A Decade of Avian Influenza in Bangladesh: Where Are We Now?
Abstract
:1. Background
2. Clades of HPAI H5N1 Detected in Bangladesh
3. Surveillance
3.1. Poultry Surveillance
3.2. Surveillance for Human Infection with AIVs
4. Biosecurity
4.1. Backyard Poultry Sector
4.2. Commercial Poultry Sector
4.3. Live Bird Market Sector
5. Vaccination
6. Other Research
7. Avian Influenza Policy
8. Discussion
9. Future Directions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- OIE. World Animal Health Information Database (WAHIS Interface) [Internet]. 2013. Available online: http://www.oie.int/wahis_2/public/wahid.php/Countryinformation/Diseasetimeseries#charts (accessed on 3 January 2019).
- Loth, L.; Gilbert, M.; Osmani, M.G.; Kalam, A.M.; Xiao, X. Risk factors and clusters of Highly Pathogenic Avian Influenza H5N1 outbreaks in Bangladesh. Prev Vet Med. 2010, 96, 104–113. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Negovetich, N.J.; Feeroz, M.M.; Jones-Engel, L.; Walker, D.; Alam, S.M.; Hasan, K.; Seiler, P.; Ferguson, A.; Friedman, K.; Barman, S.; et al. Live bird markets of Bangladesh: H9N2 viruses and the near absence of highly pathogenic H5N1 influenza. PLoS ONE 2011, 6, e19311. [Google Scholar] [CrossRef] [PubMed]
- Giasuddin, M.; Ali, M.Z.; Karim, M.R. Emergence of novel H5N6 avian influenza virus in Bangladesh. In Proceedings of the 24th Annual Scientific Conference of Bangladesh Society for Veterinary Education and Research (BSVER), Mymensingh, Bangladesh, 24–25 March 2018. [Google Scholar]
- OIE. Follow-Up Report No 43 (Final Report) 2013. Available online: http://www.oie.int/wahis_2/public%5C..%5Ctemp%5Creports/en_fup_0000014568_20131223_145541.pdf (accessed on 11 May 2019).
- Haider, N.; Sturm-Ramirez, K.; Khan, S.; Rahman, M.; Sarkar, S.; Poh, M.; Shivaprasad, H.; Kalam, M.; Paul, S.; Karmakar, P. Unusually high mortality in waterfowl caused by highly pathogenic avian influenza A (H5N1) in Bangladesh. Transbound Emerg. Dis. 2017, 64, 144–156. [Google Scholar] [CrossRef] [PubMed]
- Khan, S.U.; Berman, L.; Haider, N.; Gerloff, N.; Rahman, M.Z.; Shu, B.; Rahman, M.; Dey, T.K.; Davis, T.C.; Das, B.C.; et al. Investigating a crow die-off in January-February 2011 during the introduction of a new clade of highly pathogenic avian influenza virus H5N1 into Bangladesh. Arch. Virol. 2013, 159, 509–518. [Google Scholar] [CrossRef] [PubMed]
- Sarkar, S.; Khan, S.U.; Mikolon, A.; Rahman, M.Z.; Abedin, J.; Zeidner, N.; Sturm-Ramirez, K.; Luby, S.P. An epidemiological study of avian influenza A (H5) virus in nomadic ducks and their raising practices in northeastern Bangladesh, 2011–2012. Influenza Other Respir. Viruses 2017, 11, 275–282. [Google Scholar] [CrossRef]
- World Health Organization. Cumulative Number of Confirmed Human Cases for Avian Influenza A (H5N1) Reported to WHO, 2003–2015: WHO. 2015. Available online: http://www.who.int/influenza/human_animal_interface/EN_GIP_20150303cumulativeNumberH5N1cases.pdf?ua=1 (accessed on 11 March 2019).
- Chakraborty, A.; Rahman, M.; Hossain, M.J.; Khan, S.U.; Haider, M.S.; Sultana, R.; Ali Rimi, N.; Islam, M.S.; Haider, N.; Islam, A. Mild respiratory illness among young children caused by highly pathogenic avian influenza A (H5N1) virus infection in Dhaka, Bangladesh, 2011. J. Infect. Dis. 2017, 216, S520–S528. [Google Scholar] [CrossRef] [PubMed]
- Sturm-Ramirez, K.M.; Afreen, S.; Rahman, M.Z.; Chowdhury, S.; Khan, S.U.; Rahman, M.M.; Sharif, A.R.; Rahman, M.; Azim, T.; Nasreen, S.; et al. Avian influenza at the animal-human interface: Investigations among poultry workers in live bird markets in Dhaka city, Bangladesh, 2012–2013. In Proceedings of the Options for the Control of Influenza VIII Conference, Cape Town, South Africa, 5–10 September 2013. [Google Scholar]
- Sims, L.D. Intervention strategies to reduce the risk of zoonotic infection with avian influenza viruses: Scientific basis, challenges and knowledge gaps. Influenza Other Respir Viruses 2013, 7, 15–25. [Google Scholar] [CrossRef]
- Food and Agriculture Organization. Approaches to Controlling, Preventing and Eliminating H5N1 Highly Pathogenic Avian Influenza in Endemic Countries. 2011. Available online: http://www.fao.org/3/i2150e/i2150e00.htm (accessed on 11 March 2019).
