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Title: Genetically Diverse Low Pathogenicity Avian Influenza A Virus Subtypes Co-Circulate among Poultry in Bangladesh

Abstract

Influenza virus surveillance, poultry outbreak investigations and genomic sequencing were assessed to understand the ecology and evolution of low pathogenicity avian influenza (LPAI) A viruses in Bangladesh from 2007 to 2013. We analyzed 506 avian specimens collected from poultry in live bird markets and backyard flocks to identify influenza A viruses. Virus isolation-positive specimens (n = 50) were subtyped and their coding-complete genomes were sequenced. The most frequently identified subtypes among LPAI isolates were H9N2, H11N3, H4N6, and H1N1. Less frequently detected subtypes included H1N3, H2N4, H3N2, H3N6, H3N8, H4N2, H5N2, H6N1, H6N7, and H7N9. Gene sequences were compared to publicly available sequences using phylogenetic inference approaches. Among the 14 subtypes identified, the majority of viral gene segments were most closely related to poultry or wild bird viruses commonly found in Southeast Asia, Europe, and/or northern Africa. LPAI subtypes were distributed over several geographic locations in Bangladesh, and surface and internal protein gene segments clustered phylogenetically with a diverse number of viral subtypes suggesting extensive reassortment among these LPAI viruses. H9N2 subtype viruses differed from other LPAI subtypes because genes from these viruses consistently clustered together, indicating this subtype is enzootic in Bangladesh. The H9N2 strains identified in Bangladesh weremore » phylogenetically and antigenically related to previous human-derived H9N2 viruses detected in Bangladesh representing a potential source for human infection. In contrast, the circulating LPAI H5N2 and H7N9 viruses were both phylogenetically and antigenically unrelated to H5 viruses identified previously in humans in Bangladesh and H7N9 strains isolated from humans in China. In Bangladesh, domestic poultry sold in live bird markets carried a wide range of LPAI virus subtypes and a high diversity of genotypes. Here these findings, combined with the seven year timeframe of sampling, indicate a continuous circulation of these viruses in the country.« less

Authors:
 [1];  [2];  [1];  [1];  [2];  [2];  [2];  [2];  [3];  [4];  [2];  [2];  [1];  [1];  [5];  [1];  [6]
  1. Centers for Disease Control and Prevention, Atlanta, GA (United States)
  2. International Centre for Diarrhoeal Disease Research, Dhaka (Bangladesh)
  3. Ministry of Fisheries and Livestock, Dhaka (Bangladesh)
  4. EcoHealth Alliance, New York, NY (United States)
  5. Centers for Disease Control and Prevention, Atlanta, GA (United States); International Centre for Diarrhoeal Disease Research, Dhaka (Bangladesh)
  6. Linneaus Univ. (Sweden)
Publication Date:
Research Org.:
Oak Ridge Institute for Science and Education (ORISE), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1377073
Resource Type:
Accepted Manuscript
Journal Name:
PLoS ONE
Additional Journal Information:
Journal Volume: 11; Journal Issue: 3; Journal ID: ISSN 1932-6203
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES; H7N9; Animal phylogenetics; Poultry; Bird genetics; Microbial genetics; Viral pathogens; Birds; Bangladesh

