Risk of spill-over of diseases (in particular avian influenza) from wild aquatic birds in North Queensland

Hoque, Ahasanul (2011) Risk of spill-over of diseases (in particular avian influenza) from wild aquatic birds in North Queensland. PhD thesis, James Cook University.

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Abstract

Disease surveillance programs and longitudinal studies are uncommon in wild bird populations across the world. But many wild bird species are important sources of pathogens that are of particular importance to animal and human health, for example, avian influenza viruses.

This project included both active and passive surveillance in order to study the diseases and pathogens (in particular avian influenza) in wild aquatic birds of north Queensland. A three-year longitudinal study was conducted on wild aquatic birds at Billabong Sanctuary from April 2007 to March 2010 while a two-year longitudinal study was performed at Green Acres Lagoon (Cromarty), from December 2007 to 2009. Cross sectional studies were also performed on wild aquatic birds at Cape York and on the Atherton Tableland between 2007 and 2009.

The objective of this project was to determine the level of avian influenza and Newcastle disease viral RNA and avian influenza viral antibody, identify the associated potential risk factors and determine the distribution of avian influenza and Newcastle disease viral subtypes and their phylogenetic relationship with other isolates in Australia and overseas. This study also aimed to identify causes of mortality in wild aquatic birds of north Queensland and explore the connection between mortality in birds and avian influenza.

Birds were sampled quarterly at Billabong Sanctuary and Cromarty and sporadically on Cape York and the Atherton Tableland. Birds were captured mostly using funnel traps. A total of 1,555 live birds were captured and this resulted in the collection of 1,522 serum samples, 1,458 cloacal and 1,368 oropharyngeal swab samples. Tissue samples were obtained from 42 sick and dead birds and 1,157 fresh faecal samples of wild aquatic birds were collected from the environment surrounding water bodies. Samples were evaluated by serological, molecular, bacteriological and histopathological examinations where necessary.

Overall avian influenza viral RNA prevalence was ~1.0% in the samples of wild aquatic birds in north Queensland, whereas the avian influenza viral antibody prevalence was 11 times higher. These findings make biological sense given the fact that avian influenza viral shedding periods are relatively shorter than the presence of avian influenza viral antibodies in the blood.

Multivariate regression analysis was performed to identify potential risk factors for avian influenza antibody levels in wild aquatic birds. The odds ratio of being reactive for avian influenza antibodies was 13.1 (95% Confidence interval 5.9-28.9) for Pacific black ducks (53.7%) compared with plumed whistling ducks (10.1%) (Table 3.12; Chapter 3). This result was also supported by the linear regression analysis (Chapter 3; Table 3.11). An identical species pattern was identified in an unadjusted statistical analysis on the viral RNA data of avian influenza (Chapter 4; Table 4.7).

The odds ratios of being reactive for avian influenza antibodies were 2.9 (95% Confidence interval 1.3-6.6) for adult over ≤ sub-adult ducks (Table 3.10; Chapter 3). A similar age pattern was identified in the linear regression analysis (Table 3.9; Chapter 3). This age pattern might be due to more exposure to infections because of more opportunity in addition to longer lasting avian influenza antibodies in older ducks. A different age pattern was, however, identified in unadjusted analysis using the molecular data (Chapter 3; Table 3.11). This analysis indicated that immature birds were more commonly infected which may be due to the fact that they have more frequent infections because they are immunologically naïve whereas adults are more resistant, particularly to viruses to which they may have previously been exposed.

Avian influenza antibodies were at higher levels during warm wet weather (January-April) compared with warm dry weather (September-December) in linear regression analysis (Coefficient 8.3; 95% Confidence interval 3.0-13.6) (Chapter 3; Table 3.7). The warm wet season might reduce the immune status of birds, thus making them more vulnerable to infection which may in turn increase the levels of avian influenza antibodies.

The surveillance programs demonstrated the presence of low pathogenic avian influenza viral subtypes H6 and H9 in samples collected from wild aquatic birds. One of the H6 viruses was likely to have been newly introduced, probably through migratory species of birds such as the sharptailed sandpiper. This migratory bird regularly travels between Australia and Asia. Hence, there is a possibility of highly pathogenic avian influenza exotic viral subtypes such as H5N1 being introduced into Australia. The second H6 virus had a matrix gene similar to those found associated with Australian H7 subtypes. This would suggest an earlier introduction of a H6 subtype which had an opportunity to reassort with local viruses. The low pathogenic avian influenza viral subtype H9 had a matrix gene similar to that found in Asian H9 viruses. Some H9 viruses have been shown to cause mortality in poultry elsewhere in the world. This subtype has also been isolated from pigs and humans in different countries, which indicates its pandemic potential.

At the time that the H6 and H9 subtypes were detected in samples collected from wild birds in north Queensland the serological study demonstrated periods of infection with H6 and H9 serotypes.

The serological study also demonstrated a constant circulation of H5 and sporadic circulation of H7 subtypes in wild aquatic birds. These viruses are perhaps non-pathogenic as evident in other studies elsewhere in Australia. However, these low pathogenic avian influenza viral subtypes have potential to mutate to virulent types once introduced into commercial poultry.

