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Highly Pathogenic Avian Influenza A(H5N1) Virus Infection among Workers at Live Bird Markets, Bangladesh, 2009–2010 - Volume 21, Number 4—April 2015 - Emerging Infectious Disease journal - CDC


Highly Pathogenic Avian Influenza A(H5N1) Virus Infection among Workers at Live Bird Markets, Bangladesh, 2009–2010 - Volume 21, Number 4—April 2015 - Emerging Infectious Disease journal - CDC

Volume 21, Number 4—April 2015


Highly Pathogenic Avian Influenza A(H5N1) Virus Infection among Workers at Live Bird Markets, Bangladesh, 2009–2010

Sharifa NasreenComments to Author , Salah Uddin Khan, Stephen P. Luby, Emily S. Gurley, Jaynal Abedin, Rashid Uz Zaman, Badrul Munir Sohel, Mustafizur Rahman, Kathy Hancock, Min Z. Levine, Vic Veguilla, David Wang, Crystal Holiday, Eric Gillis, Katharine Sturm-Ramirez, Joseph S. Bresee, Mahmudur Rahman, Timothy M. Uyeki, Jacqueline M. Katz, and Eduardo Azziz-Baumgartner
Author affiliations: icddr,b, Dhaka, Bangladesh (S. Nasreen, S.U. Khan, S.P. Luby, E.S. Gurley, J. Abedin, R.U. Zaman, B.M. Sohel, M. Rahman, K. Sturm-Ramirez, E. Azziz-Baumgartner)Centers for Disease Control and Prevention, Atlanta, Georgia, USA (S.P. Luby, K. Hancock, M.Z. Levine, V. Veguilla, D. Wang, C. Holiday, E. Gillis, K. Sturm-Ramirez, J.S. Bresee, T.M. Uyeki, J.M. Katz, E. Azziz-Baumgartner)Institute of Epidemiology, Disease Control and Research, Dhaka (M. Rahman)


The risk for influenza A(H5N1) virus infection is unclear among poultry workers in countries where the virus is endemic. To assess H5N1 seroprevalence and seroconversion among workers at live bird markets (LBMs) in Bangladesh, we followed a cohort of workers from 12 LBMs with existing avian influenza surveillance. Serum samples from workers were tested for H5N1 antibodies at the end of the study or when LBM samples first had H5N1 virus–positive test results. Of 404 workers, 9 (2%) were seropositive at baseline. Of 284 workers who completed the study and were seronegative at baseline, 6 (2%) seroconverted (7 cases/100 poultry worker–years). Workers who frequently fed poultry, cleaned feces from pens, cleaned food/water containers, and did not wash hands after touching sick poultry had a 7.6 times higher risk for infection compared with workers who infrequently performed these behaviors. Despite frequent exposure to H5N1 virus, LBM workers showed evidence of only sporadic infection.
Human infections and deaths caused by highly pathogenic avian influenza A (H5N1) viruses in several countries (1); by A(H9N2) virus in Bangladesh (2); and by A(H7N2), A(H7N9), A(H9N2), and A(H10N8) viruses in China (35) reflect the persistent public health threat posed by different avian influenza A virus subtypes. Subtype H5N1 virus remains endemic among poultry in Bangladesh, China, Egypt, Indonesia, and Vietnam (6). Among these countries the first human cases of H5N1 virus were identified in China and Vietnam during 2003 (1). The seroprevalence of antibodies against H5N1 virus among poultry workers was 0%–4% in Bangladesh, China, Indonesia, and Vietnam during 2001–2009 (713); published data on seroprevalence among poultry workers in Egypt are not available. Beyond the countries where H5N1 is endemic, 0%–10% seroprevalence has been reported among poultry workers in Nigeria; South Korea; Thailand; and Hong Kong, China (1417). The incidence of H5N1 virus infection among occupationally exposed populations has not been determined in countries where the virus is endemic or nonendemic.
In Bangladesh, a country with a population density of 964/km2 and 257 million poultry (18,19), H5N1 virus infection was first detected among poultry in 2007. By the end of 2013, the country had reported 549 outbreaks among poultry to the World Organisation for Animal Health (20). The first human case of H5N1 virus infection in Bangladesh was identified during 2008 (21). Live bird markets (LBMs) are often associated with poultry-to-human transmission of H5N1 virus (22). For example, butchering and exposure to sick poultry were associated with detection of H5 antibody among LBM workers in Hong Kong (17). In one study, workers from 16 LBMs in Bangladesh were rarely observed using personal protective equipment (PPE) or washing their hands during the handling of poultry, suggesting a high likelihood of exposures to H5N1 virus (23). Data are limited on the risk for avian influenza A virus infections among poultry workers in Bangladesh (7).
Seroprevalence studies among humans yield information about how many persons have serologic evidence of infection at a certain point and time, but they do not provide information about when people became infected or the risk for infection with prolonged exposures to contaminated animals or environments. Studies designed to estimate the rate of seroconversion of antibodies to H5N1 virus among poultry workers may also help elucidate the risks of poultry-to-human transmission of H5N1 virus in countries, such as Bangladesh, where H5N1 virus is endemic among poultry. Such information may help public health officials develop, prioritize, and reinforce prevention and control strategies. During 2009–2010, a total of 61 H5N1 outbreaks, resulting in the culling of 220,432 birds, were reported among poultry in Bangladesh (24); no human cases were identified during this period. We followed a cohort of LBM workers in Bangladesh to determine the seroprevalence of antibodies to H5N1 virus, the incidence of seroconversion, and risk factors for poultry-to-human transmission of H5N1 virus.