Citation Formats

Gerloff, Nancy A., Khan, Salah Uddin, Zanders, Natosha, Balish, Amanda, Haider, Najmul, Islam, Ausraful, Chowdhury, Sukanta, Rahman, Mahmudur Ziaur, Haque, Ainul, Hosseini, Parviez, Gurley, Emily S., Luby, Stephen P., Wentworth, David E., Donis, Ruben O., Sturm-Ramirez, Katharine, Davis, C. Todd, and Waldenstrom, Jonas. Genetically Diverse Low Pathogenicity Avian Influenza A Virus Subtypes Co-Circulate among Poultry in Bangladesh. United States: N. p., 2016. Web. doi:10.1371/journal.pone.0152131.
Gerloff, Nancy A., Khan, Salah Uddin, Zanders, Natosha, Balish, Amanda, Haider, Najmul, Islam, Ausraful, Chowdhury, Sukanta, Rahman, Mahmudur Ziaur, Haque, Ainul, Hosseini, Parviez, Gurley, Emily S., Luby, Stephen P., Wentworth, David E., Donis, Ruben O., Sturm-Ramirez, Katharine, Davis, C. Todd, & Waldenstrom, Jonas. Genetically Diverse Low Pathogenicity Avian Influenza A Virus Subtypes Co-Circulate among Poultry in Bangladesh. United States. https://doi.org/10.1371/journal.pone.0152131
Gerloff, Nancy A., Khan, Salah Uddin, Zanders, Natosha, Balish, Amanda, Haider, Najmul, Islam, Ausraful, Chowdhury, Sukanta, Rahman, Mahmudur Ziaur, Haque, Ainul, Hosseini, Parviez, Gurley, Emily S., Luby, Stephen P., Wentworth, David E., Donis, Ruben O., Sturm-Ramirez, Katharine, Davis, C. Todd, and Waldenstrom, Jonas. Thu . "Genetically Diverse Low Pathogenicity Avian Influenza A Virus Subtypes Co-Circulate among Poultry in Bangladesh". United States. https://doi.org/10.1371/journal.pone.0152131. https://www.osti.gov/servlets/purl/1377073.
@article{osti_1377073,
title = {Genetically Diverse Low Pathogenicity Avian Influenza A Virus Subtypes Co-Circulate among Poultry in Bangladesh},
author = {Gerloff, Nancy A. and Khan, Salah Uddin and Zanders, Natosha and Balish, Amanda and Haider, Najmul and Islam, Ausraful and Chowdhury, Sukanta and Rahman, Mahmudur Ziaur and Haque, Ainul and Hosseini, Parviez and Gurley, Emily S. and Luby, Stephen P. and Wentworth, David E. and Donis, Ruben O. and Sturm-Ramirez, Katharine and Davis, C. Todd and Waldenstrom, Jonas},
abstractNote = {Influenza virus surveillance, poultry outbreak investigations and genomic sequencing were assessed to understand the ecology and evolution of low pathogenicity avian influenza (LPAI) A viruses in Bangladesh from 2007 to 2013. We analyzed 506 avian specimens collected from poultry in live bird markets and backyard flocks to identify influenza A viruses. Virus isolation-positive specimens (n = 50) were subtyped and their coding-complete genomes were sequenced. The most frequently identified subtypes among LPAI isolates were H9N2, H11N3, H4N6, and H1N1. Less frequently detected subtypes included H1N3, H2N4, H3N2, H3N6, H3N8, H4N2, H5N2, H6N1, H6N7, and H7N9. Gene sequences were compared to publicly available sequences using phylogenetic inference approaches. Among the 14 subtypes identified, the majority of viral gene segments were most closely related to poultry or wild bird viruses commonly found in Southeast Asia, Europe, and/or northern Africa. LPAI subtypes were distributed over several geographic locations in Bangladesh, and surface and internal protein gene segments clustered phylogenetically with a diverse number of viral subtypes suggesting extensive reassortment among these LPAI viruses. H9N2 subtype viruses differed from other LPAI subtypes because genes from these viruses consistently clustered together, indicating this subtype is enzootic in Bangladesh. The H9N2 strains identified in Bangladesh were phylogenetically and antigenically related to previous human-derived H9N2 viruses detected in Bangladesh representing a potential source for human infection. In contrast, the circulating LPAI H5N2 and H7N9 viruses were both phylogenetically and antigenically unrelated to H5 viruses identified previously in humans in Bangladesh and H7N9 strains isolated from humans in China. In Bangladesh, domestic poultry sold in live bird markets carried a wide range of LPAI virus subtypes and a high diversity of genotypes. Here these findings, combined with the seven year timeframe of sampling, indicate a continuous circulation of these viruses in the country.},
doi = {10.1371/journal.pone.0152131},
journal = {PLoS ONE},
number = 3,
volume = 11,
place = {United States},
year = {Thu Mar 24 00:00:00 EDT 2016},
month = {Thu Mar 24 00:00:00 EDT 2016}
}

