Authors:
Mohsen Bashashati Department of Avian Disease Research and Diagnostic, Razi Vaccine and Serum Research Institute, Agricultural Research Education and Extension Organization (AREEO), Karaj, Iran

Search for other papers by Mohsen Bashashati in
Current site
Google Scholar
PubMed
Close
,
Zohreh Mojahedi Department of Viral Vaccine Quality Control, Razi Vaccine and Serum Research Institute, Agricultural Research Education and Extension Organization (AREEO), Karaj, Iran

Search for other papers by Zohreh Mojahedi in
Current site
Google Scholar
PubMed
Close
,
Ali Ameghi Roudsari Department of Research and Development, Razi Vaccine and Serum Research Institute, Agricultural Research Education and Extension Organization (AREEO), Karaj, Iran

Search for other papers by Ali Ameghi Roudsari in
Current site
Google Scholar
PubMed
Close
,
Morteza Taghizadeh Department of Research and Development, Razi Vaccine and Serum Research Institute, Agricultural Research Education and Extension Organization (AREEO), Karaj, Iran

Search for other papers by Morteza Taghizadeh in
Current site
Google Scholar
PubMed
Close
,
Aidin Molouki Department of Avian Disease Research and Diagnostic, Razi Vaccine and Serum Research Institute, Agricultural Research Education and Extension Organization (AREEO), Karaj, Iran

Search for other papers by Aidin Molouki in
Current site
Google Scholar
PubMed
Close
,
Najmeh Motamed Department of Poultry Vaccine Research and Production, Razi Vaccine and Serum Research Institute, Agricultural Research Education and Extension Organization (AREEO), Karaj, Iran

Search for other papers by Najmeh Motamed in
Current site
Google Scholar
PubMed
Close
,
Fereshteh Sabouri Department of Avian Disease Research and Diagnostic, Razi Vaccine and Serum Research Institute, Agricultural Research Education and Extension Organization (AREEO), Karaj, Iran

Search for other papers by Fereshteh Sabouri in
Current site
Google Scholar
PubMed
Close
, and
Mohammad Hossein Fallah Mehrabadi Department of Avian Disease Research and Diagnostic, Razi Vaccine and Serum Research Institute, Agricultural Research Education and Extension Organization (AREEO), Karaj, Iran

Search for other papers by Mohammad Hossein Fallah Mehrabadi in
Current site
Google Scholar
PubMed
Close
https://orcid.org/0000-0002-1221-7771
Restricted access

Abstract

Despite the use of wide-scale vaccination programmes against the H9N2 virus, enzootic outbreaks of H9N2 avian influenza (AI) have often occurred and caused serious nationwide economic losses, particularly in broiler chickens. In this study, the haemagglutinin (HA) and neuraminidase (NA) genes of nine recent H9N2s and a common vaccine strain were fully sequenced and compared with other representative Iranian viruses. Phylogenetic analysis revealed that all Iranian viruses were grouped into the G1 sub-lineage with different clusters in which recent isolates (2014–2017) formed a distinct cluster compared to the vaccine group (1998–2004). All Iranian H9N2s exhibited low pathogenicity AI connecting peptide feature with an R/KSSR motif. Amino acid 226, located in the 220 loop of the receptor binding site, was leucine among the recent Iranian viruses, a characteristic of human influenza viruses. With an overall gradual increase in the genetic diversity of H9N2s, Bayesian skyline plots of Iranian HA and NA genes depicted a fluctuation and a relative stable situation, respectively. It is recommended to apply constant surveillance to assess any increase in viral human adaptation and evolutionary changes in circulating field H9N2s. Moreover, antigenic characterisation of the prevailing H9N2 viruses seems to be necessary for evaluating the possible antigenic drift from the vaccine strain.

Supplementary Materials

    • Supplemental Materials
  • Alexander, D. J. (2007): An overview of the epidemiology of avian influenza. Vaccine 25, 56375644.

