zum Zitat Cutler J, Schleihauf E, Hatchette TF et al (2009) Investigation of the first cases of human-to-human infection with the new swine-origin influenza A (H1N1) virus in Canada. CMAJ 181:159–163CrossRefPubMedPubMedCentral Cutler J, Schleihauf E, Hatchette TF et al (2009) Investigation of the first cases of human-to-human infection with the new swine-origin influenza A (H1N1) virus in Canada. CMAJ 181:159–163CrossRefPubMedPubMedCentral
16.
Zurück zum Zitat Fisman DN, Savage R, Gubbay J et al (2009) Older age and a reduced likelihood of 2009 H1N1 virus infection. N Engl J Med 361:2000–2001CrossRefPubMed Fisman DN, Savage R, Gubbay J et al (2009) Older age and a reduced likelihood of 2009 H1N1 virus infection. N Engl J Med 361:2000–2001CrossRefPubMed
17.
Zurück zum Zitat Hancock K, Veguilla V, Lu X et al (2009) Cross-reactive antibody responses to the 2009 pandemic H1N1 influenza virus. N Engl J Med 361:1945–1952CrossRefPubMed Hancock K, Veguilla V, Lu X et al (2009) Cross-reactive antibody responses to the 2009 pandemic H1N1 influenza virus. N Engl J Med 361:1945–1952CrossRefPubMed
18.
Zurück zum Zitat Dorigatti I, Cauchemez S, Ferguson NM (2013) Increased transmissibility explains the third wave of infection by the 2009 H1N1 pandemic virus in England. Proc Natl Acad Sci USA 110:13422–13427CrossRefPubMedPubMedCentral Dorigatti I, Cauchemez S, Ferguson NM (2013) Increased transmissibility explains the third wave of infection by the 2009 H1N1 pandemic virus in England. Proc Natl Acad Sci USA 110:13422–13427CrossRefPubMedPubMedCentral
19.
Zurück zum Zitat Otte A, Sauter M, Daxer MA et al (2015) Adaptive mutations that occurred during circulation in humans of H1N1 influenza virus in the 2009 pandemic enhance virulence in mice. J Virol 89:7329–7337CrossRefPubMedPubMedCentral Otte A, Sauter M, Daxer MA et al (2015) Adaptive mutations that occurred during circulation in humans of H1N1 influenza virus in the 2009 pandemic enhance virulence in mice. J Virol 89:7329–7337CrossRefPubMedPubMedCentral
20.
Zurück zum Zitat Dong G, Peng C, Luo J et al (2015) Adamantane-resistant influenza A viruses in the world (1902–2013): frequency and distribution of M2 gene mutations. PLoS One 10:e0119115CrossRefPubMedPubMedCentral Dong G, Peng C, Luo J et al (2015) Adamantane-resistant influenza A viruses in the world (1902–2013): frequency and distribution of M2 gene mutations. PLoS One 10:e0119115CrossRefPubMedPubMedCentral
21.
Zurück zum Zitat Cobbin JCA, Alfelali M, Barasheed O et al (2017) Multiple sources of genetic diversity of influenza A viruses during the Hajj. J Virol 91:e00096-17CrossRefPubMedPubMedCentral Cobbin JCA, Alfelali M, Barasheed O et al (2017) Multiple sources of genetic diversity of influenza A viruses during the Hajj. J Virol 91:e00096-17CrossRefPubMedPubMedCentral
22.
Zurück zum Zitat Benkouiten S, Charrel R, Belhouchat K et al (2014) Respiratory viruses and bacteria among pilgrims during the 2013 Hajj. Emerg Infect Dis 20:1821–1827CrossRefPubMedPubMedCentral Benkouiten S, Charrel R, Belhouchat K et al (2014) Respiratory viruses and bacteria among pilgrims during the 2013 Hajj. Emerg Infect Dis 20:1821–1827CrossRefPubMedPubMedCentral
23.
Zurück zum Zitat Memish ZA, Assiri A, Turkestani A et al (2015) Mass gathering and globalization of respiratory pathogens during the 2013 Hajj. Clin Microbiol Infect 21:571.e571–571.e578 Memish ZA, Assiri A, Turkestani A et al (2015) Mass gathering and globalization of respiratory pathogens during the 2013 Hajj. Clin Microbiol Infect 21:571.e571–571.e578
24.
