Top

Virology Journal

Published in:

Open Access 01-12-2016 | Research

First outbreaks and phylogenetic analyses of avian influenza H9N2 viruses isolated from poultry flocks in Morocco

Authors: Mohammed EL Houadfi, Siham Fellahi, Saadia Nassik, Jean-Luc Guérin, Mariette F. Ducatez

Published in: Virology Journal | Issue 1/2016

Abstract

Background

H9N2 avian influenza viruses continue to spread in poultry and wild birds worldwide. Morocco just faced its first H9N2 influenza virus outbreaks early 2016 affecting different types of poultry production. After its introduction, the virus spread very rapidly throughout the country.

Methods

Samples were collected from 11 chicken flocks with high morbidity and mortality rates. Four viruses were successfully isolated from broiler chickens and one from broiler breeders and fully sequenced.

Results

Phylogenetic and molecular markers analyses showed the Moroccan viruses belonged to the G1 lineage and likely originated from the Middle East. As known for H9N2 viruses, the Moroccanisolates possess several genetic markers that enhance virulence in poultry and transmission to humans.

Conclusion

The present study demonstrated that under field conditions H9N2 could have a devastating effect on egg production and mortalities and highlighted a lack of surveillance data on the pathogen in the region.

Butt KM, Smith GJ, Chen H, et al. Human infection with an avian H9N2 influenza A virus in Hong Kong in 2003. J Clin Microbiol. 2005;43:5760–67.

Sun Y, Liu J. H9N2 influenza virus in China: a cause of concern. Protein Cell. 2015;6:18–25.CrossRefPubMed

Li C, Yu K, Tian G, Yu D, Liu L, Jing B, et al. Evolution of H9N2 influenza viruses from domestic poultry in Mainland China. Virology. 2005;340:70–83.CrossRefPubMed

Lee D-H, Song C-S. H9N2 avian influenza virus in Korea: evolution and vaccination. Clin Exp Vaccine Res. 2013;2:26.CrossRefPubMedPubMedCentral

Naeem K, Ullah A, Manvell RJ, Alexander DJ. Avian influenza A subtype H9N2 in poultry in Pakistan. Vet Rec. 1999;145:560.CrossRefPubMed

Nili H, Asasi K. Avian influenza (H9N2) outbreak in Iran. Avian Dis. 2003;47:828–31.CrossRefPubMed

Perk S, Banetnoach C, Shihmanter E, Pokamunski S, Pirak M, Lipkind M, et al. Genetic characterization of the H9N2 influenza viruses circulated in the poultry population in Israel. Comp Immunol Microbiol Infect Dis. 2006;29:207–23.CrossRefPubMed

Aamir UB, Wernery U, Ilyushina N, Webster RG. Characterization of avian H9N2 influenza viruses from United Arab Emirates 2000 to 2003. Virology. 2007;361:45–55.CrossRefPubMed

Body MH, Alrarawahi AH, Alhubsy SS, Saravanan N, Rajmony S, Mansoor MK. Characterization of Low Pathogenic Avian Influenza Virus Subtype H9N2 Isolated from Free-Living Mynah Birds (Acridotheres tristis) in the Sultanate of Oman. Avian Dis. 2015;59:329–34.CrossRefPubMed

10.

Monne I, Ormelli S, Salviato A, De Battisti C, Bettini F, Salomoni A, et al. Development and Validation of a One-Step Real-Time PCR Assay for Simultaneous Detection of Subtype H5, H7, and H9 Avian Influenza Viruses. J Clin Microbiol. 2008;46:1769–73.CrossRefPubMedPubMedCentral

11.

Kammon A, Heidari A, Dayhum A, Eldaghayes I, Sharif M, Monne I, et al. Characterization of Avian Influenza and Newcastle Disease Viruses from Poultry in Libya. Avian Dis. 2015;59:422–30.CrossRefPubMed

12.

Seifi S, Asasi K, Mohammadi A. An experimental study on broiler chicken co-infected with the specimens containing avian influenza (H9 subtype) and infectious bronchitis (4/91 strain) viruses. Iran J Vet Res. 2012;13:138–42.

13.

Azizpour A, Goudarzi H, Charkhkar S, Momayez R, Hablolvarid MH. Experimental study on tissue tropism and dissemination of H9N2 avian influenza virus and Ornithobacterium rhinotracheale co-infection in SPF chickens. JAPS J Anim Plant Sci. 2014;24:1655–62.