Overall Newcastle disease viral RNA prevalence was 3.5% at the individual bird level which indicates the presence of Newcastle disease viruses in wild bird populations in north Queensland. The prevalence was significantly higher in plumed whistling ducks. Avirulent Newcastle disease viruses (class-one and class-two Australian type) were identified in samples collected from wild aquatic birds. This indicates that wild birds remain a reservoir of paramyxoviruses that could be transmitted to domestic poultry.

A logistic regression model was performed to identify potential risk factors for the level of Newcastle disease viral RNA prevalence in plumed whistling ducks. The odds of reactor samples were 2.7 (95% Confidence interval 1.5-4.9) times more likely in younger than older ducks (Chapter 5; Table 5.5). A similar age pattern of prevalence was observed in the study of avian influenza. This age susceptibility to infection may be due to the fact that young birds are immunologically naïve.

Only univariate logistic analysis indicated birds caught in the warm wet season (January-April) as being significantly associated with a higher prevalence of Newcastle disease viral RNA. This result virtually correlates with an increase in the numbers of immature birds at that time associated with the breeding season of adult birds.

The above identified risk factors will significantly contribute to the design of a targeted avian influenza and Newcastle disease surveillance program in wild aquatic birds in northern Australia by wildlife authorities.

Morbidity and mortality were sporadic and more commonly observed in chicks and juvenile birds in April than other months of the year. Identified bacterial diseases that could be attributable to causing bird mortality were colibacillosis, pasteurellosis and salmonellosis. The investigation identified Salmonella enterica serotype virchow and Salmonella enterica serotype hvittingfoss from dead bird samples of an Australian white ibis and two plumed whistling ducks, respectively. These serotypes have been identified as causing disease in Australians and are therefore relevant to public health. No avian influenza viral RNA was detected from any sick or dead birds by the molecular screening assay. There is an opportunity for establishing a long term passive disease surveillance programme for wild aquatic birds in north Queensland.

The project developed a reliable screening assay "competitive enzyme linked immunosorbent assay" (designated as James Cook University-2) and this assay was used to detect avian influenza viral antibodies from serum samples of wild aquatic birds. A semi-nested PCR approach was designed and applied on direct field reactor samples for amplification and sequencing of different avian influenza viral genes (matrix, haemagglutinin and non-structural protein). Overall findings therefore suggest that there is an opportunity for establishing a long term active and passive surveillance program for monitoring pathogens and diseases of wild aquatic birds in north Queensland, an important region in Australian biosecurity. This would provide valuable information for risk assessment and mitigation and potentially have a significant benefit for public health and the economy for the region and the nation.

Item ID: 21582
Item Type: Thesis (PhD)
Keywords: antibodies, aquatic birds, avian influenza, disease resistance, epidemiology, immunity, infectious diseases, Newcastle disease, North Queensland, prevalence, wild birds
Additional Information:

Publications arising from this thesis are available from the Related URLs field. The publications are:

Hoque, MD, Skerratt, Lee, Cook, A, Khan, S, Grace, D, Alam, MR, Vidal-Diez, A, and Debnath, NC (2011) Factors limiting the health of semi-scavenging ducks in Bangladesh. Tropical Animal Health and Production, 43 (2). pp. 441-450.

Hoque, M.A., Skerratt, L.F., Rahman, M.A., Rabiul Alam Beg, A.B.M., and Debnath, N.C. (2011) A descriptive study of the health of ducklings on smallholdings, Hatia Island, Bangladesh. Journal of Applied Poultry Research, 20 (3). pp. 335-346.

Hoque, M.A., Skerratt, L.F., Rahman, M.A., Beg, A.B.M.Rabiul Alam, and Debnath, N.C. (2010) Factors limiting traditional household duck production in Bangladesh. Tropical Animal Health and Production, 42 (7). pp. 1579-1587.

Hoque, M.A., Skerratt, L.F., Rahman, M.A., Alim, M.A., Grace, D., Gummow, B., Beg, A.B.M. Rabiul Alam, and Debnath, N.C. (2011) Monitoring the health and production of household Jinding ducks on Hatia Island of Bangladesh. Tropical Animal Health and Production, 43 (2). pp. 431-440.

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Date Deposited: 04 Apr 2012 02:54
FoR Codes: 07 AGRICULTURAL AND VETERINARY SCIENCES > 0707 Veterinary Sciences > 070704 Veterinary Epidemiology @ 34%
11 MEDICAL AND HEALTH SCIENCES > 1117 Public Health and Health Services > 111706 Epidemiology @ 33%
07 AGRICULTURAL AND VETERINARY SCIENCES > 0707 Veterinary Sciences > 070712 Veterinary Virology @ 33%
SEO Codes: 92 HEALTH > 9201 Clinical Health (Organs, Diseases and Abnormal Conditions) > 920109 Infectious Diseases @ 34%
97 EXPANDING KNOWLEDGE > 970111 Expanding Knowledge in the Medical and Health Sciences @ 33%
92 HEALTH > 9204 Public Health (excl. Specific Population Health) > 920404 Disease Distribution and Transmission (incl. Surveillance and Response) @ 33%
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