Zurück zum Zitat Tolah AM, Azhar EI, Hashem AM (2016) Susceptibility of influenza viruses circulating in Western Saudi Arabia to neuraminidase inhibitors. Saudi Med J 37:461–465CrossRefPubMedPubMedCentral Tolah AM, Azhar EI, Hashem AM (2016) Susceptibility of influenza viruses circulating in Western Saudi Arabia to neuraminidase inhibitors. Saudi Med J 37:461–465CrossRefPubMedPubMedCentral
26.
Zurück zum Zitat Al-Saeed MS, El-Kafrawy SA, Farraj SA et al (2017) Phylogenetic characterization of circulating Dengue and Alkhumra Hemorrhagic Fever viruses in western Saudi Arabia and lack of evidence of Zika virus in the region: a retrospective study, 2010–2015. J Med Virol 89:1339–1346CrossRefPubMed Al-Saeed MS, El-Kafrawy SA, Farraj SA et al (2017) Phylogenetic characterization of circulating Dengue and Alkhumra Hemorrhagic Fever viruses in western Saudi Arabia and lack of evidence of Zika virus in the region: a retrospective study, 2010–2015. J Med Virol 89:1339–1346CrossRefPubMed
28.
Zurück zum Zitat Kearse M, Moir R, Wilson A et al (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649CrossRefPubMedPubMedCentral Kearse M, Moir R, Wilson A et al (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649CrossRefPubMedPubMedCentral
29.
30.
Zurück zum Zitat Tamura K (1992) Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G + C-content biases. Mol Biol Evol 9:678–687PubMed Tamura K (1992) Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G + C-content biases. Mol Biol Evol 9:678–687PubMed
31.
Zurück zum Zitat Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120CrossRefPubMed Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120CrossRefPubMed
32.
Zurück zum Zitat Hasegawa M, Kishino H, Yano T (1985) Dating the human-ape split by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174CrossRefPubMed Hasegawa M, Kishino H, Yano T (1985) Dating the human-ape split by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174CrossRefPubMed
33.
Zurück zum Zitat Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York
34.
Zurück zum Zitat Houng HS, Garner J, Zhou Y et al (2012) Emergent 2009 influenza A(H1N1) viruses containing HA D222N mutation associated with severe clinical outcomes in the Americas. J Clin Virol 53:12–15CrossRefPubMed Houng HS, Garner J, Zhou Y et al (2012) Emergent 2009 influenza A(H1N1) viruses containing HA D222N mutation associated with severe clinical outcomes in the Americas. J Clin Virol 53:12–15CrossRefPubMed
35.
Zurück zum Zitat Nguyen HK, Nguyen PT, Nguyen TC et al (2015) Virological characterization of influenza H1N1pdm09 in Vietnam, 2010–2013. Influenza Other Respir Viruses 9:216–224CrossRefPubMedPubMedCentral Nguyen HK, Nguyen PT, Nguyen TC et al (2015) Virological characterization of influenza H1N1pdm09 in Vietnam, 2010–2013. Influenza Other Respir Viruses 9:216–224CrossRefPubMedPubMedCentral
36.
Zurück zum Zitat Parida M, Dash PK, Kumar JS et al (2016) Emergence of influenza A(H1N1)pdm09 genogroup 6B and drug resistant virus, India, January to May 2015. Euro Surveill 21:6–11CrossRefPubMed Parida M, Dash PK, Kumar JS et al (2016) Emergence of influenza A(H1N1)pdm09 genogroup 6B and drug resistant virus, India, January to May 2015. Euro Surveill 21:6–11CrossRefPubMed
37.
Zurück zum Zitat Wedde M, Biere B, Wolff T et al (2015) Evolution of the hemagglutinin expressed by human influenza A(H1N1)pdm09 and A(H3N2) viruses circulating between 2008–2009 and 2013–2014 in Germany. Int J Med Microbiol 305:762–775CrossRefPubMed Wedde M, Biere B, Wolff T et al (2015) Evolution of the hemagglutinin expressed by human influenza A(H1N1)pdm09 and A(H3N2) viruses circulating between 2008–2009 and 2013–2014 in Germany. Int J Med Microbiol 305:762–775CrossRefPubMed
43.
