Abstract
Slaughtering sick poultry is a risk factor for human infection with highly pathogenic avian influenza and is a common practice in Bangladesh. This paper describes human exposures to poultry during slaughtering process and the customs and rituals influencing these practices in two Bangladeshi rural communities. In 2009, we conducted 30 observations to observe slaughtering practices and 110 in-depth and short interviews and 36 group discussions to explore reasons behind those practices. The villagers reported slaughtering 103 poultry, including 20 sick poultry during 2 months. During different stages of slaughtering, humans, the environment, healthy poultry, and other animals were exposed to poultry blood and body parts. Women performed most of the slaughtering tasks, including evisceration. Defeathering required the most time and involved several persons. During festivals, ceremonies, and rituals, many people gathered and participated in the slaughtering of poultry. Exposure to poultry slaughtering created numerous opportunities for potential avian influenza transmission. Strategies that can be further tested to determine if they reduce the risk of transmission include skinning the carcasses of sick poultry, using hot water for defeathering and cleaning, using a bucket to contain slaughtering blood and carcass, burying the offal and encouraging handwashing.
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References
Abdel-Ghafar AN, Chotpitayasunondh T, Gao Z, Hayden FG, Nguyen DH, de Jong MD, et al. (2008). Update on avian influenza A (H5N1) virus infection in humans. N Engl J Med 358:261-273.
Aklilu HA, Almekinders CJ, Udo HM, and Van der Zijpp AJ (2007). Village poultry consumption and marketing in relation to gender, religious festivals and market access. Tropical Animal Health and Production 39:165-177.
Aklilu HA, Udo HMJ, Almekinders CJM, and Van der Zijpp AJ (2008). How resource poor households value and access poultry: Village poultry keeping in Tigray, Ethiopia. Agricultural Systems 96:175-183.
Areechokchai D, Jiraphongsa C, Laosiritaworn Y, Hanshaoworakul W, O’Reilly M (2006) Investigation of avian influenza (H5N1) outbreak in humans—Thailand, 2004. Global Epidemiology 55:3–6.
Barennes H, Harimanana AN, Lorvongseng S, Ongkhammy S, and Chu C (2010). Paradoxical risk perception and behaviours related to Avian Flu outbreak and education campaign, Laos. BMC Infectious Diseases 10:294.
Bean B, Moore BM, Sterner B, Peterson LR, Gerding DN, and Balfour HH, Jr. (1982). Survival of influenza viruses on environmental surfaces. Journal of Infectious Diseases 146:47-51.
Biswas PK, Christensen JP, Ahmed SS, Das A, Rahman MH, Barua H, et al. (2009) Risk for infection with highly pathogenic avian influenza virus (H5N1) in backyard chickens, Bangladesh. Emerging Infectious Diseases 15:1931–1936. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=19961672.
Brooks WA, Alamgir AS, Sultana R, Islam MS, Rahman M, Fry AM, et al. (2009). Avian influenza virus A (H5N1), detected through routine surveillance, in child, Bangladesh. Emerging Infectious Diseases 15:1311-1313.
Busquets N, Abad FX, Alba A, Dolz R, Allepuz A, Rivas R, et al. (2010). Persistence of highly pathogenic avian influenza virus (H7N1) in infected chickens: feather as a suitable sample for diagnosis. Journal of General Virology 91:2307-2313.
Cavailler P, Chu S, Ly S, Garcia JM, Hado Q, Bergeri I, et al. (2010) Seroprevalence of anti-H5 antibody in rural Cambodia, 2007. Journal of Clinical Virology 48:123-126.
Chakraborty A (2011). Outbreak of mild respiratory disease caused by H5N1 and H9N2 infections among young children in Dhaka, Bangladesh, 2011 Health and Science Bulletin 9:5-12.
Dinh PN, Long HT, Tien NT, Hien NT, Mai le TQ, Phong le H, et al. (2006). Risk factors for human infection with avian influenza A H5N1, Vietnam, 2004. Emerging Infectious Diseases 12:1841-1847.
Dolberg F (2008) Poultry sector country review: Bangladesh. Rome: Food and Agriculture Organization of the United Nations.
Fasina FO, Ifende VI, and Ajibade AA (2010). Avian influenza A(H5N1) in humans: lessons from Egypt. Euro Surveill 15:19473.
Food and Agriculture Organization (2008) Rural Livelihood and Biosecurity of Smallholder Poultry Producers and Poultry Value Chain. Rome: FAO. http://www.commdev.org/userfiles/Smallholder%20biosecurity%20in%20Poultry%20Value%20Chain.pdf. Accessed August 24, 2013.
Gilsdorf A, Boxall N, Gasimov V, Agayev I, Mammadzade F, Ursu P, et al. (2006). Two clusters of human infection with influenza A/H5N1 virus in the Republic of Azerbaijan, February-March 2006. Euro Surveill 11:122-126.