- Jackson, S.; Van Hoeven, N.; Chen, L.M.; Maines, T.R.; Cox, N.J.; Katz, J.M.; Donis, R.O. Reassortment between avian H5N1 and human H3N2 influenza viruses in ferrets: A public health risk assessment. J. Virol. 2009, 83, 8131–8140. [Google Scholar] [CrossRef]
- World Health Organization. Regional Influenza Pandemic Preparedness Plan (2006–2008); WHO Regional Office for South-East Asia, WHO: Geneva, Switzerland, 2006. [Google Scholar]
- Herfst, S.; Mok, C.K.; van den Brand, J.M.; van der Vliet, S.; Rosu, M.E.; Spronken, M.I.; Yang, Z.; de Meulder, D.; Lexmond, P.; Bestebroer, T.M. Human clade 2.3. 4.4 A/H5N6 influenza virus lacks mammalian adaptation markers and does not transmit via the airborne route between ferrets. Msphere 2018, 3, e00405-17. [Google Scholar] [CrossRef]
- Turner, J.C.; Feeroz, M.M.; Hasan, M.K.; Akhtar, S.; Walker, D.; Seiler, P.; Barman, S.; Franks, J.; Jones-Engel, L.; McKenzie, P. Insight into live bird markets of Bangladesh: An overview of the dynamics of transmission of H5N1 and H9N2 avian influenza viruses. Emerg. Microbes Infect. 2017, 6, 1–8. [Google Scholar] [CrossRef]
- Government of Bangladesh, Directorate General of Health Services. National Avian Influenza and Human Pandemic Influenza Preparedness and Response Plan Bangladesh; Directorate General of Health Services: Dhaka, Bangladesh, 2006.
- Islam, M.R.; Haque, M.E.; Giasuddin, M.; Chowdhury, E.H.; Samad, M.A.; Parvin, R.; Nooruzzaman, M.; Rahman, M.M.; Monoura, P. New Introduction of Clade 2.3.2.1 Avian Influenza Virus (H5N1) into Bangladesh. Transbound Emerg. Dis. 2011, 59, 460–463. [Google Scholar] [CrossRef] [PubMed]
- Haque, M.; Giasuddin, M.; Chowdhury, E.; Islam, M. Molecular evolution of H5N1 highly pathogenic avian influenza viruses in Bangladesh between 2007 and 2012. Avian Pathol. 2014, 43, 183–194. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Parvin, R.; Kamal, A.H.; Haque, M.E.; Chowdhury, E.H.; Giasuddin, M.; Islam, M.R.; Vahlenkamp, T.W. Genetic characterization of highly pathogenic H5N1 avian influenza virus from live migratory birds in Bangladesh. Virus Genes 2014, 49, 438–448. [Google Scholar] [CrossRef] [PubMed]
- Marinova-Petkova, A.; Feeroz, M.M.; Alam, S.R.; Hasan, M.K.; Akhtar, S.; Jones-Engel, L.; Walker, D.; McClenaghan, L.; Rubrum, A.; Franks, J. Multiple introductions of highly pathogenic avian influenza H5N1 viruses into Bangladesh. Emerg. Microbes Infect. 2014, 3, 1–14. [Google Scholar] [CrossRef] [PubMed]
- Marinova-Petkova, A.; Shanmuganatham, K.; Feeroz, M.M.; Jones-Engel, L.; Hasan, M.K.; Akhtar, S.; Turner, J.; Walker, D.; Seiler, P.; Franks, J. The continuing evolution of H5N1 and H9N2 influenza viruses in Bangladesh between 2013 and 2014. Avian Dis. 2015, 60, 108–117. [Google Scholar] [CrossRef] [PubMed]
- Barman, S.; Marinova-Petkova, A.; Hasan, M.K.; Akhtar, S.; El-Shesheny, R.; Turner, J.C.; Franks, J.; Walker, D.; Seiler, J.; Friedman, K. Role of domestic ducks in the emergence of a new genotype of highly pathogenic H5N1 avian influenza A viruses in Bangladesh. Emerg. Microbes Infect. 2017, 6, 1–13. [Google Scholar] [CrossRef] [Green Version]
- Shaman, J.; Kohn, M. Absolute humidity modulates influenza survival, transmission, and seasonality. Proc. Natl. Acad. Sci. USA 2009, 106, 3243–3248. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- World Bank. Implementation Completion and Results Report (IDA-43400 TF-90662) on a Credit in the Amount of SDR 10.5 Million (US $16.0 Million Equivalent) to the People’s Republic of Bangladesh for an Avian Influenza Preparedness and Response Project under the Global Program for Avian Influenza and Human Pandemic Preparedness and Response; The World Bank: Washington, DC, USA, 2013. [Google Scholar]
- Khan, S.U.; Gurley, E.S.; Gerloff, N.; Rahman, M.Z.; Simpson, N.; Rahman, M.; Haider, N.; Chowdhury, S.; Balish, A.; Zaman, R.U. Avian influenza surveillance in domestic waterfowl and environment of live bird markets in Bangladesh, 2007–2012. Sci Rep. 2018, 8, 9396. [Google Scholar] [CrossRef]
- Nasreen, S.; Khan, S.U.; Luby, S.P.; Gurley, E.S.; Abedin, J.; Zaman, R.U.; Sohel, B.M.; Rahman, M.; Hancock, K.; Levine, M.Z.; et al. Highly Pathogenic Avian Influenza A(H5N1) Virus Infection among Workers at Live Bird Markets, Bangladesh, 2009–2010. Emerg. Infect. Dis. 2015. [Google Scholar] [CrossRef]
- Zaman, R.U.; Alamgir, A.; Rahman, M.; Azziz-Baumgartner, E.; Gurley, E.S.; Sharker, M.A.Y.; Brooks, W.A.; Azim, T.; Fry, A.M.; Lindstrom, S. Influenza in outpatient ILI case-patients in national hospital-based surveillance, Bangladesh, 2007–2008. PLoS ONE 2009, 4, e8452. [Google Scholar] [CrossRef]
- Samad, M.A.; Hasan, Z.; Karim, M.R.; Giasuddin, M.; Hossain, M.; Pramanik, P.; Belot, G.; VonDobschuetz, S.; Debnath, N.C.; Brum, E. Novel sink environmental surveillance method for detection of avian influenza viruses in live bird markets in Dhaka, Bangladesh. In Proceedings of the One Health EcoHealth, Melbourne, Australia, 3–7 December 2016. [Google Scholar]