Zurück zum Zitat Al-Qahtani AA, Mubin M, Dela Cruz DM et al (2017) Phylogenetic and nucleotide sequence analysis of influenza A (H1N1) HA and NA genes of strains isolated from Saudi Arabia. J Infect Dev Ctries 11:81–88CrossRefPubMed Al-Qahtani AA, Mubin M, Dela Cruz DM et al (2017) Phylogenetic and nucleotide sequence analysis of influenza A (H1N1) HA and NA genes of strains isolated from Saudi Arabia. J Infect Dev Ctries 11:81–88CrossRefPubMed
46.
Zurück zum Zitat Hurt AC, Leang SK, Speers DJ et al (2012) Mutations I117V and I117M and oseltamivir sensitivity of pandemic (H1N1) 2009 viruses. Emerg Infect Dis 18:109–112CrossRefPubMedPubMedCentral Hurt AC, Leang SK, Speers DJ et al (2012) Mutations I117V and I117M and oseltamivir sensitivity of pandemic (H1N1) 2009 viruses. Emerg Infect Dis 18:109–112CrossRefPubMedPubMedCentral
47.
Zurück zum Zitat Kong W, Liu L, Wang Y et al (2014) Hemagglutinin mutation D222N of the 2009 pandemic H1N1 influenza virus alters receptor specificity without affecting virulence in mice. Virus Res 189:79–86CrossRefPubMed Kong W, Liu L, Wang Y et al (2014) Hemagglutinin mutation D222N of the 2009 pandemic H1N1 influenza virus alters receptor specificity without affecting virulence in mice. Virus Res 189:79–86CrossRefPubMed
48.
Zurück zum Zitat Matos-Patrón A, Byrd-Leotis L, Steinhauer DA et al (2015) Amino acid substitution D222N from fatal influenza infection affects receptor-binding properties of the influenza A(H1N1)pdm09 virus. Virology 484:15–21CrossRefPubMed Matos-Patrón A, Byrd-Leotis L, Steinhauer DA et al (2015) Amino acid substitution D222N from fatal influenza infection affects receptor-binding properties of the influenza A(H1N1)pdm09 virus. Virology 484:15–21CrossRefPubMed
49.
Zurück zum Zitat Goka EA, Vallely PJ, Mutton KJ et al (2014) Mutations associated with severity of the pandemic influenza A(H1N1)pdm09 in humans: a systematic review and meta-analysis of epidemiological evidence. Arch Virol 159:3167–3183CrossRefPubMed Goka EA, Vallely PJ, Mutton KJ et al (2014) Mutations associated with severity of the pandemic influenza A(H1N1)pdm09 in humans: a systematic review and meta-analysis of epidemiological evidence. Arch Virol 159:3167–3183CrossRefPubMed
50.
Zurück zum Zitat Jagger BW, Wise HM, Kash JC et al (2012) An overlapping protein-coding region in influenza A virus segment 3 modulates the host response. Science 337:199–204CrossRefPubMedPubMedCentral Jagger BW, Wise HM, Kash JC et al (2012) An overlapping protein-coding region in influenza A virus segment 3 modulates the host response. Science 337:199–204CrossRefPubMedPubMedCentral
52.
Zurück zum Zitat Shi M, Jagger BW, Wise HM et al (2012) Evolutionary conservation of the PA-X open reading frame in segment 3 of influenza A virus. J Virol 86:12411–12413CrossRefPubMedPubMedCentral Shi M, Jagger BW, Wise HM et al (2012) Evolutionary conservation of the PA-X open reading frame in segment 3 of influenza A virus. J Virol 86:12411–12413CrossRefPubMedPubMedCentral
53.
Zurück zum Zitat Kosik I, Holly J, Russ G (2013) PB1-F2 expedition from the whole protein through the domain to aa residue function. Acta Virol 57:138–148CrossRefPubMed Kosik I, Holly J, Russ G (2013) PB1-F2 expedition from the whole protein through the domain to aa residue function. Acta Virol 57:138–148CrossRefPubMed
54.