  • Bahari, P., Pourbakhsh, S. A., Shoushtari, H. and Bahmaninejad, M. A. (2015): Molecular characterization of H9N2 avian influenza viruses isolated from vaccinated broiler chickens in northeast Iran. Trop. Anim. Health Prod. 47, 11951201.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Bashashati, M., Vasfi Marandi, M. and Sabouri. F. (2013): Genetic diversity of early (1998) and recent (2010) avian influenza H9N2 virus strains isolated from poultry in Iran. Arch. Virol. 158, 20892100.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Boni, M. F., Posada, D. and Feldman, M. W. (2007): An exact nonparametric method for inferring mosaic structure in sequence triplets. Genetics 176, 10351047.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Butt, A. M., Siddique, S., Idrees, M. and Tong, Y. (2010): Avian influenza A (H9N2): computational molecular analysis and phylogenetic characterization of viral surface proteins isolated between 1997 and 2009 from the human population. Virol. J. 7, 319.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Fusaro, A., Monne, I., Salviato, A., Valastro, V., Schivo, A., Amarin, N. M., Gonzalez, C., Ismail, M. M., Al-Ankari, A. R., Al-Blowi, M. H., Khan, O. A., Maken Ali, A. S., Hedayati, A., Garcia Garcia, J., Ziay, G. M., Shoushtari, A., Al Qahtani, K. N., Capua, I., Holmes, E. C. and Cattoli, G. (2011): Phylogeography and evolutionary history of reassortant H9N2 viruses with potential human health implications. J. Virol. 85, 84138421.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Gibbs, M. J., Armstrong, J. S. and Gibbs, A. J. (2000): Sister-scanning: a Monte Carlo procedure for assessing signals in recombinant sequences. Bioinformatics 16, 573582.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Guan, Y., Shortridge, K. F., Krauss, S. and Webster, R. G. (1999): Molecular characterization of H9N2 influenza viruses: were they the donors of the ‘internal’ genes of H5N1 viruses in Hong Kong? Proc. Natl. Acad. Sci. U.S.A. 96, 93639367.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Guo, Y., Li, J. and Cheng, X. (1999): Discovery of men infected by avian influenza A (H9N2) virus [in Chinese]. Zhonghua Shi Yan He Lin Chuang Bing Du Xue Za Zhi 13, 105108.

    • Search Google Scholar
    • Export Citation
  • Hall, T. A. (1999): BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41, 9598.

    • Search Google Scholar
    • Export Citation
  • Hoffmann, E., Stech, J., Guan, Y., Webster, R. G. and Perez, D. R (2001): Universal primer set for the full-length amplification of all influenza A viruses. Arch. Virol. 146, 22752289.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Homme, P. J. and Easterday, B. C. (1970): Avian influenza virus infections. I. Characteristics of influenza A-turkey-Wisconsin-1966 virus. Avian Dis. 14, 6674.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Kaverin, N. V., Rudneva, I. A., Ilyushina, N. A., Lipatov, A. S., Krauss, S. and Webster, R. G. (2004): Structural differences among hemagglutinins of influenza A virus subtypes are reflected in their antigenic architecture: analysis of H9 escape mutants. J. Virol. 78, 240249.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Kumar, S., Stecher, G. and Tamura, K. (2016): MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 18701874.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Lee, D. H., Fusaro, A., Song, C. S., Suarez, D. L. and Swayne, D. E. (2016): Poultry vaccination directed evolution of H9N2 low pathogenicity avian influenza viruses in Korea. Virology 488, 225231.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Martin, D. and Rybicki, E. (2000): RDP: detection of recombination amongst aligned sequences. Bioinformatics 16, 562563.

  • Martin, D. P., Murrell, B., Golden, M., Khoosal, A. and Muhire, B. (2015): RDP4: detection and analysis of recombination patterns in virus genomes. Virus Evol. 1, vev003.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Matrosovich, M. N., Krauss, S. and Webster, R. G. (2001): H9N2 influenza A viruses from poultry in Asia have human virus-like receptor specificity. Virology 281, 156162.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Matrosovich, M., Stech, J. and Klenk, H. D. (2009): Influenza receptors, polymerase and host range. Rev. Sci. Tech. 28, 203217.