- Zihadi, M.A.H.; Vahlenkamp, T.W. Short Review on Vaccination and Surveillance on Avian Influenza in Bangladesh: Existing Gaps and Recent Insights. Bangladesh J. Infect. Dis. 2017, 4, 48–51. [Google Scholar] [CrossRef]
- Islam, A.; Hill, N.; Mikolon, A.; Sturm-Ramirez, K.; Rahman, M.; Paul, S.; Islam, A.; Hossain, K.; Rahman, M.; Khan, S.; et al. Avian influenza A viruses in wild birds and domestic ducks in Bangladesh. In Proceedings of the Options for the Control of Influenza VIII Conference, Cape Town, South Africa, 5–10 September 2013. [Google Scholar]
- Hassan, M.M.; Hoque, M.A.; Debnath, N.C.; Yamage, M.; Klaassen, M. Are poultry or wild birds the main reservoirs for avian influenza in Bangladesh? Ecohealth 2017, 14, 490–500. [Google Scholar] [CrossRef] [PubMed]
- Hassan, M.M.; Hoque, M.A.; Ujvari, B.; Klaassen, M. Live bird markets in Bangladesh as a potentially important source for Avian Influenza Virus transmission. Prev. Vet. Med. 2018, 156, 22–27. [Google Scholar] [CrossRef] [PubMed]
- Biswas, P.; Giasuddin, M.; Chowdhury, P.; Barua, H.; Debnath, N.; Yamage, M. Incidence of contamination of live bird markets in Bangladesh with influenza A virus and subtypes H5, H7 and H9. Transbound Emerg. Dis. 2018, 65, 687–695. [Google Scholar] [CrossRef]
- Hassan, M.Z.; Afreen, S.; Nasreen, S.; Mamun, A.A.; Rahman, M.Z.; Rahman, M.; Luby, S.P.; Kafi, M.A.H.; Chowdhury, S.; Azim, T.; et al. Incidence of avian-influenza virus exposure and associated risk behavior among a cohort of live bird market poultry workers, Bangladesh: 2012–2015. In Proceedings of the Options IX for the Control of Inlfuenza, Chicago, IL, USA, 24–28 August 2016. [Google Scholar]
- Institute of Epidemiology Disease Control and Research. Ongoing Surveillance at IEDCR 2012. Available online: http://www.iedcr.gov.bd/index.php/surveillance (accessed on 28 December 2018).
- Kelly, T.R.; Hawkins, M.G.; Sandrock, C.E.; Boyce, W.M. A review of highly pathogenic avian influenza in birds, with an emphasis on Asian H5N1 and recommendations for prevention and control. J. Avian Med. Surg. 2008, 22, 1–16. [Google Scholar] [CrossRef] [PubMed]
- Food and Agriculture Organization. The Global Strategy for Prevention and Control of H5N1 Highly Pathogenic Avian Influenza; FAO: Rome, Italy, 2007. [Google Scholar]
- Food and Agriculture Organization. Biosecurity for Highly Pathogenic Avian Influenza; FAO: Rome, Italy, 2008. [Google Scholar]
- The World Bank. Agriculture & Rural Development 2013. Available online: http://data.worldbank.org/topic/agriculture-and-rural-development?display=graph (accessed on 15 April 2019).
- Avian Influenza Knowledge, Attitude and Practice (KAP) Survey among the General Public and Poultry Farmers in Bangladesh; UNICEF Bangladesh: Dhaka, Bangladesh, 2007.
- Sultana, R.; Nahar, N.; Rimi, N.A.; Azad, S.; Islam, M.S.; Gurley, E.S.; Luby, S.P. Backyard poultry raising in Bangladesh: A valued resource for the villagers and a setting for zoonotic transmission of avian influenza. A qualitative study. Rural Remote Health 2012, 12, 1927. [Google Scholar] [PubMed]
- Rimi, N.A.; Sultana, R.; Ishtiak-Ahmed, K.; Rahman, M.Z.; Hasin, M.; Islam, M.S.; Azziz-Baumgartner, E.; Nahar, N.; Gurley, E.S.; Luby, S.P. Understanding the failure of a behavior change intervention to reduce risk behaviors for avian influenza transmission among backyard poultry raisers in rural Bangladesh: A focused ethnography. BMC Public Health 2016, 16, 858. [Google Scholar] [CrossRef]
- Popy, F.Y.; Chowdhury, Q.M.K.; Alam, S.; Roy, S.; Dipta, P.M.; Ahmed, J. Backyard Poultry Management and Production System at Barlekha Upazila, Moulvibazar, Bangladesh. Int. J. Sci. Bus. 2018, 2, 90–100. [Google Scholar]
- SAPPLPP. Combating Bird Flu through Bio-security Measures at Farm and Community Level: Evidence from Bangladesh; Good Practice Note: Delhi, India, 2010. [Google Scholar]
- Conan, A.; Goutard, F.L.; Sorn, S.; Vong, S. Biosecurity measures for backyard poultry in developing countries: A systematic review. BMC Vet. Res. 2012, 8, 240. [Google Scholar] [CrossRef]
- Sultana, R.; Rimi, N.A.; Azad, S.; Islam, M.S.; Khan, M.S.; Gurley, E.S.; Nahar, N.; Luby, S.P. Bangladeshi backyard poultry raisers‘ perceptions and practices related to zoonotic transmission of avian influenza. J. Infect. Dev. Ctries. 2012, 6, 156–165. [Google Scholar] [CrossRef]
- Shanta, I.S.; Hasnat, M.A.; Zeidner, N.; Gurley, E.S.; Azziz-Baumgartner, E.; Sharker, M.A.; Hossain, K.; Khan, S.U.; Haider, N.; Bhuyan, A.A.; et al. Raising backyard poultry in rural Bangladesh: Financial and nutritional benefits, but persistent risky practices. Transbound Emerg. Dis. 2016, 64, 1454–1464. [Google Scholar] [CrossRef] [PubMed]
- Government of Bangladesh. Bird Flu: What You Need to Know and Do 2007. Available online: http://www.mofl.gov.bd/bird_flu.aspx (accessed on 12 May 2019).