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Works referenced in this record:

Clinical and epidemiological characteristics of a fatal case of avian influenza A H10N8 virus infection: a descriptive study
journal, February 2014


Multiple introductions of highly pathogenic avian influenza H5N1 viruses into Bangladesh
journal, January 2014

  • Marinova-Petkova, Atanaska; Feeroz, Mohammed M.; Rabiul Alam, Sm
  • Emerging Microbes & Infections, Vol. 3, Issue 1
  • DOI: 10.1038/emi.2014.11

Origin and Molecular Characteristics of a Novel 2013 Avian Influenza A(H6N1) Virus Causing Human Infection in Taiwan
journal, November 2013

  • Yuan, Jian; Zhang, Lei; Kan, Xianzhao
  • Clinical Infectious Diseases, Vol. 57, Issue 9
  • DOI: 10.1093/cid/cit479

H9N2 Influenza Viruses from Israeli Poultry: A Five-Year Outbreak
journal, March 2007


H9N2 influenza viruses isolated from poultry in Korean live bird markets continuously evolve and cause the severe clinical signs in layers
journal, December 2006


Detection of a Broad Range of Class I and II Newcastle Disease Viruses Using a Multiplex Real-Time Reverse Transcription Polymerase Chain Reaction Assay
journal, July 2008

  • Kim, L. Mia; Suarez, David L.; Afonso, Claudio L.
  • Journal of Veterinary Diagnostic Investigation, Vol. 20, Issue 4
  • DOI: 10.1177/104063870802000402

Ecological Determinants of Highly Pathogenic Avian Influenza (H5N1) Outbreaks in Bangladesh
journal, March 2012


Ducks: The “Trojan Horses” of H5N1 influenza
journal, July 2009


Multiple reassortment events among highly pathogenic avian influenza A(H5N1) viruses detected in Bangladesh
journal, February 2014


Isolation and pathotyping of H9N2 avian influenza viruses in Indian poultry
journal, January 2009


MEGA5: Molecular Evolutionary Genetics Analysis Using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods
journal, May 2011

  • Tamura, K.; Peterson, D.; Peterson, N.
  • Molecular Biology and Evolution, Vol. 28, Issue 10
  • DOI: 10.1093/molbev/msr121

Basic local alignment search tool
journal, October 1990

  • Altschul, Stephen F.; Gish, Warren; Miller, Webb
  • Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410
  • DOI: 10.1016/S0022-2836(05)80360-2

Molecular characterization of H9N2 influenza viruses: Were they the donors of the "internal" genes of H5N1 viruses in Hong Kong?
journal, August 1999

  • Guan, Y.; Shortridge, K. F.; Krauss, S.
  • Proceedings of the National Academy of Sciences, Vol. 96, Issue 16
  • DOI: 10.1073/pnas.96.16.9363

Surveillance of avian influenza virus type A in semi-scavenging ducks in Bangladesh
journal, January 2013

  • Khatun, Amina; Giasuddin, Mohammed; Islam, Kazi
  • BMC Veterinary Research, Vol. 9, Issue 1
  • DOI: 10.1186/1746-6148-9-196

Global Patterns of Influenza A Virus in Wild Birds
journal, April 2006


Isolation and characterization of H7N9 viruses from live poultry markets — Implication of the source of current H7N9 infection in humans
journal, April 2013


Reassortant Avian Influenza A(H9N2) Viruses in Chickens in Retail Poultry Shops, Pakistan, 2009–2010
journal, April 2015

  • Chaudhry, Mamoona; Angot, Angélique; Rashid, Hamad B.
  • Emerging Infectious Diseases, Vol. 21, Issue 4
  • DOI: 10.3201/eid2104.141570

Live Bird Markets of Bangladesh: H9N2 Viruses and the Near Absence of Highly Pathogenic H5N1 Influenza
journal, April 2011