Dr. Nasreen works on respiratory infection research at the Centre for Communicable Diseases, icddr,b. Her research area of interest is infectious disease epidemiology, including prevention and control in low-income countries.


We thank the field staff and all study participants for their contribution to the study. We also acknowledge the contribution of Yaohui Bai for technical assistance and Dorothy Southern for providing support with the scientific writing and clarity of this manuscript. icddr,b acknowledges with gratitude the commitment of CDC to its research efforts.
This research study was funded by the CDC through their cooperative agreement with icddr,b (grant no. 1-U01-CI000298). icddr,b is thankful to the governments of Australia, Bangladesh, Canada, Sweden, and the United Kingdom for providing core/unrestricted support.


  1. World Health Organization. Cumulative number of confirmed human cases for avian influenza A/(H5N1) reported to WHO, 2003–2014 [cited 2014 Dec 7]. http://www.who.int/influenza/human_animal_interface/EN_GIP_20131008CumulativeNumberH5N1cases.pdf
  2. icddr,b. Outbreak of mild respiratory disease caused by H5N1 and H9N2 infections among young children in Dhaka, Bangladesh, 2011. Health and Science Bulletin. 2011;9:512.
  3. World Health Organization. WHO risk assessment. Human infections with avian influenza A (H7N9) virus. 2014 Feb 28 [cited 2014 Mar 1].http://www.who.int/influenza/human_animal_interface/influenza_h7n9/140225_H7N9RA_for_web_20140306FM.pdf?ua=1
  4. World Health Organization. Influenza at the human-animal interface. Summary and assessment as of 24 January 2014 [cited 2014 Feb 20].http://www.who.int/influenza/human_animal_interface/Influenza_Summary_IRA_HA_interface_24January14.pdf?ua=1
  5. World Health Organization. Avian influenza A (H10N8). World Health Organization (WHO), Western Pacific Region [cited 2014 Feb 20].http://www.wpro.who.int/china/mediacentre/factsheets/h10n8/en/
  6. Food and Agriculture Organization of the United Nations, World Organisation for Animal Health, World Health Organization. FAO-OIE-WHO technical update: current evolution of avian influenza H5N1 viruses [cited 2014 Dec 27].http://www.who.int/influenza/human_animal_interface/tripartite_notes_H5N1.pdf
  7. Nasreen SUddin Khan SAzziz-Baumgartner EHancock KVeguilla VWang DSeroprevalence of antibodies against highly pathogenic avian influenza A (H5N1) virus among poultry workers in Bangladesh, 2009. PLoS ONE2013;8:e73200DOIPubMed
  8. Lu CYLu JHChen WQJiang LFTan BYLing WHPotential infections of H5N1 and H9N2 avian influenza do exist in Guangdong populations of China. Chin Med J (Engl)2008;121:20503 .PubMed
  9. Wang MFu C-XZheng B-JAntibodies against H5 and H9 avian influenza among poultry workers in China. N Engl J Med2009;360:25834.DOIPubMed
  10. Huo XZu RQi XQin YLi LTang FSeroprevalence of avian influenza A (H5N1) virus among poultry workers in Jiangsu Province, China: an observational study. BMC Infect Dis2012;12:93DOIPubMed
  11. Santhia KRamy AJayaningsih PSamaan GPutra AAGDibia NAvian influenza A H5N1 infections in Bali Province, Indonesia: a behavioral, virological and seroepidemiological study. Influenza Other Respir Viruses. 2009;3:81–9.