- UNICEF Bangladesh. Our Work-Avian Influenza 2009. Available online: https://www.unicef.org/bangladesh/activities_4992.html (accessed on 18 October 2018).
- FAO-ECTAD. Teacher Training Programme for Avian Influenza Outbreak Reporting; Emergency Centre for Transboundary Diseases: Dar es Salaam, Tanzania, 2009. [Google Scholar]
- Rimi, N.A.; Sultana, R.; Fahad, M.H.; Mortaza, S.M.G.; Haider, N.; Sturm-Ramirez, K.; Luby, S.P. Safe home slaughtering recommendations to reduce human exposure to airborne transmission of avian influenza viruses among two Bangladeshi rural communities. In Proceedings of the Options for the Control of Influenza IX, Chicago, IL, USA, 24–28 August 2016. [Google Scholar]
- Hill, E.M.; House, T.; Dhingra, M.S.; Kalpravidh, W.; Morzaria, S.; Osmani, M.G.; Brum, E.; Yamage, M.; Kalam, M.A.; Prosser, D.J. The impact of surveillance and control on highly pathogenic avian influenza outbreaks in poultry in Dhaka division, Bangladesh. Biorxiv 2018, 193177. [Google Scholar] [CrossRef] [PubMed]
- Chowdhury, E.H. End-of-Assignment Report: Review Existing Environmental Safeguard and Biosafety of FDILs, Live Bird Market and Demo and Adapter Farms; Food and Agriculture Organization: Dar es Salaam, Tanzania, 2013. [Google Scholar]
- Evaluation of Avian Influenza Communication for Development Initiative- Improving Biosecurity in Live Bird Markets: Lessons Learned Report; Unicef: Dhaka, Bangladesh, 2013.
- Rimi, N.A.; Sultana, R.; Muhsina, M.; Uddin, B.; Haider, N.; Nahar, N.; Zeidner, N.; Sturm-Ramirez, K.; Luby, S.P. Biosecurity conditions in small commercial chicken farms, Bangladesh 2011–2012. Ecohealth 2017, 14, 244–258. [Google Scholar] [CrossRef] [PubMed]
- Bertran, K.; Clark, A.; Swayne, D.E. Mitigation strategies to reduce the generation and transmission of airborne highly pathogenic avian influenza virus particles during processing of infected poultry. Int. J. Hyg. Environ. Health 2018, 221, 893–900. [Google Scholar] [CrossRef] [PubMed]
- Haider, M.; Applebaum, B. Disease Management of Avian Influenza H5N1 in Bangladesh—A Focus on Maintaining Healthy Live Birds; Smigorski, D.K., Ed.; Health Management—Different Approaches and Solutions; Intechopen: London, UK, 2011; pp. 259–270. [Google Scholar]
- Mondal, S.P.; Tardif-Douglin, D.; Ryan-Silva, R.; Magnani, R. Controlling highly pathogenic avian influenza, Bangladesh. Emerg. Infect. Dis. 2012, 18, 2083–2085. [Google Scholar] [CrossRef]
- Walking the Talk Regionally; FAO-ECTAD: Dar es Salaam, Tanzania, 2011.
- Biswas, P.; Giasuddin, M.; Nath, B.; Islam, M.; Debnath, N.; Yamage, M. Biosecurity and circulation of influenza A (H5N1) virus in live-bird markets in Bangladesh, 2012. Transbound Emerg. Dis. 2015, 64, 883–891. [Google Scholar] [CrossRef]
- Islam, M.R.; Rahman, M.M.; Chowdhury, E.H.; Das, P.M. Community engagement in biosecurity (CEB) for the prevention of infectious diseases of poultry based on epidemiological risk analysis. In Proceedings of the BAURES Research Review Workshop, Mymensingh, Bangladesh, 15–18 March 2018. [Google Scholar]
- Rimi, N.A.; Fahad, M.H.; Mortaza, S.M.G.; Mahmud, A.A.; Islam, M.A.; Hassan, M.Z.; Sultana, R.; Sturm-Ramirez, K. Piloting workstations to improve hygiene practices among poultry workers during poultry processing in a live bird market in Bangladesh. In Proceedings of the 66th Annual Meeting of American Society of Tropical Medicine and Hygiene (ASTMH), Baltimore, MD, USA, 5–9 November 2017. [Google Scholar]
- Hassan, M.Z.; Rimi, N.A.; Fahad, M.H.; Sultana, R.; Mortaza, S.M.G.; Mahmud, A.A.; Islam, M.A.; Amin, N.; Rahman, M.Z.; Sturm-Ramirez, K. Exploring the effectiveness, acceptability and feasibility of handwashing with soapy water for removal of influenza viruses from poultry workers hands in a Bangladeshi live bird market. In Proceedings of the International Conference on Emerging Infectious Diseases, Atlanta, GA, USA, 26–29 August 2018. [Google Scholar]
- Sarker, S.; Sumon, S.; Khan, M.A.; Islam, M. Knowledge, attitude and practices survey on avian influenza in three districts of Bangladesh. Bangladesh J. Vet. Med. 2016, 14, 27–36. [Google Scholar] [CrossRef]
- Department of Livestock Services. Registered Poultry Farms 2012; Government of Bangladesh: Dhaka, Bangladesh, 2012.
- Ibrahim, N.; Akhter, M.; Al Mamun, S.; Chowdhury, E.H.; Das, P.M. Bio-security in small scale poultry farms against avian influenza: Knowledge, attitude and practices. Asian J. Med. Biol. Res. 2016, 1, 670–676. [Google Scholar] [CrossRef]
- Islam, M.S.; Huque, Q.M.E. Practices of bio-security in small-scale broiler farms. Bangladesh Vet. 2007, 24, 72–78. [Google Scholar]
- Sarker, B.C.; Alam, M.A.; Rahman, M.M.; Islam, A.F.M.T.; Chowdhury, M.G.F. Waste management of commercial poultry farms in Bangladesh. J. Innov. Dev. Strategy 2009, 3, 34–37. [Google Scholar]
- Department of Livestock Services. Biosecurity Guideline for the Commercial Poultry Industry in Bangladesh; Government of Bangladesh: Dhaka, Bangladesh, 2010.