MUSCLE: multiple sequence alignment with high accuracy and high throughput
journal, March 2004

  • Edgar, R. C.
  • Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797
  • DOI: 10.1093/nar/gkh340

Influenza Virus in a Natural Host, the Mallard: Experimental Infection Data
journal, January 2010


An overview of the epidemiology of avian influenza
journal, July 2007


Epidemiology of Human Infections with Avian Influenza A(H7N9) Virus in China
journal, February 2014

  • Li, Qun; Zhou, Lei; Zhou, Minghao
  • New England Journal of Medicine, Vol. 370, Issue 6
  • DOI: 10.1056/NEJMoa1304617

A High Diversity of Eurasian Lineage Low Pathogenicity Avian Influenza A Viruses Circulate among Wild Birds Sampled in Egypt
journal, July 2013


Human Infection with a Novel Avian-Origin Influenza A (H7N9) Virus
journal, May 2013

  • Gao, Rongbao; Cao, Bin; Hu, Yunwen
  • New England Journal of Medicine, Vol. 368, Issue 20
  • DOI: 10.1056/NEJMoa1304459

Evolution of H9N2 influenza viruses from domestic poultry in Mainland China
journal, September 2005


Invasive Pneumococcal Disease Burden and Implications for Vaccine Policy in Urban Bangladesh
journal, November 2007

  • Naheed, Aliya; El Arifeen, Shams; Sack, David A.
  • The American Journal of Tropical Medicine and Hygiene, Vol. 77, Issue 5
  • DOI: 10.4269/ajtmh.2007.77.795

Genome-wide identification, structural analysis and expression profiles of GRAS gene family in orchardgrass
journal, February 2020


An overview of the epidemiology of avian influenza
journal, July 2007


H9N2 influenza viruses isolated from poultry in Korean live bird markets continuously evolve and cause the severe clinical signs in layers
journal, December 2006


Isolation and pathotyping of H9N2 avian influenza viruses in Indian poultry
journal, January 2009


Evolution of H9N2 influenza viruses from domestic poultry in Mainland China
journal, September 2005


Multiple reassortment events among highly pathogenic avian influenza A(H5N1) viruses detected in Bangladesh
journal, February 2014


Avian influenza A H7N9 in Zhejiang, China
journal, June 2013


Genesis of avian-origin H7N9 influenza A viruses
journal, June 2013


Avian influenza A H10N8—a virus on the verge?
journal, February 2014


Multiple introductions of highly pathogenic avian influenza H5N1 viruses into Bangladesh
journal, January 2014

  • Marinova-Petkova, Atanaska; Feeroz, Mohammed M.; Rabiul Alam, Sm
  • Emerging Microbes & Infections, Vol. 3, Issue 1
  • DOI: 10.1038/emi.2014.11

Molecular characterization of H9N2 influenza viruses: Were they the donors of the "internal" genes of H5N1 viruses in Hong Kong?
journal, August 1999

  • Guan, Y.; Shortridge, K. F.; Krauss, S.
  • Proceedings of the National Academy of Sciences, Vol. 96, Issue 16
  • DOI: 10.1073/pnas.96.16.9363

Origin and Molecular Characteristics of a Novel 2013 Avian Influenza A(H6N1) Virus Causing Human Infection in Taiwan
journal, November 2013

  • Yuan, Jian; Zhang, Lei; Kan, Xianzhao
  • Clinical Infectious Diseases, Vol. 57, Issue 9
  • DOI: 10.1093/cid/cit479

MUSCLE: multiple sequence alignment with high accuracy and high throughput
journal, March 2004

  • Edgar, R. C.
  • Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797
  • DOI: 10.1093/nar/gkh340

Detection of a Broad Range of Class I and II Newcastle Disease Viruses Using a Multiplex Real-Time Reverse Transcription Polymerase Chain Reaction Assay
journal, July 2008

  • Kim, L. Mia; Suarez, David L.; Afonso, Claudio L.
  • Journal of Veterinary Diagnostic Investigation, Vol. 20, Issue 4
  • DOI: 10.1177/104063870802000402