  • Norouzian, H., Bashashati, M. and Vasfimarandi, M. (2014): Phylogenetic analysis of neuraminidase gene of H9N2 avian influenza viruses isolated from chicken in Iran during 2010–2011. Iran. J. Microbiol. 6, 9197.

    • Search Google Scholar
    • Export Citation
  • Obadan, A. O., Santos, J., Ferreri, L., Thompson, A. J., Carnaccini, S., Geiger, G., Gonzalez Reiche, A. S., Rajão, D. S., Paulson, J. C. and Perez, D. R. (2019): Flexibility in vitro of amino acid 226 in the receptor-binding site of an H9 subtype influenza A virus and its effect in vivo on virus replication, tropism, and transmission. J. Virol. 93, pii: e02011-18.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • OIE (2019): Avian influenza (infection with avian influenza viruses). In: Manual of diagnostic tests and vaccines for terrestrial animals. Office International des Epizooties, Paris, France. pp. 821843.

    • Search Google Scholar
    • Export Citation
  • Padidam, M., Sawyer, S. and Fauquet, C. M. (1999): Possible emergence of new geminiviruses by frequent recombination. Virology 265, 218225.

  • Park, K. J., Kwon, H. I., Song, M. S., Pascua, P. N., Baek, Y. H., Lee, J. H., Jang, H. L., Lim, J. Y., Mo, I. P., Moon, H. J., Kim, C. J. and Choi, Y. K. (2011): Rapid evolution of low-pathogenic H9N2 avian influenza viruses following poultry vaccination programmes. J. Gen. Virol. 92, 3650.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Peacock, T., Reddy, K., James, J., Adamiak, B., Barclay, W., Shelton, H. and Iqbal, M. (2016): Antigenic mapping of an H9N2 avian influenza virus reveals two discrete antigenic sites and a novel mechanism of immune escape. Sci. Rep. 6, 18745.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Posada, D. and Crandall, K. A. (2001): Evaluation of methods for detecting recombination from DNA sequences: computer simulations. Proc. Natl. Acad. Sci. U.S.A. 98, 1375713762.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Pu, J., Wang, S., Yin, Y., Zhang, G., Carter, R. A., Wang, J., Xu, G., Sun, H., Wang, M., Wen, C., Wei, Y., Wang, D., Zhu, B., Lemmon, G., Jiao, Y., Duan, S., Wang, Q., Du, Q., Sun, M., Bao, J., Sun, Y., Zhao, J., Zhang, H., Wu, G., Liu, J. and Webster, R. G. (2015): Evolution of the H9N2 influenza genotype that facilitated the genesis of the novel H7N9 virus. Proc. Natl. Acad. Sci. U.S.A. 112, 548553.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Qi, W., Zhou, X., Shi, W., Huang, L., Xia, W., Liu, D., Li, H., Chen, S., Lei, F., Cao, L., Wu, J., He, F., Song, W., Li, Q., Li, H., Liao, M. and Liu, M. (2014): Genesis of the novel human-infecting influenza A(H10N8) virus and potential genetic diversity of the virus in poultry, China. Euro. Surveill. 19, 20841.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Rambaut, A., Drummond, A. J., Xie, D., Baele, G. and Suchard, M. A. (2018): Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Syst. Biol. 67, 901904.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Saito, T., Lim, W., Suzuki, T., Suzuki, Y., Kida, H., Nishimura, S. I. and Tashiro, M. (2001): Characterization of a human H9N2 influenza virus isolated in Hong Kong. Vaccine 20,125133.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Salminen, M. O., Carr, J. K., Burke, D. S. and McCutchan, F. E. (1995): Identification of breakpoints in intergenotypic recombinants of HIV type 1 by bootscanning. AIDS Res. Hum. Retrovir. 11, 14231425.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • SJCEIRS Working Group (2013): Assessing the fitness of distinct clades of influenza A (H9N2) viruses. Emerg. Microb. Infect. 2, e75.