- Rashid, M.H. Poultry Trading and Farm Biosecurity Status: Introduction of Avian Influenza to Broiler Farms in Chittagong, Bangladesh. Master’s Thesis, Chittagong Veterinary and Animal Sciences University (CVASU), Chittagong, Bangladesh, 2018. [Google Scholar]
- Rahman, M.M.; Badhy, S.C.; Islam, M.T.; Osmani, M.G.; Chowdhury, E.H.; Das, P.M.; Islam, M.R. (Eds.) A baseline survey on biosecurity practices of layer farmers in Bhaluka and Sakhipur upazila of Bangladesh. In Proceedings of the Tenth International Poultry Show and Seminar, WPSA-BB, Dhaka, Bangladesh, 2 March 2017. [Google Scholar]
- Rimi, N.A.; Sultana, R.; Ishtiak-Ahmed, K.; Haider, N.; Azziz-Baumgartner, E.; Nahar, N.; Luby, S.P. Where backyard poultry raisers seek care for sick poultry: Implications for avian influenza prevention in Bangladesh. BMC Public Health 2018, 18, 969. [Google Scholar] [CrossRef] [PubMed]
- Laxminarayan, R.; Duse, A.; Wattal, C.; Zaidi, A.K.; Wertheim, H.F.; Sumpradit, N.; Vlieghe, E.; Hara, G.L.; Gould, I.M.; Goossens, H.; et al. Antibiotic resistance-the need for global solutions. Lancet. Infect. Dis. 2013, 13, 1057–1098. [Google Scholar] [CrossRef]
- Dolberg, F. Poultry Sector Country Review: Bangladesh; FAO: Dar es Salaam, Tanzania, 2008. [Google Scholar]
- Institute of Epidemiology Disease Control and Research. Fourth H5N1 human case in Bangladesh 2012. Available online: http://www.iedcr.org/pdf/files/influenza/Fourth-H5N1-human-case-in-Bangladesh.pdf (accessed on 11 May 2019).
- Institute of Epidemiology Disease Control and Research. Fifth and Sixth H5N1 human case in Bangladesh 2012. Available online: http://www.iedcr.org/pdf/files/influenza/Fifth_and_Sixth_H5N1.pdf (accessed on 15 March 2019).
- Sirajul Islam, M.; Ali, M.Y.; Kabir, M.H.; Al- Rahman, M.O.; Akter, M.S.; Karim, M.R.; Islam, K.T.; Majumder, M.K.H. Assessment of present bio-security practices in live poultry markets in some selected areas of Bangladesh. Asian Australas J. Biosci. Biotechnol. 2016, 1, 333–337. [Google Scholar]
- Kim, Y.; Biswas, P.K.; Giasuddin, M.; Hasan, M.; Mahmud, R.; Chang, Y.-M.; Essen, S.; Samad, M.A.; Lewis, N.S.; Brown, I.H. Prevalence of Avian Influenza A (H5) and A (H9) Viruses in Live Bird Markets, Bangladesh. Emerg. Infect. Dis. 2018, 24, 2309–2316. [Google Scholar] [CrossRef] [PubMed]
- Sayeed, M.A.; Smallwood, C.; Imam, T.; Mahmud, R.; Hasan, R.B.; Hasan, M.; Anwer, M.S.; Rashid, M.H.; Hoque, M.A. Assessment of hygienic conditions of live bird markets on avian influenza in Chittagong metro, Bangladesh. Prev. Vet. Med. 2017, 142, 7–15. [Google Scholar] [CrossRef] [PubMed]
- Fournie, G.; Guitian, F.; Mangtani, P.; Ghani, A. Impact of the implementation of rest days in live bird markets on the dynamics of H5N1 highly pathogenic avian influenza. J. R. Soc. Interface 2011, 8, 1079–1089. [Google Scholar] [CrossRef] [PubMed]
- Kash, J.C.; Tumpey, T.M.; Proll, S.C.; Carter, V.; Perwitasari, O.; Thomas, M.J.; Basler, C.F.; Palese, P.; Taubenberger, J.K.; García-Sastre, A. Genomic analysis of increased host immune and cell death responses induced by 1918 influenza virus. Nature 2006, 443, 578. [Google Scholar] [CrossRef] [PubMed]
- Van der Goot, J.; Koch, G.; De Jong, M.; Van Boven, M. Quantification of the effect of vaccination on transmission of avian influenza (H7N7) in chickens. Proc. Natl. Acad. Sci. USA 2005, 102, 18141–18146. [Google Scholar] [CrossRef] [Green Version]
- Liu, Q.; Mena, I.; Ma, J.; Bawa, B.; Krammer, F.; Lyoo, Y.S.; Lang, Y.; Morozov, I.; Mahardika, G.N.; Ma, W. Newcastle disease virus-vectored H7 and H5 live vaccines protect chickens from challenge with H7N9 or H5N1 avian influenza viruses. J. Virol. 2015, 89, 7401–7408. [Google Scholar] [CrossRef]
- Magalhães, R.J.S.; Pfeiffer, D.U.; Otte, J. Evaluating the control of HPAIV H5N1 in Vietnam: Virus transmission within infected flocks reported before and after vaccination. BMC Vet. Res. 2010, 6, 31. [Google Scholar] [CrossRef]
- Government of Bangladesh. Introduce Bird flu Vaccines for Poultry Farms from Mid-December. Dhaka Herald, 3 December 2013. [Google Scholar]
- PoultryMed. Bangladesh: Avian Influenza Immunization Program 2012. Available online: http://www.poultrymed.com/Poultrymed/Templates/showpage.asp?DBID=1&LNGID=1&TMID=178&FID=1585&PID=0&IID=3418 (accessed on 11 May 2019).
