Village and farm-level risk factors for avian influenza infection on backyard chicken farms in Bangladesh

www.nature.com/scientificreports OPEN Village and farm‑level risk factors for avian influenza infection on backyard chicken farms in Bangladesh Suman Das Gupta1*, Brishti Barua2, Guillaume Fournié3, Md. Ahasanul Hoque2 & Joerg Henning1 A cross-sectional study was conducted with 144 small-scale poultry farmers across 42 Bangladeshi villages to explore risk factors associated with avian influenza H5 and H9 seropositivity on backyard chicken farms. Using mixed-effects logistic regression with village as random effect, we identified crow abundance in garbage dumping places and presence of migratory wild birds within villages to be associated with higher odds of H5 and H9 seropositivity. At farm-level, garbage around poultry houses was also associated with higher odds of H5 and H9 seropositivity. In addition, specific trading practices (such as, purchase of chickens from live bird markets (LBM) and neighboring farms to raise them on their own farms, frequency of visits to LBM, purchase of poultry at LBM for consumption) and contact of backyard chickens with other animals (such as, feeding of different poultry species together, using pond water as drinking source for poultry, access of feral and wild animals to poultry houses) were associated with higher odds of H5 or H9 seropositivity. Resource-constrained smallscale poultry farmers should be able to address risk factors identified in this study without requiring large investments into poultry management, thereby reducing the likelihood of avian influenza virus transmission and ultimately occurrence of avian influenza outbreaks. Backyard chickens reared under traditional scavenging conditions are an essential source of nutritious food1 and income for rural households in low and middle-income countries (LMICs) like B angladesh2,3. However, the low level of biosecurity in this farming system may put backyard poultry at a high risk of infection with avian influenza viruses (AIVs)4. Backyard poultry is therefore often considered to promote the spread and persistence of AIVs5,6. On the other hand, it has been hypothesized that, due to their small flock size, the risk of a viral introduction and spread may be substantially lower for backyard compared to commercial flocks7,8, and that local breeds, raised on backyard farms, are less susceptible to infection than exotic breeds reared in commercial enterprises9,10. However, there is no experimental and observational evidence supporting these h ypotheses11. Highly Pathogenic Avian Influenza (HPAI) H5N1 was first reported in Bangladesh in 2007. It is now endemic in Bangladesh with multiple AIV subtypes, including Low Pathogenic Avian Influenza (LPAI) H9N2, circulating in the country’s poultry population, raising concerns about the emergence of a new AIV variant with significant public health concern12,13. A recent study conducted in Bangladeshi Live Bird Markets (LBM) estimated a prevalence of H5 and H9 AIVs of 1.3% and 8.3% in backyard chickens, 7.6% and 3.4% in waterfowl (ducks and geese), respectively14. In contrast, in another field study conducted by Gupta et al.15, none of the chickens and ducks sampled on backyard flocks tested positive for H5 AIV, and only 0.2% of chickens tested positive for H9 AIV15. The H5 and H9 seroprevalence in this study was 4.2% and 16.0% in unvaccinated backyard chickens, and 14.2% and 15.7% in unvaccinated ducks, respectively, indicating past exposure of backyard chicken to circulating H5 and H9 virus15. The implementation of comprehensive biosecurity practices is notoriously challenging, if at all feasible, in backyard chicken farming s ystems16. The lack of adherence to recommended biosecurity practices is also likely influenced by backyard farmers’ beliefs that their poultry does not play a significant role in AIV transmission5. It is therefore essential to identify risk factors contributing to AIV infection, in order to develop specific extension messages and recommendations for improved biosecurity that are low-cost and feasible for backyard poultry 1 School of Veterinary Science, University of Queensland, Gatton, QLD 4343, Australia. 2Chattogram Veterinary and Animal Sciences University, Chattogram, Bangladesh. 3Department of Pathobiology and Population Sciences, Royal Veterinary College, University of London, London, UK. *email: Scientific Reports | (2022) 12:13009 | https://doi.org/10.1038/s41598-022-16489-5 1 Vol.:(0123456789) www.nature.com/scientificreports/ Risk factors (listed in risk groups) Univariate analysis Category Multi-variable analysis H5 positive (%) H5 negative (%) H5 OR (95% CI) No crows or absence of garbage dumping place 20 (19.6) 82 (80.4) Reference Yes 20 (47.6) 22 (52.4) 3.7 (1.7–8.1) 0 25 (20.5) 97 (79.5) Reference 1–3 6 (54.6) 5 (45.5) 4.7 (1.3–16.5) >3 9 (81.8) 2 (18.2) 17.5 (3.5–86.0) No 23 (19.0) 98 (81.0) Reference Yes 17 (73.9) 6 (26.1) 30.8 (5.6–168.7) No Feeding of different poultry species with the same feeder or in the Yes same location 10 (13.0) 67 (87.0) Reference 30 (44.8) 37 (55.2) 5.8 (2.4–14.3) No 13 (16.3) 67 (83.8) Reference Yes 27 (42.2) 37 (57.8) 4.1 (1.7–10.2) H5 p value H5 OR (95% CI) H5 p value Village-level factors (N = 144 farms, N = 42 villages) Environmental or ecological features Crow abundance around a garbage dumping places within the village 0.001 Reference 0.039 3.4 (1.1–10.8) Farm-level factors (N = 144 farms) Trading practices Number of chickens bought from live bird markets in the last 12 months Reference 0.000 9.5 (1.3–69.9) 0.016 8.8 (1.2–65.9) Disposal of garbage Garbage piled up around the poultry houses or on the farm 0.000 Reference 9.1 (1.7–48.8) 0.010 Indirect contact with other animals Pond water used as source of drinking water for poultry 0.000 0.002 Reference 5.2 (1.7–15.7) Reference 4.6 (1.4–14.9) 0.003 0.010 Table 1.  Results of the univariate and multi-variable analysis for village and farm-level risk factors (N = 144 farms, N = 42 villages) associated with H5 flock-level seroprevalence on backyard chicken farms in Bangladesh, 2016. Significant values are in bold. farmers. To our knowledge, only one case–control study was conducted in Bangladesh more than 13 years ago, that focused on the identification of farm-level factors associated with the occurrence of H5N1 outbreaks on backyard farms17. Risk factors for current H5 and H9 circulation in apparently healthy backyard poultry have not been described in Bangladesh. In this study, we focused on clinically healthy chickens to monitor their past exposure to AIV. By focusing on chickens without clinical signs, we can describe the circulation of AIV in chickens that might had occurred in these flocks and risk factors associated with this AIV exposure. We are also able to inform farmers about potential threats to their current poultry production so that they can take appropriate actions. Furthermore, as the coinfection of the HPAI virus with (...truncated)