  12. Schultsz CDung NVHai LTHa DQPeiris JSMLim WPrevalence of antibodies against avian influenza A (H5N1) virus among cullers and poultry workers in Ho Chi Minh City, 2005. PLoS ONE2009;4:e7948DOIPubMed
  13. Uyeki TMNguyen DCRowe TLu XHu-Primmer JHuynh LPSeroprevalence of antibodies to avian influenza A (H5) and A (H9) viruses among market poultry workers, Hanoi, Vietnam, 2001. PLoS ONE2012;7:e43948 . DOIPubMed
  14. Ortiz JRKatz MAMahmoud MNAhmed SBawa SIFarnon ECLack of evidence of avian-to-human transmission of avian influenza A (H5N1) virus among poultry workers, Kano, Nigeria, 2006. J Infect Dis2007;196:168591DOIPubMed
  15. Kwon DLee J-YChoi WChoi J-HChung Y-SLee N-JAvian influenza A (H5N1) virus antibodies in poultry cullers, South Korea, 2003–2004.Emerg Infect Dis2012;18:9868.PubMed
  16. Hinjoy SPuthavathana PLaosiritaworn YLimpakarnjanarat KPooruk PChuxnum TLow frequency of infection with avian influenza virus (H5N1) among poultry farmers, Thailand, 2004. Emerg Infect Dis2008;14:499501DOIPubMed
  17. Bridges CBLim WHu-Primmer JSims LFukuda KMak KHRisk of influenza A (H5N1) infection among poultry workers, Hong Kong, 1997–1998.J Infect Dis2002;185:100510DOIPubMed
  18. Directorate General of Health Services Bangladesh. 2nd National Avian and Pandemic Influenza Preparedness and Response Plan, Bangladesh, 2009–2011 [cited 2010 Feb 12]. http://oldweb.dghs.gov.bd/bn/important-documents-software/category/7-2012-07-09-07-43-26?download=6:2nd-national-avian-and-pandemic-influenza-preparedness-and-response-plan-bangladesh
  19. Bangladesh Bureau of Statistics2011 Population and housing census: preliminary results 2011 [cited 2011 Dec 20].http://www.bbs.gov.bd/WebTestApplication/userfiles/Image/BBS/PHC2011Preliminary%20Result.pdf
  20. World Organization for Animal Health. Update on highly pathogenic avian influenza in animals (type H5 and H7): Follow-up report no. 43 (final report) [cited 2013 Jun 27]. http://www.oie.int/wahis_2/public%5C.%5Ctemp%5Creports/en_fup_0000014568_20131223_145541.pdf
  21. Brooks WAAlamgir ASMSultana RIslam MSRahman MFry AAvian influenza virus A (H5N1), detected through routine surveillance, in child, Bangladesh. Emerg Infect Dis2009;15:13113DOIPubMed
  22. Wan X-FDong LLan YLong L-PXu CZou SIndications that live poultry markets are a major source of human H5N1 influenza virus infection in China. J Virol2011;85:134328DOIPubMed
  23. Bangladesh UNICEF. icddr,b. Evaluation of avian influenza communication for development initiative—improving biosecurity in live bird markets. Pre-intervention assessment report. Dhaka (Bangladesh): United Nations Children Fund; 2013.
  24. World Organization for Animal Health. Update on highly pathogenic avian influenza in animals (type H5 and H7) [cited 2013 Jan 5].http://www.oie.int/animal-health-in-the-world/update-on-avian-influenza/2004/
  25. Khan SURahman MGurley ESMikolon ARahman MZHossain MJLive bird market environmental sampling: an efficient tool for poultry influenza surveillance. Am J Trop Med Hyg2011;85(Suppl 6):285 .PubMed