- Ansari, W.K.; Parvej, M.S.; El Zowalaty, M.E.; Jackson, S.; Bustin, S.A.; Ibrahim, A.K.; El Zowalaty, A.E.; Rahman, M.T.; Zhang, H.; Khan, M.F.R. Surveillance, epidemiological, and virological detection of highly pathogenic H5N1 avian influenza viruses in duck and poultry from Bangladesh. Vet. Microbiol. 2016, 193, 49–59. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Biswas, P.K.; Christensen, J.P.; Ahmed, S.S.; Das, A.; Rahman, M.H.; Barua, H.; Giasuddin, M.; Hannan, A.S.; Habib, M.A.; Debnath, N.C. Risk for infection with highly pathogenic avian influenza virus (H5N1) in backyard chickens, Bangladesh. Emerg. Infect. Dis. 2009, 15, 1931–1936. [Google Scholar] [CrossRef] [PubMed]
- Biswas, P.; Rahman, M.; Das, A.; Ahmed, S.; Giasuddin, M.; Christensen, J.P. Risk for Highly Pathogenic Avian Influenza H5N1 Virus Infection in Chickens in Small-Scale Commercial Farms, in a High-Risk Area, Bangladesh, 2008. Transbound Emerg. Dis. 2011, 58, 519–525. [Google Scholar] [CrossRef] [PubMed]
- Biswas, P.; Christensen, J.P.; Ahmed, S.; Barua, H.; Das, A.; Rahman, M.; Giasuddin, M.; Hannan, A.; Habib, A.; Debnath, N. Risk factors for infection with highly pathogenic influenza A virus (H5N1) in commercial chickens in Bangladesh. Vet. Rec. 2009, 164, 743–746. [Google Scholar] [CrossRef] [PubMed]
- Osmani, M.; Thornton, R.; Dhand, N.; Hoque, M.; Milon, S.; Kalam, M.; Hossain, M.; Yamage, M. Risk factors for highly pathogenic avian influenza in commercial layer chicken farms in Bangladesh during 2011. Transbound Emerg. Dis. 2014, 61, e44–e51. [Google Scholar] [CrossRef] [PubMed]
- Ahmed, S.; Ersbøll, A.K.; Biswas, P.; Christensen, J.P. The space–time clustering of highly pathogenic avian influenza (HPAI) H5N1 outbreaks in Bangladesh. Epidemiol. Infect. 2010, 138, 843–852. [Google Scholar] [CrossRef] [PubMed]
- Ahmed, S.S.; Ersbøll, A.K.; Biswas, P.K.; Christensen, J.P.; Toft, N. Spatio-temporal magnitude and direction of highly pathogenic avian influenza (H5N1) outbreaks in Bangladesh. PLoS ONE 2011, 6, e24324. [Google Scholar] [CrossRef] [PubMed]
- Ahmed, S.S.; Ersbøll, A.K.; Biswas, P.K.; Christensen, J.P.; Hannan, A.S.; Toft, N. Ecological determinants of highly pathogenic avian influenza (H5N1) outbreaks in Bangladesh. PLoS ONE 2012, 7, e33938. [Google Scholar] [CrossRef] [PubMed]
- Moyen, N.; Ahmed, G.; Gupta, S.; Tenzin, T.; Khan, R.; Khan, T.; Debnath, N.; Yamage, M.; Pfeiffer, D.; Fournie, G. A large-scale study of a poultry trading network in Bangladesh: Implications for control and surveillance of avian influenza viruses. BMC Vet. Res. 2018, 14, 12. [Google Scholar] [CrossRef]
- Government of Bangladesh. 2nd National Avian and Pandemic Influenza Preparedness and Response Plan, Bangladesh; 2009–2011; DGHS: Dhaka, Bangladesh, 2009.
- Chattopadhyay, D.K. Policy Options for Avian Influenza and Other Poultry-Related Zoonoses in Bangladesh; Chatham House: London, UK, 2016. [Google Scholar]
- Gerloff, N.A.; Khan, S.U.; Balish, A.; Shanta, I.S.; Simpson, N.; Berman, L.; Haider, N.; Poh, M.K.; Islam, A.; Gurley, E. Multiple reassortment events among highly pathogenic avian influenza A (H5N1) viruses detected in Bangladesh. Virology 2014, 450–451, 297–307. [Google Scholar] [CrossRef]
- Gerloff, N.A.; Khan, S.U.; Zanders, N.; Balish, A.; Haider, N.; Islam, A.; Chowdhury, S.; Rahman, M.Z.; Haque, A.; Hosseini, P. Genetically diverse low pathogenicity avian influenza A virus subtypes co-circulate among poultry in Bangladesh. PLoS ONE 2016, 11, e0152131. [Google Scholar] [CrossRef] [PubMed]
- Nasreen, S.; Uddin Khan, S.; Azziz-Baumgartner, E.; Hancock, K.; Veguilla, V.; Wang, D.; Rahman, M.; Alamgir, A.S.; Sturm-Ramirez, K.; Gurley, E.S.; et al. Seroprevalence of antibodies against highly pathogenic avian influenza A (H5N1) virus among poultry workers in Bangladesh, 2009. PLoS ONE 2013, 8, e73200. [Google Scholar] [CrossRef] [PubMed]
- Oladokun, A.T.; Meseko, C.A.; Ighodalo, E.; John, B.; Ekong, P.S. Effect of intervention on the control of highly pathogenic avian influenza in Nigeria. Pan Afr. Med. J. 2012, 13, 14. [Google Scholar] [CrossRef] [PubMed]
- Pittman, M.; Laddomada, A.; Freigofas, R.; Piazza, V.; Brouw, A.; Brown, I.H. Surveillance, prevention, and disease management of avian influenza in the European Union. J. Wildl. Dis. 2007, 43, S64–S70. [Google Scholar]
- Fournié, G.; Tripodi, A.; Nguyen, T.T.T.; Tran, T.T.; Bisson, A.; Pfeiffer, D.U.; Newman, S.H. Investigating poultry trade patterns to guide avian influenza surveillance and control: A case study in Vietnam. Sci. Rep. 2016, 6, 1–10. [Google Scholar] [CrossRef] [PubMed]
- Machalaba, C.C.; Elwood, S.E.; Forcella, S.; Smith, K.M.; Hamilton, K.; Jebara, K.B.; Swayne, D.E.; Webby, R.J.; Mumford, E.; Mazet, J.A. Global avian influenza surveillance in wild birds: A strategy to capture viral diversity. Emerg. Infect. Dis. 2015, 21, e141415. [Google Scholar] [CrossRef]
- Swayne, D.E. Impact of vaccines and vaccination on global control of avian influenza. Avian Dis. 2012, 56, 818–828. [Google Scholar] [CrossRef] [PubMed]
- Capua, I.; Marangon, S. Vaccination for avian influenza in Asia. Vaccine 2004, 22, 4137–4138. [Google Scholar] [CrossRef]
- Capua, I.; Terregino, C.; Cattoli, G.; Toffan, A. Increased resistance of vaccinated turkeys to experimental infection with an H7N3 low-pathogenicity avian influenza virus. Avian Pathol. 2004, 33, 158–163. [Google Scholar] [CrossRef]