Epidemic of avian influenza A (H7N9) virus in China
journal, June 2014


Avian influenza surveillance reveals presence of low pathogenic avian influenza viruses in poultry during 2009-2011 in the West Bengal State, India
journal, January 2012

  • Pawar, Shailesh D.; Kale, Sandeep D.; Rawankar, Amol S.
  • Virology Journal, Vol. 9, Issue 1
  • DOI: 10.1186/1743-422x-9-151

Surveillance of avian influenza virus type A in semi-scavenging ducks in Bangladesh
journal, January 2013

  • Khatun, Amina; Giasuddin, Mohammed; Islam, Kazi
  • BMC Veterinary Research, Vol. 9, Issue 1
  • DOI: 10.1186/1746-6148-9-196

Influenza Virus in a Natural Host, the Mallard: Experimental Infection Data
journal, January 2010


Live Bird Markets of Bangladesh: H9N2 Viruses and the Near Absence of Highly Pathogenic H5N1 Influenza
journal, April 2011


Ecological Determinants of Highly Pathogenic Avian Influenza (H5N1) Outbreaks in Bangladesh
journal, March 2012


A High Diversity of Eurasian Lineage Low Pathogenicity Avian Influenza A Viruses Circulate among Wild Birds Sampled in Egypt
journal, July 2013


Avian influenza A(H7N9) and the closure of live bird markets
journal, May 2013


Works referencing / citing this record:

Review analysis and impact of co-circulating H5N1 and H9N2 avian influenza viruses in Bangladesh
journal, May 2018

  • Parvin, Rokshana; Begum, Jahan Ara; Nooruzzaman, Mohammed
  • Epidemiology and Infection, Vol. 146, Issue 10
  • DOI: 10.1017/s0950268818001292

Avian influenza surveillance in domestic waterfowl and environment of live bird markets in Bangladesh, 2007–2012
journal, June 2018


Continuing evolution of highly pathogenic H5N1 viruses in Bangladeshi live poultry markets
journal, January 2019


Avian influenza virus surveillance in migratory birds in Egypt revealed a novel reassortant H6N2 subtype
journal, October 2019


A Decade of Avian Influenza in Bangladesh: Where Are We Now?
journal, September 2019


A Qualitative Stakeholder Analysis of Avian Influenza Policy in Bangladesh
journal, November 2017


Role of domestic ducks in the emergence of a new genotype of highly pathogenic H5N1 avian influenza A viruses in Bangladesh
journal, January 2017

  • Barman, Subrata; Marinova-Petkova, Atanaska; Hasan, M. Kamrul
  • Emerging Microbes & Infections, Vol. 6, Issue 1
  • DOI: 10.1038/emi.2017.60

Avian influenza surveillance in domestic waterfowl and environment of live bird markets in Bangladesh, 2007–2012
journal, June 2018


Novel multiplex assay platforms to detect influenza A hemagglutinin subtype-specific antibody responses for high-throughput and in-field applications
journal, April 2017

  • Li, Zhu-Nan; Trost, Jessica F.; Weber, Kimberly M.
  • Influenza and Other Respiratory Viruses, Vol. 11, Issue 3
  • DOI: 10.1111/irv.12449

Serological and virological surveillance of avian influenza virus in domestic ducks of the north-east region of Bangladesh
journal, June 2017

  • Sarker, Rahul Deb; Giasuddin, Mohammad; Chowdhury, Emdadul Haque
  • BMC Veterinary Research, Vol. 13, Issue 1
  • DOI: 10.1186/s12917-017-1104-6

Semi-Scavenging Poultry as Carriers of Avian Influenza Genes
journal, February 2022

  • Badruzzaman, A. T. M.; Rahman, Md. Masudur; Hasan, Mahmudul
  • Life, Vol. 12, Issue 2
  • DOI: 10.3390/life12020320

A Decade of Avian Influenza in Bangladesh: Where Are We Now?
journal, September 2019