  26. icddr,b. Avian influenza virus surveillance at live bird markets in Bangladesh, 2007–2012. Health and Science Bulletin. 2013;11:816.
  27. Centers for Disease Control and Prevention. CDC protocol of realtime RTPCR for influenza A(H1N1) [cited 2012 Feb 12].http://www.who.int/csr/resources/publications/swineflu/CDCRealtimeRTPCR_SwineH1Assay-2009_20090430.pdf
  28. Rowe TAbernathy RAHu-Primmer JThompson WWLu XLim WDetection of antibody to avian influenza A (H5N1) virus in human serum by using a combination of serologic assays. J Clin Microbiol1999;37:93743 .PubMed
  29. World Health Organization. Serological diagnosis of influenza by microneutralization assay [cited 2011 Jan 18].http://www.who.int/influenza/gisrs_laboratory/2010_12_06_serological_diagnosis_of_influenza_by_microneutralization_assay.pdf
  30. Stephenson IWood JMNicholson KGCharlett AZambon MCDetection of anti-H5 responses in human sera by HI using horse erythrocytes following MF59-adjuvanted influenza A/Duck/Singapore/97 vaccine. Virus Res2004;103:915DOIPubMed
  31. Kaiser HA second generation little jiffy. Psychometrika1970;35:40115DOI
  32. Bursac ZGauss CHWilliams DKHosmer DWPurposeful selection of variables in logistic regression. Source Code Biol Med2008;3:17.DOIPubMed
  33. Wooldridge JM. Econometric analysis of cross section and panel data. 2nd ed. Cambridge (MA): MIT Press; 2010.
  34. Buchy PVong SChu SGarcia J-MHien TTHien VMKinetics of neutralizing antibodies in patients naturally infected by H5N1 virus. PLoS ONE.2010;5:e10864DOIPubMed
  35. Park AWGlass KDynamic patterns of avian and human influenza in East and Southeast Asia. Lancet Infect Dis2007;7:5438 and. DOIPubMed
  36. Wang MDi BZhou D-HZheng B-JJing HLin Y-PFood markets with live birds as source of avian influenza. Emerg Infect Dis.2006;12:17735.PubMed
  37. World Health Organization. Protection of individuals with high poultry contact in areas affected by avian influenza H5N1: consolidation of pre-existing guidance [cited 2008 Mar 15]. http://www.who.int/influenza/resources/documents/guidance_protection_h5n1_02_2008/en/
  38. Rimi NASultana RKhan SNasreen SPuri AAlamgir ASMBiosecurity conditions and biosafety practices in the live bird markets of Dhaka city, Bangladesh, 2012. In: Abstracts of the Options for the Control of Influenza VIII; Cape Town, South Africa; 2013 Sep 5–10. Abstract P2-475. London: International Society for Influenza and Other Respiratory Virus Diseases; 2013.
  39. icddr,b. The first fatal human infection with highly pathogenic avian influenza A (H5N1) virus detected in Bangladesh. Health and Science Bulletin.2013;11:16.
  40. Uyeki TMBresee JSDetecting human-to-human transmission of avian influenza A (H5N1). Emerg Infect Dis2007;13:196971DOIPubMed



Technical Appendices

Suggested citation for this article: Nasreen S, Khan SU, Luby SP, Gurley ES, Abedin J, Zaman RU, et al. Highly pathogenic avian influenza A(H5N1) virus infection among workers at live bird markets, Bangladesh, 2009–2010. Emerg Infect Dis. 2015 Apr [date cited].http://dx.doi.org/10.3201/eid2104.141281
DOI: 10.3201/eid2104.141281

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