Gondwe TN, and Wollny CB (2007). Local chicken production system in Malawi: household flock structure, dynamics, management and health. Tropical Animal Health and Production 39:103-113.
Gove S, and Pelto GH (1994). Focused ethnographic studies in the WHO Programme for the Control of Acute Respiratory Infections. Medical Anthropology 15:409-424.
Government of Bangladesh (2007) Bird Flu: What You Need to Know and Do. http://www.mofl.gov.bd/bird_flu.aspx. Accessed August 24, 2013.
Horm SV, Gutierrez RA, Sorn S, and Buchy P (2012). Environment: a potential source of animal and human infection with influenza A (H5N1) virus. Influenza Other Respi Viruses 6:442-448.
IEDCR (2012a) Fifth and Sixth H5N1 Human Case in Bangladesh. http://www.iedcr.org/pdf/files/influenza/Fifth_and_Sixth_H5N1.pdf. Accessed September 20, 2013.
IEDCR (2012b) Fourth H5N1 Human Case in Bangladesh. http://www.iedcr.org/pdf/files/influenza/Fourth-H5N1-human-case-in-Bangladesh.pdf. Accessed September 20, 2013.
Islam MR, Haque ME, Giasuddin M, Chowdhury EH, Samad MA, Parvin R, et al. (2011). New Introduction of Clade 2.3.2.1 Avian Influenza Virus (H5N1) into Bangladesh. Transbound Emerg Dis 59: 460-463.
Jackson S, Van Hoeven N, Chen LM, Maines TR, Cox NJ, Katz JM, et al. (2009). Reassortment between avian H5N1 and human H3N2 influenza viruses in ferrets: a public health risk assessment. J Virol 83:8131-8140.
Kandeel A, Manoncourt S, Abd el Kareem E, Mohamed Ahmed AN, El-Refaie S, Essmat H, et al. (2010). Zoonotic transmission of avian influenza virus (H5N1), Egypt, 2006-2009. Emerging Infectious Diseases 16:1101-1107.
Liu T (2008). Custom, taste and science: raising chickens in the Pearl River Delta Region, South China. Anthropology & Medicine 15:7-18.
Loth L, Gilbert M, Osmani MG, Kalam AM, and Xiao X (2010). Risk factors and clusters of Highly Pathogenic Avian Influenza H5N1 outbreaks in Bangladesh. Prev Vet Med 96:104-113.
Maas R, Tacken M, Ruuls L, Koch G, van Rooij E, and Stockhofe-Zurwieden N (2007). Avian influenza (H5N1) susceptibility and receptors in dogs. Emerging Infectious Diseases 13:1219-1221.
Manabe T, Pham TP, Vu VC, Takasaki J, Dinh TT, Nguyen TM, et al. (2011). Impact of educational intervention concerning awareness and behaviors relating to avian influenza (H5N1) in a high-risk population in Vietnam. PLoS One 6:e23711.
Manabe T, Tran TH, Doan ML, Do TH, Pham TP, Dinh TT, et al. (2012). Knowledge, attitudes, practices and emotional reactions among residents of avian influenza (H5N1) hit communities in Vietnam. PLoS One 7:e47560.
OIE (2013) Update on Highly Pathogenic Avian Influenza in Animals (Type H5 and H7). Follow-up Report 42. http://www.oie.int/wahis_2/public%5C..%5Ctemp%5Creports/en_fup_0000013335_20130430_165153.pdf. Accessed August 24, 2013.
Oner AF, Bay A, Arslan S, Akdeniz H, Sahin HA, Cesur Y, et al. (2006). Avian influenza A (H5N1) infection in eastern Turkey in 2006. N Engl J Med 355:2179-2185.
Padmawatia S, and Nichter M (2008). Community response to avian flu in Central Java, Indonesia. Anthropology & Medicine 15:31-51.
Paul M, Baritaux V, Wongnarkpet S, Poolkhet C, Thanapongtharm W, Roger F, et al. (2013). Practices associated with Highly Pathogenic Avian Influenza spread in traditional poultry marketing chains: Social and economic perspectives. Acta Trop 126:43-53.
Pelto PJ, and Pelto GH (1997). Studying knowledge, culture, and behavior in applied medical anthropology. Medical Anthropology Quarterly 11:147-163.
Rabinowitz P, Perdue M, and Mumford E (2010). Contact variables for exposure to avian influenza H5N1 virus at the human-animal interface. Zoonoses Public Health 57:227-238.
Rahman MW, Gurley ES, Islam MS, Aleem MA, Salimuzzaman M, Sharif AR, et al. (2013) The first reported fatal pediatric case of H5N1 with atypical symptoms, Bangladesh. In: Options for the Control of Influenza VIII Conference, Cape Town, South Africa.