- Vandersmissen, A.; Welburn, S. Current initiatives in one health: Consolidating the one health global network. Rev. Sci. Tech. 2014, 33, 421–432. [Google Scholar] [CrossRef]
- Rwego, I.B.; Babalobi, O.O.; Musotsi, P.; Nzietchueng, S.; Tiambo, C.K.; Kabasa, J.D.; Naigaga, I.; Kalema-Zikusoka, G.; Pelican, K. One Health capacity building in sub-Saharan Africa. Infect. Ecol. Epidemiol. 2016, 6, 34032. [Google Scholar] [CrossRef] [PubMed]
- Chatterjee, P.; Kakkar, M.; Chaturvedi, S. Integrating one health in national health policies of developing countries: India’s lost opportunities. Infect. Dis. Poverty 2016, 5, 87. [Google Scholar] [CrossRef] [PubMed]
Types of Surveillance | Species | Duration | Type of Samples Collected | Laboratory Tests Used | References |
---|---|---|---|---|---|
Poultry surveillance [icddr,b] | Waterfowl, commercial chickens, backyard chickens, market environment | 2007–till date | Cloacal swabs, swabs from freshly laid feces, tracheal swabs, environmental pooled swabs | rRT-PCR for typing and subtyping of influenza A viruses | [27] |
Poultry surveillance [DLS-FAO-ECTAD] | Waterfowl, commercial chickens, backyard chickens | 2008–2013 | Cloacal swabs, swabs from freshly laid feces, tracheal swabs | rRT-PCR for typing and subtyping of influenza A viruses | Personal communication, DLS |
Sink surveillance [DLS-FAO-ECTAD] | Market environment | 2016–till date | Environmental pooled swabs | rRT-PCR for typing and subtyping of influenza A viruses | Personal communication, DLS |
Poultry worker’s surveillance [icddr,b] | Humans | 2012–2017 | Nasopharyngeal and throat swab (respiratory swabs), acute and convalescent blood specimens | Respiratory swabs: rRT-PCR for influenza A and B viruses and subtyping for influenza A Serum: haemagglutination inhibition (HI) and microneutralization (MN) assay | [28] |
Hospital-based Influenza Surveillance (HBIS) [icddr,b] | Humans | 2007–till date | Nasopharyngeal and throat swab | rRT-PCR for influenza A and B viruses and subtyping for influenza A | [29] |
National Influenza Surveillance, Bangladesh (NISB) [IEDCR] | Humans | 2010–till date | Nasopharyngeal and throat swab | rRT-PCR for influenza A and B viruses and subtyping for influenza A | [29] |
Programs | Description | Results |
---|---|---|
Nationwide mass media campaigns Duration: 2007–2008 Implemented by: GoB, WHO, FAO, OIE, UNICEF, BRAC, CARE, USAID, AI.COMM, icddr,b, other NGOs Targeted for: All poultry sectors | Safe behaviors, 10-step recommendations (including basic hygiene messages, e.g., using masks, handwashing, and not touching sick poultry) were disseminated through radio, television, newspapers, public meetings, folk songs and plays, rickshaws and vans equipped with megaphones, posters, training manuals [46,50,51] | 70% backyard and 90% commercial poultry farmers and 65% live bird handlers were aware of good biosecurity; 80% targeted journalists accepted good reporting practices; however, adoption of recommended practices remained poor in all sectors; 84% of HPAI outbreaks involving commercial farms indicated a disconnect between the KAP and practice as well as persisting weak biosecurity BPMC: some improvements in the structural biosecurity of the LBM and the farms under intervention was reported, however, operational biosecurity was poor for both the markets and the farms, and biosafety practices were almost absent [26,48,49,55,56,57] |
Avian Influenza Preparedness and Response Project Duration: 2007–2012 Implemented by: DLS, Department of Mass Communications, Ministry of Fisheries and Livestock (MoFL), FAO Targeted for: All poultry sectors | Public awareness and risk communication campaigns conducted in 20 sub-districts in 20 districts using film shows, folk songs, school programs, distribution of leaflets, posters and banners; DLS trained poultry farmers, veterinarians, paraprofessionals, community health workers, media persons, news reporters, and students; piloted Biosecure Poultry Market Chains (BPMC) in 9 LBMs, 18 broiler and layer farms, among 324 poultry farmers, 180 LBM workers, 90 middlemen/transporters, and 1260 poultry chain stakeholders in 9 of the districts at highest risk of HPAI, to establish good biosecurity practices along the entire poultry value chain [26] | |
Teacher training program for AI outbreak reporting Duration: 2009 Implemented by: FAO, DLS Targeted for: All poultry sectors | One-day workshops conducted in three selected sub-districts involving school and madrassa teachers on disease reporting and the risks and prevention of HPAI [52] | Not available |
Behavior change pilot intervention Duration: 2009–2010 Implemented by: icddr,b Targeted for: Backyard poultry raisers | Context-appropriate behavior change recommendations piloted among the rural raisers in one community in each of the two districts [44] | Awareness increased but behavior remained unchanged; reasons for non-compliance: perceived absence of AIV in raisers’ flocks, low-risk of AIV, cost, inconvenience, personal discomfort, fear of being rebuked or ridiculed, and doubt about the necessity of the intervention [44] |
Safe poultry slaughter pilot intervention Duration: 2014 Implemented by: icddr,b Targeted for: Rural communities | A safe poultry slaughtering method piloted in two rural communities in a district in order to reduce human exposure to airborne virus by performing poultry slaughtering in a closed container [53,58] | The recommendations were found to be acceptable and feasible for the villagers with minor modification [53] |