  • Smith, J. M. (1992): Analyzing the mosaic structure of genes. J. Mol. Evol. 34, 126129.

  • Song, X. F., Han, P. and Chen, Y. P. (2011): Genetic variation of the hemagglutinin of avian influenza virus H9N2. J. Med. Virol. 83, 838846.

  • Steinhauer, D. A. (1999): Role of hemagglutinin cleavage for the pathogenicity of influenza virus. Virology 258, 120.

  • Suarez, D. L., Garcia, M., Latimer, J., Senne, D. and Perdue, M. (1999): Phylogenetic analysis of H7 avian influenza viruses isolated from the live bird markets of the Northeast United States. J. Virol. 73, 35673573.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Suchard, M. A., Lemey, P., Baele, G., Ayres, D. L., Drummond, A. J. and Rambaut, A. (2018): Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evol. 4, vey016.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Uhlendorff, J., Matrosovich, T., Klenk, H. D. and Matrosovich, M. (2009): Functional significance of the hemadsorption activity of influenza virus neuraminidase and its alteration in pandemic viruses. Arch. Virol. 154, 945957.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Varghese, J. N., Colman, P. M., van Donkelaar, A., Blick, T. J., Sahasrabudhe, A., McKimm-Breschkin, J. L. (1997): Structural evidence for a second sialic acid binding site in avian influenza virus neuraminidases. Proc. Natl Acad. Sci. U.S.A. 94, 1180811812.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Wan, H., Sorrell, E. M., Song, H., Hossain, M. J., Ramirez-Nieto, G., Monne, I., Stevens, J., Cattoli, G., Capua, I., Chen, L. M., Donis, R. O., Busch, J., Paulson, J. C., Brockwell, C., Webby, R., Blanco, J., Al-Natour, M. Q. and Perez, D. R. (2008): Replication and transmission of H9N2 influenza viruses in ferrets: evaluation of pandemic potential. PLoS One 3, e2923.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Weaver, S., Shank, S. D., Spielman, S. J., Li, M., Muse, S. V. and Kosakovsky Pond, S. L. (2018): Datamonkey 2.0: a modern web application for characterizing selective and other evolutionary processes. Mol. Biol. Evol. 35, 773777.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Xia, J., Cui, J., He, X., Liu, Y. Y., Yao, K. C., Cao, S. J., Han, X. F. and Huang, Y. (2017): Genetic and antigenic evolution of H9N2 subtype avian influenza virus in domestic chickens in southwestern China, 2013–2016. PLoS One 12, e0171564.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Collapse
  • Expand

Senior editors

Editor-in-Chief: Ferenc BASKA

Editorial assistant: Szilvia PÁLINKÁS

 

Editorial Board

  • Mária BENKŐ (Acta Veterinaria Hungarica, Budapest, Hungary)
  • Gábor BODÓ (University of Veterinary Medicine, Budapest, Hungary)
  • Béla DÉNES (University of Veterinary Medicine, Budapest Hungary)
  • Edit ESZTERBAUER (Veterinary Medical Research Institute, Budapest, Hungary)
  • Hedvig FÉBEL (University of Veterinary Medicine, Budapest, Hungary)
  • László FODOR (University of Veterinary Medicine, Budapest, Hungary)
  • János GÁL (University of Veterinary Medicine, Budapest, Hungary)
  • Balázs HARRACH (Veterinary Medical Research Institute, Budapest, Hungary)
  • Peter MASSÁNYI (Slovak University of Agriculture in Nitra, Nitra, Slovak Republic)
  • Béla NAGY (Veterinary Medical Research Institute, Budapest, Hungary)
  • Tibor NÉMETH (University of Veterinary Medicine, Budapest, Hungary)
  • Zsuzsanna NEOGRÁDY (University of Veterinary Medicine, Budapest, Hungary)
  • Dušan PALIĆ (Ludwig Maximilian University, Munich, Germany)
  • Alessandra PELAGALLI (University of Naples Federico II, Naples, Italy)
  • Kurt PFISTER (Ludwig-Maximilians-University of Munich, Munich, Germany)
  • László SOLTI (University of Veterinary Medicine, Budapest, Hungary)
  • József SZABÓ (University of Veterinary Medicine, Budapest, Hungary)
  • Péter VAJDOVICH (University of Veterinary Medicine, Budapest, Hungary)
  • János VARGA (University of Veterinary Medicine, Budapest, Hungary)
  • Štefan VILČEK (University of Veterinary Medicine in Kosice, Kosice, Slovak Republic)
  • Károly VÖRÖS (University of Veterinary Medicine, Budapest, Hungary)
  • Herbert WEISSENBÖCK (University of Veterinary Medicine, Vienna, Austria)
  • Attila ZSARNOVSZKY (Szent István University, Gödöllő, Hungary)