14.

Iqbal M, Yaqub T, Mukhtar N, Shabbir MZ, McCauley JW. Infectivity and transmissibility of H9N2 avian influenza virus in chickens and wild terrestrial birds. Vet Res. 2013;44:100.CrossRefPubMedPubMedCentral

15.

Zhang K, Zhang Z, Yu Z, Li L, Cheng K, Wang T, et al. Domestic cats and dogs are susceptible to H9N2 avian influenza virus. Virus Res. 2013;175:52–7.CrossRefPubMed

16.

Khan SU, Anderson BD, Heil GL, Liang S, Gray GC. A Systematic Review and Meta-Analysis of the Seroprevalence of Influenza A(H9N2) Infection Among Humans. J Infect Dis. 2015;212:562-9.CrossRefPubMed

17.

Group TSHW. Assessing the fitness of distinct clades of influenza A (H9N2) viruses. Emerg Microbes Infect. 2013;2:e75.CrossRef

18.

Xu KM, Li KS, Smith GJD, Li JW, Tai H, Zhang JX, et al. Evolution and Molecular Epidemiology of H9N2 Influenza A Viruses from Quail in Southern China, 2000 to 2005. J Virol. 2007;81:2635–45.CrossRefPubMed

19.

Wise MG, Suarez DL, Seal BS, Pedersen JC, Senne DA, King DJ, et al. Development of a Real-Time Reverse-Transcription PCR for Detection of Newcastle Disease Virus RNA in Clinical Samples. J Clin Microbiol. 2004;42:329–38.CrossRefPubMedPubMedCentral

20.

Meir R, Maharat O, Farnushi Y, Simanov L. Development of a real-time TaqMan® RT-PCR assay for the detection of infectious bronchitis virus in chickens, and comparison of RT-PCR and virus isolation. J Virol Methods. 2010;163:190–4.CrossRefPubMed

21.

Tomás G, Hernández M, Marandino A, Panzera Y, Maya L, Hernández D, et al. Development and validation of a TaqMan-MGB real-time RT-PCR assay for simultaneous detection and characterization of infectious bursal disease virus. J Virol Methods. 2012;185:101–7.CrossRefPubMed

22.

Hoffmann E, Stech J, Guan Y, Webster RG, Perez DR. Universal primer set for the full-length amplification of all influenza A viruses. Arch Virol. 2001;146:2275–89.CrossRefPubMed

23.

Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 1999;95–8

24.

Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Mol Biol Evol. 2013;30:2725–9.CrossRefPubMedPubMedCentral

25.

Wagner R, Wolff T, Herwig A, Pleschka S, Klenk HD. Interdependence of hemagglutinin glycosylation and neuraminidase as regulators of influenza virus growth: a study by reverse genetics. J Virol. 2000;74:6316–23.CrossRefPubMedPubMedCentral

26.

Wanzeck K, Boyd KL, McCullers JA. Glycan shielding of the influenza virus hemagglutinin contributes to immunopathology in mice. Am J Respir Crit Care Med. 2011;183:767–73.CrossRefPubMed

27.

Kandeil A, El-Shesheny R, Maatouq AM, Moatasim Y, Shehata MM, Bagato O, et al. Genetic and antigenic evolution of H9N2 avian influenza viruses circulating in Egypt between 2011 and 2013. Arch Virol. 2014;159:2861–76.CrossRefPubMedPubMedCentral

28.

Shaw M, Cooper L, Xu X, Thompson W, Krauss S, Guan Y, et al. Molecular changes associated with the transmission of avian influenza a H5N1 and H9N2 viruses to humans. J Med Virol. 2002;66:107–14.CrossRefPubMed

29.

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

30.

Wernery U, Shanmuganatham KK, Krylov PS, Joseph S, Friedman K, Krauss S, et al. H9N2 influenza viruses from birds used in falconry. Influenza Other Respir Viruses. 2013;7:1241–5.CrossRefPubMedPubMedCentral

31.

Chen G-W, Chang S-C, Mok C, Lo Y-L, Kung Y-N, Huang J-H, et al. Genomic signatures of human versus avian influenza A viruses. Emerg Infect Dis. 2006;12:1353–60.CrossRefPubMed

32.