Zurück zum Zitat Hayashi T, MacDonald LA, Takimoto T (2015) Influenza A virus protein PA-X contributes to viral growth and suppression of the host antiviral and immune responses. J Virol 89:6442–6452CrossRefPubMedPubMedCentral Hayashi T, MacDonald LA, Takimoto T (2015) Influenza A virus protein PA-X contributes to viral growth and suppression of the host antiviral and immune responses. J Virol 89:6442–6452CrossRefPubMedPubMedCentral
55.
Zurück zum Zitat Bavagnoli L, Cucuzza S, Campanini G et al (2015) The novel influenza A virus protein PA-X and its naturally deleted variant show different enzymatic properties in comparison to the viral endonuclease PA. Nucleic Acids Res 43:9405–9417CrossRefPubMedPubMedCentral Bavagnoli L, Cucuzza S, Campanini G et al (2015) The novel influenza A virus protein PA-X and its naturally deleted variant show different enzymatic properties in comparison to the viral endonuclease PA. Nucleic Acids Res 43:9405–9417CrossRefPubMedPubMedCentral
56.
Zurück zum Zitat Gao H, Sun H, Hu J et al (2015) Twenty amino acids at the C-terminus of PA-X are associated with increased influenza A virus replication and pathogenicity. J Gen Virol 96:2036–2049CrossRefPubMedPubMedCentral Gao H, Sun H, Hu J et al (2015) Twenty amino acids at the C-terminus of PA-X are associated with increased influenza A virus replication and pathogenicity. J Gen Virol 96:2036–2049CrossRefPubMedPubMedCentral
57.
Zurück zum Zitat Xu G, Zhang X, Sun Y et al (2016) Truncation of C-terminal 20 amino acids in PA-X contributes to adaptation of swine influenza virus in pigs. Sci Rep 6:21845CrossRefPubMedPubMedCentral Xu G, Zhang X, Sun Y et al (2016) Truncation of C-terminal 20 amino acids in PA-X contributes to adaptation of swine influenza virus in pigs. Sci Rep 6:21845CrossRefPubMedPubMedCentral
58.
Zurück zum Zitat Lee J, Yu H, Li Y et al (2017) Impacts of different expressions of PA-X protein on 2009 pandemic H1N1 virus replication, pathogenicity and host immune responses. Virology 504:25–35CrossRefPubMedPubMedCentral Lee J, Yu H, Li Y et al (2017) Impacts of different expressions of PA-X protein on 2009 pandemic H1N1 virus replication, pathogenicity and host immune responses. Virology 504:25–35CrossRefPubMedPubMedCentral
59.
Zurück zum Zitat Trifonov V, Racaniello V, Rabadan R (2009) The contribution of the PB1-F2 protein to the fitness of influenza A viruses and its recent evolution in the 2009 influenza A (H1N1) pandemic virus. PLoS Curr 1:RRN1006CrossRefPubMedPubMedCentral Trifonov V, Racaniello V, Rabadan R (2009) The contribution of the PB1-F2 protein to the fitness of influenza A viruses and its recent evolution in the 2009 influenza A (H1N1) pandemic virus. PLoS Curr 1:RRN1006CrossRefPubMedPubMedCentral
Metadaten
Titel
Genetic characterization and diversity of circulating influenza A/H1N1pdm09 viruses isolated in Jeddah, Saudi Arabia between 2014 and 2015
verfasst von
Anwar M. Hashem
Esam I. Azhar
Sarah Shalhoub
Turki S. Abujamel
Norah A. Othman
Abdulwahab B. Al Zahrani
Hanan M. Abdullah
Maha M. Al-Alawi
Anees A. Sindi
Publikationsdatum
02.02.2018
Verlag
Springer Vienna
Erschienen in
Archives of Virology / Ausgabe 5/2018
Print ISSN: 0304-8608
Elektronische ISSN: 1432-8798
DOI
https://doi.org/10.1007/s00705-018-3732-y

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