Regenstein JM CM, Regenstein CE (2003). The kosher and halal food laws. Comprehensive Reviews in Food Science and Food Safety 2:111-127.
Rimi NA, Sultana R, Khan S, Nasreen S, Puri A, Alamgir ASM, et al. (2013) Biosecurity conditions and biosafety practices in the live bird markets of Dhaka city, Bangladesh, 2012. In: Options for the Control of Influenza VIII conference, Cape Town, South Africa.
Sultana R, Nahar N, Rimi NA, Azad S, Islam MS, Gurley ES, et al. (2012a). 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 12:1927.
Sultana R, Rimi NA, Azad S, Islam MS, Khan MS, Gurley ES, et al. (2012b). Bangladeshi backyard poultry raisers’ perceptions and practices related to zoonotic transmission of avian influenza. J Infect Dev Ctries 6:156-165.
UNICEF Bangladesh (2007) Avian Influenza Knowledge, Attitude and Practice (KAP) Survey among the General Public and Poultry Farmers in Bangladesh. Dhaka: UNICEF Bangladesh.
Van Kerkhove MD (2012). Poultry Movement and Sustained HPAI Risk in Cambodia. In: Health and Animal Agriculture in Developing Countries, Van Kerkhove MD, editor, pp. 233–263. New York: Springer.
Van Kerkhove MD, Ly S, Holl D, Guitian J, Mangtani P, Ghani AC, et al. (2008). Frequency and patterns of contact with domestic poultry and potential risk of H5N1 transmission to humans living in rural Cambodia. Influenza Other Respi Viruses 2:155-163.
Van Kerkhove MD, Ly S, Guitian J, Holl D, San S, Mangtani P, et al. (2009). Changes in poultry handling behavior and poultry mortality reporting among rural Cambodians in areas affected by HPAI/H5N1. PLoS One 4:e6466.
Van Kerkhove MD, Mumford E, Mounts AW, Bresee J, Ly S, Bridges CB, et al. (2011). Highly pathogenic avian influenza (H5N1): pathways of exposure at the animal-human interface, a systematic review. PLoS One 6:e14582.
Vong S, Ly S, Van Kerkhove MD, Achenbach J, Holl D, Buchy P, et al. (2009). Risk factors associated with subclinical human infection with avian influenza A (H5N1) virus-Cambodia, 2006. J Infect Dis 199:1744-1752.
Webster RG, Yakhno M, Hinshaw VS, Bean WJ, and Murti KG (1978). Intestinal influenza: replication and characterization of influenza viruses in ducks. Virology 84:268-278.
WHO (2006a) Human Cases of Influenza A (H5N1) Infection in Eastern Turkey, December 2005–January 2006. Geneva: WHO. http://www.who.int/wer/2006/wer8143.pdf.
WHO (2006b) Review of Latest Available Evidence on Potential Transmission of Avian Influenza (H5N1) Through Water and Sewage and Ways to Reduce the Risks to Human Health. Geneva: WHO.
WHO (2007) Avian Influenza: Food Safety Issues. Geneva: WHO. http://www.who.int/foodsafety/micro/avian/en/index1.html. Accessed March 1, 2012.
WHO (2013) Cumulative Number of Confirmed Human Cases of Avian Influenza A/(H5N1). Geneva: WHO. http://www.who.int/influenza/human_animal_interface/H5N1_cumulative_table_archives/en/index.html. Accessed September 20, 2013.
Zhou L, Liao Q, Dong L, Huai Y, Bai T, Xiang N, et al. (2009). Risk factors for human illness with avian influenza A (H5N1) virus infection in China. J Infect Dis 199:1726-1734.
Acknowledgments
This research was funded by the Centers of Disease Control and Prevention (CDC) under the agreement of CoAg Grant 5-U51-CI000298. icddr,b acknowledges the commitment of CDC to its research efforts with gratitude. We are grateful to our study participants for their time and invaluable information. We thank Marufa Hasin, Afroza Khanam Roza, and Md. Zahidur Rahman for their valuable contribution in data collection, Shamim Azad for his contribution to data organizing and Kamal Hossain for preparing the map. We also thank Dorothy Southern for her guidance in writing and Andrea Mikolon, Najmul Haider, and Meghan Scott for reviewing the manuscript.
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Rimi, N.A., Sultana, R., Ishtiak-Ahmed, K. et al. Poultry Slaughtering Practices in Rural Communities of Bangladesh and Risk of Avian Influenza Transmission: A Qualitative Study. EcoHealth 11, 83–93 (2014). https://doi.org/10.1007/s10393-013-0885-8
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DOI: https://doi.org/10.1007/s10393-013-0885-8
Keywords
- Avian influenza
- Bangladesh
- poultry slaughtering
- qualitative research
- focused ethnography