ACTA VETERINARIA HUNGARICA
Institute for Veterinary Medical Research
Centre for Agricultural Research
Hungarian Academy of Sciences
P.O. Box 18, H-1581 Budapest, Hungary
Phone: (36 1) 287 7073 (ed.-in-chief) or (36 1) 467 4081 (editor)

E-mail: acta.veterinaria@univet.hu (ed.-in-chief)

Indexing and Abstracting Services:

  • Biological Abstracts
  • BIOSIS Previews
  • CAB Abstracts
  • Chemical Abstracts
  • Current Contents: Agriculture, Biology and Environmental Sciences
  • Elsevier Science Navigator
  • Focus On: Veterinary Science and Medicine
  • Global Health
  • Index Medicus
  • Index Veterinarius
  • Medline
  • Science Citation Index
  • Science Citation Index Expanded (SciSearch)
  • SCOPUS
  • The ISI Alerting Services
  • Zoological Abstracts

 

2023  
Web of Science  
Journal Impact Factor 0.7
Rank by Impact Factor Q3 (Veterinary Sciences)
Journal Citation Indicator 0.4
Scopus  
CiteScore 1.8
CiteScore rank Q2 (General Veterinary)
SNIP 0.39
Scimago  
SJR index 0.258
SJR Q rank Q3

Acta Veterinaria Hungarica
Publication Model Hybrid
Submission Fee none
Article Processing Charge 1100 EUR/article
Printed Color Illustrations 40 EUR (or 10 000 HUF) + VAT / piece
Regional discounts on country of the funding agency World Bank Lower-middle-income economies: 50%
World Bank Low-income economies: 100%
Further Discounts Editorial Board / Advisory Board members: 50%
Corresponding authors, affiliated to an EISZ member institution subscribing to the journal package of Akadémiai Kiadó: 100%
Subscription fee 2025 Online subsscription: 832 EUR / 916 USD
Print + online subscription: 960 EUR / 1054 USD
Subscription Information Online subscribers are entitled access to all back issues published by Akadémiai Kiadó for each title for the duration of the subscription, as well as Online First content for the subscribed content.
Purchase per Title Individual articles are sold on the displayed price.

Acta Veterinaria Hungarica
Language English
Size A4
Year of
Foundation
1951
Volumes
per Year
1
Issues
per Year
4
Founder Magyar Tudományos Akadémia
Founder's
Address
H-1051 Budapest, Hungary, Széchenyi István tér 9.
Publisher Akadémiai Kiadó
Publisher's
Address
H-1117 Budapest, Hungary 1516 Budapest, PO Box 245.
Responsible
Publisher
Chief Executive Officer, Akadémiai Kiadó
ISSN 0236-6290 (Print)
ISSN 1588-2705 (Online)

Monthly Content Usage

Abstract Views Full Text Views PDF Downloads
Jun 2024 56 0 0
Jul 2024 56 1 1
Aug 2024 103 2 2
Sep 2024 145 0 0
Oct 2024 188 1 1
Nov 2024 178 1 1
Dec 2024 13 0 0