Serological Evidence of Avian Influenza in Captive Wild Birds in a Zoo and Two Safari Parks in Bangladesh

Abstract

Avian influenza (AI) is endemic and frequently causes seasonal outbreaks in winter in Bangladesh due to high pathogenic avian influenza (HPAI) H5N1 and low pathogenic avian influenza (LPAI) H9N2. Among avian influenza A viruses (AIV), H5, H7, and H9 subtypes have the most zoonotic potential. Captive birds in zoos and safari parks are used for educational, recreational, breeding, and conservational purposes in Bangladesh. To screen for AIV in captive birds to assess potential public health threats, we conducted a cross-sectional study in two safari parks and one zoo in Bangladesh for four months, from November to December 2013 and from January to February 2014. We collected blood samples, oropharyngeal, and cloacal swabs from 228 birds. We tested serum samples for AIV antibodies using competitive enzyme-linked immunosorbent assay (c-ELISA) and AIV sero-subtype H5, H7, and H9 using hemagglutination inhibition (HI) test. Swab samples were tested for the presence of avian influenza viral RNA using real-time reverse transcription-polymerase chain reaction (rRT-PCR). Across all the samples, AIV antibody prevalence was 9.7% (95% CI: 6.1–14.2, n = 228) and AIV HA subtype H5, H7 and H9 sero-prevalence was 0% (95% CI: 0–1.6, n = 228), 0% (95% CI: 0–1.6, n = 228) and 6.6% (95% CI: 3.72–10.6, n = 228), respectively. No AI viral RNA (M-gene) was detected in any swab sample (0%, 95% CI: 0–1.6, n = 228). Birds in the Safari park at Cox’s Bazar had a higher prevalence in both AIV antibody prevalence (13.5%) and AIV H9 sero-prevalence (9.6%) than any of the other sites, although the difference was not statistically significant. Among eight species of birds, Emu (Dromaius novaehollandiae) had the highest sero-positivity for both AIV antibody prevalence (26.1%) and AIV H9 prevalence (17.4%) followed by Golden pheasant (Chrysolophus pictus) with AIV antibody prevalence of 18.2% and AIV H9 prevalence of 11.4%. Our results highlight the presence of AI antibodies indicating low pathogenic AIV mingling in captive birds in zoos and safari parks in Bangladesh. Continuous programmed surveillance is therefore recommended to help better understand the diversity of AIVs and provide a clear picture of AI in captive wild birds, enabling interventions to reduce the risk of AIV transmission to humans.

Serological Evidence of West Nile Virus in Wild Birds in Bangladesh

“…Depending on the season, migratory birds annually overfly countries in both the Northern and Southern hemisphere [ 9 ], thus playing an essential role in the spread of WNV in Asia, Africa, and Europe [ 1 ]. When migratory birds visit different tropical and subtropical countries to avoid the intense cold weather during winter, they carry viruses, including avian influenza [ 10 , 11 , 12 , 13 ] and others, from temperate to tropical regions. The presence of WNV has been reported in different countries, like Mexico, the USA, India, Pakistan, and Germany, covering various continents, including Asia, Europe, Australasia, and Africa.…”

Prevalence and Distribution of Avian Influenza Viruses in Domestic Ducks at the Waterfowl-Chicken Interface in Wetlands

“…High AI seroprevalence (63.8%) in ducks at an individual level was recorded in the present study, which is similar to a previous study (55.6%) conducted in the northeastern and western parts of Bangladesh [ 41 ]. Variable individual level of AI seroprevalence was previously reported to be 15–90.2% in Bangladesh [ 8 , 9 , 13 , 14 , 42 ]. Complex production systems involving household ducks and rice production are likely to be important epidemiological factors for the maintenance and spread of IAVs, which might explain the existing high AI seroprevalence in the study sites [ 43 ].…”

An Outbreak of Highly Pathogenic Avian Influenza (H7N7) in Australia and the Potential for Novel Influenza A Viruses to Emerge

“…With the emu displaying a cell tropism that could be favourable to both avian and human influenza A strains, should this species be recognised as a possible mixing vessel for the emergence of novel IAV strains? Evidence shows that the emu can carry human and avian IAVs [ 60 ] and many viral HA and NA subtypes [ 61 , 62 , 63 , 65 , 66 ], supporting the contention that these birds could provide the host conditions to facilitate genetic reassortment and give rise to novel IAV strains.…”

“…However, this bird appears to have an extensive internal tissue tropism that makes it susceptible to avian (H5N1, H5N2) and human (H1N1) influenza viruses [ 60 , 61 ]. Additionally, reports of seropositivity for hemagglutinin subtypes H1–H9, H11, H12 and neuraminidase subtypes N1–N9 highlights how susceptible this bird is to a range of viral subtypes [ 62 , 63 ]. Recognising that novel influenza A viruses emerge through reassortment of viral subtypes, it is appropriate to consider how these findings raise the spectre for internal mixing and viral reassortment within this species and whether this possibility necessitates a greater research focus to mitigate the emergence of strains with pandemic potential.…”

“…Nonetheless, the authors demonstrated SA receptor affinity in emus for human pandemic influenza H1N1 (A/H1N1/Virginia/2009) and LPAI H5N2 (A/chicken/PA/7659/85) viruses [ 60 ]. A study of captive birds from a zoo and two safari parks in Bangladesh concluded that in comparison to other birds in the same facilities, emus returned the highest seropositivity for AIV antibody prevalence (H5, H7, H9 subtypes) and AIV H9 subtype prevalence, thus highlighting the circulation of LPAI viruses in this specific setting [ 63 ]. In China, Kang et al (2006) reported the pathogenic emergence of H9N2 in emus, postulating transmission from chickens as the likely origin of infection [ 67 ].…”