Upazila-to-Community (U2C) Duration: 2017–till date Implemented by: DLS, FAO Targeted for: Backyard and commercial poultry sectors | Targeted to cover 496 sub-districts; avails veterinary services to rural communities to improve livestock production and disease control, increasing resilience to emerging disease events [54] | The program is still ongoing, no evaluation/result available |
Program on farm biosecurity Duration: 2005–2006 Implemented by: GoB, DLS, BRAC and other NGOs Targeted for: Commercial poultry sector | Training on farm biosecurity (i.e., the prevention and control of AIV) provided along with gloves and disinfectants to 33 breeders/hatchery farm managers and 340 large commercial farms; 150,000 small-scale farmers trained across the country [46] | Not available |
Stamping Out Pandemic and Avian Influenza (STOP AI) Duration: 2008–2010 Implemented by: USAID, FAO, city corporation, DLS Targeted for: Commercial poultry and LBM sectors | Different sectors were mobilized to improve biosecurity; biosecurity training implemented for veterinarians and livestock science graduates; 7 LBM training programs implemented in 5 divisions; cleaning and disinfection activities piloted in 2 LBMs; biosecurity improvement models (infrastructure improvements, e.g., farm boundary, footbath, biogas and compost plants) implemented in 12 commercial farms in a district and 2 LBMs in 2 districts; cleaning and disinfection activities implemented in 24 LBMs within and outside Dhaka through training, technical support, financial assistance for infrastructure renovations, renovation of the water supply, the addition of a biogas facility for proper waste disposal, and a slaughter house [54,59,60,61] | Awareness and precautionary practices increased; substantially fewer HPAI outbreaks were reported; no clusters of infection were found in the intervention farms/LBMs; the effect of the intervention on the incidence of disease was limited to a few months after completion—indicating the challenges of sustaining the progress; despite increased biosecurity, no significant reduction in virus circulation was found in the FAO-intervened markets compared to the non-intervened ones [60,62] |
Community-engaged biosecurity (CEB) model Duration: 2016–2018 Implemented by: Bangladesh Agricultural University (BAU) Targeted for: Commercial poultry sector | From each of the two sub-districts, training of trainers (ToT) was provided to 50 lead farmers, who trained their fellow farmers; regular farm visits by community animal health workers were made to monitor compliance [63] | The program is still ongoing, no evaluation/result available |
Biosecurity program in the LBMs Duration: 2007–2008 Implemented by: BRAC, IFC, SEDF Targeted for: LBM sector | A series of trainings and practical demonstrations on biosecurity and the use of personal protective equipment (PPE), along with gloves, masks, disinfectants, and small spray machines, were provided in retail and wholesale shops from 38 LBMs of Dhaka [46] | Not available |
The LBM C4D initiative Duration: 2012–2013 Implemented by: UNICEF, GoB Targeted for: LBM sector | Intervention implemented in 16 LBMs to improve the knowledge and threat perception of AIV, as well as the bio-security practices of the poultry workers [56] | Despite an improved knowledge level, no significant change observed in biosecurity measures after the intervention; major barriers: lack of proper infrastructure to adopt the recommendations, concern of negative financial impact, lack of self-risk perception [56] |
Piloting workstations for poultry workers Duration: 2008–2012 Implemented by: icddr,b Targeted for: LBM sector | Portable workstations (including a worktop and handwashing facility with soapy water) were designed and piloted in 13 shops in a LBM to reduce the risk of environmental contamination and improve handwashing practices [64,65] | The workstations were acceptable, functional, improved handwashing practices and the use of clean water; soapy water was effective in removing influenza viruses from poultry workers’ hands; however, handwashing decreased over time; major barriers: the difficulty to manage the increased cost for water and detergent by shops and the inability to frequently wash hands during busy hours [64,65] |
Use of wooden shelters Duration: Not available Implemented by: BRAC Targeted for: Backyard poultry sector | Moveable wooden poultry shelters were developed and promoted to help the smallholder farmers to maintain bio-security measures at low costs [46] | Not available |
© 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Rimi, N.A.; Hassan, M.Z.; Chowdhury, S.; Rahman, M.; Sultana, R.; Biswas, P.K.; Debnath, N.C.; Islam, S.S.; Ross, A.G. A Decade of Avian Influenza in Bangladesh: Where Are We Now? Trop. Med. Infect. Dis. 2019, 4, 119. https://doi.org/10.3390/tropicalmed4030119
Rimi NA, Hassan MZ, Chowdhury S, Rahman M, Sultana R, Biswas PK, Debnath NC, Islam SS, Ross AG. A Decade of Avian Influenza in Bangladesh: Where Are We Now? Tropical Medicine and Infectious Disease. 2019; 4(3):119. https://doi.org/10.3390/tropicalmed4030119
Chicago/Turabian StyleRimi, Nadia A., Md. Zakiul Hassan, Sukanta Chowdhury, Mahmudur Rahman, Rebeca Sultana, Paritosh K. Biswas, Nitish C. Debnath, SK Shaheenur Islam, and Allen G. Ross. 2019. "A Decade of Avian Influenza in Bangladesh: Where Are We Now?" Tropical Medicine and Infectious Disease 4, no. 3: 119. https://doi.org/10.3390/tropicalmed4030119