Rolling T, Koerner I, Zimmermann P, Holz K, Haller O, Staeheli P, et al. Adaptive mutations resulting in enhanced polymerase activity contribute to high virulence of influenza A virus in mice. J Virol. 2009;83:6673–80.CrossRefPubMedPubMedCentral

33.

Kageyama T, Fujisaki S, Takashita E, Xu H, Yamada S, Uchida Y, et al. Genetic analysis of novel avian A (H7N9) influenza viruses isolated from patients in China, February to April 2013. Euro Surveill. 2013;18:7–21.

34.

Wang Y, Yuan X, Qi L, Zhang Y, Xu H, Yang J, et al. H9N2 avian influenza virus-derived natural reassortant H5N2 virus in swan containing the hemagglutinin segment from Eurasian H5 avian influenza virus with an in-frame deletion of four basic residues in the polybasic hemagglutinin cleavage site. Infect Genet Evol. 2016;40:17–20.CrossRefPubMed

35.

Li X, Shi J, Guo J, Deng G, Zhang Q, Wang J, et al. Genetics, receptor binding property, and transmissibility in mammals of naturally isolated H9N2 Avian Influenza viruses. PLoS Pathog. 2014;10:e1004508.CrossRefPubMedPubMedCentral

36.

WHO, Influenza at the human-animal interface, Summary and assessment, 5 April to 9 May 2016, 2016. http://www.who.int/influenza/human_animal_interface/Influenza_Summary_IRA_HA_interface_05_09_2016.pdf?ua=1, Accessed 12 July 2016.

37.

Roussan DA, Khawaldeh GY, Al Rifai RH, Totanji WS, Shaheen IA. Avian influenza virus H9 subtype in poultry flocks in Jordan. Prev Vet Med. 2009;88:77–81.CrossRefPubMed

38.

Baigent SJ, McCauley JW. Influenza type A in humans, mammals and birds: Determinants of virus virulence, host-range and interspecies transmission. BioEssays. 2003;25:657–71.CrossRefPubMed

39.

Wan H, Perez DR. Amino Acid 226 in the Hemagglutinin of H9N2 Influenza Viruses Determines Cell Tropism and Replication in Human Airway Epithelial Cells. J Virol. 2007;81:5181–91.CrossRefPubMedPubMedCentral

40.

Guan Y, Shortridge KF, Krauss S, Webster RG. Molecular characterization of H9N2 influenza viruses: were they the donors of the “internal” genes of H5N1 viruses in Hong Kong? Proc Natl Acad Sci. 1999;96:9363–7.CrossRefPubMedPubMedCentral

41.

Wu D, Zou S, Bai T, Li J, Zhao X, Yang L, et al. Poultry farms as a source of avian influenza A (H7N9) virus reassortment and human infection. Sci Rep. 2015;5:7630.CrossRefPubMedPubMedCentral

Title: First outbreaks and phylogenetic analyses of avian influenza H9N2 viruses isolated from poultry flocks in Morocco
Authors: Mohammed EL Houadfi
Siham Fellahi
Saadia Nassik
Jean-Luc Guérin
Mariette F. Ducatez
Publication date: 01-12-2016
Publisher: BioMed Central
Published in: Virology Journal / Issue 1/2016
Electronic ISSN: 1743-422X
DOI: https://doi.org/10.1186/s12985-016-0596-1

ACC 2024 Congress Coverage

Heart Failure Video

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

First outbreaks and phylogenetic analyses of avian influenza H9N2 viruses isolated from poultry flocks in Morocco

Abstract

Background

Methods

Results

Conclusion

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Abstract

Background

Methods

Results

Conclusion

Please log in to get access to this content

Other articles of this Issue 1/2016

Codon optimization of antigen coding sequences improves the immune potential of DNA vaccines against avian influenza virus H5N1 in mice and chickens

Serosurveillance of viral pathogens circulating in West Africa

Circulation of avian paramyxoviruses in wild birds of Kazakhstan in 2002–2013

Prevalence of antibody to Hepatitis B core antigen and Hepatitis B virus DNA in HBsAg negative healthy blood donors

Molecular characterization of Nipah virus from Pteropus hypomelanus in Southern Thailand

Detection of the first G6P[14] human rotavirus strain in an infant with diarrhoea in Ghana

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page