Avian influenza prevalence among hunter-harvested birds in a remote Canadian First Nation community

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Introduction

Recently, we reported that over half the subsistence hunters from Fort Albany First Nation were aware of avian influenza virus (AIV) being a potential health hazard¹. Over a quarter of the total participants perceived a risk of contracting this virus while harvesting birds¹. The perception of this risk is not unfounded as several studies have noted that hunters and some bird handlers, such as wildlife biologists, may be at increased risk of exposure to highly pathogenic avian influenza A (HPAI) viruses^2-6. Within hunters, HPAI exposure risk varies greatly by location due to the viral prevalence observed during different hunting seasons in birds, species of bird, the average number of birds harvested per hunting period, and the age and ratio of juveniles to adult birds harvested^7,8. The group of hunters in this study is particularly vulnerable to exposure due to their subsistence lifestyle combined with the knowledge that HPAI outbreaks have occurred in migratory waterfowl, which is their primary hunting target^9,10.

Although relatively rare in human occurrence, the high fatality rate associated with HPAI infection creates a continued cause for human health concern¹¹. The most recent data (1 May 2015) from the WHO reports 840 cases of H5N1 resulting in 447 deaths since 2003 across the globe¹². Furthermore, the high hunter contact rate of birds in this study may act as an additional danger due to these people's remoteness and isolation from adequate medical facilities that can recognize and combat this virus. Campagna and colleagues (2011) recently reported that seropositivity of 10 zoonotic infections from two First Nations communities in Quebec was associated with hunting practices¹³. Because many remote First Nations communities rely on hunted meats for subsistence, they are at an increased risk of AIV exposure as well. In response to community hunter and Band Council (locally elected government) concerns about HPAI (particularly the H5 and H7 subtypes) in the game birds harvested from the Fort Albany First Nation region of northern Ontario, Canada, we assessed a range of hunted fowl for influenza A virus.

Methods

All sampling was conducted under the guidance of a trained local community coordinator, all hunting was performed by local traditional hunters, and the project was approved by the Fort Albany Band Council. Cloacal swabs (Starplex Scientific, Etobicoke, Canada) were taken in the spring and autumn hunting seasons of 2013 and in the spring hunting season of 2014. Samples were frozen at -20^oC and shipped directly to the laboratory for analysis. Total nucleic acids were extracted from the cloacal swab samples using the MagMAX-96 viral ribonucleic acid (RNA) Isolation Kit in a MagMAX Express-96 Magnetic Particle Processor (Applied Biosystems Inc., Foster City, California). Extracted nucleic acids were screened for the presence of influenza A virus RNA using a real-time reverse transcription polymerase chain reaction targeting a conserved region of influenza A virus M gene¹⁴. For hemagglutinin gene subtyping, influenza A virus RNA was amplified using a reverse transcription polymerase chain reaction (PCR)¹⁵ and nucleotide sequences of PCR products were determined at the University of Guelph Laboratory Services sequencing facility. Sequences were assembled using the Lasergene software (DNAStar Inc., https://www.dnastar.com) and compared with hemagglutinin gene sequences in GenBank, the US National Institutes of Health genetic sequence database. In total, 304 cloacal swabs were analyzed; the number of samples by species is presented in Table 1. The results of this project were presented to the community under the direction of the community coordinator and the researchers.

Table 1: Number of cloacal swabs, by wild game bird type, obtained in a remote First Nation community in subArctic Ontario, Canada, 2013 and 2014

Results

A 5.26% (n=16) AIV prevalence was found in the 304 cloacal swab samples analyzed. Of the 16 positive samples, 12 were found in mallard ducks, 3 were found in snow geese (wavies), and 1 positive sample was found in partridge (Fig1). Three mallard ducks were successfully subtyped for H3 and one mallard duck was subtyped for H4. The remaining positive samples were unable to be subtyped either due to being positive for multiple strains of avian influenza A, or due to reduced sensitivities in the conventional PCR process used to generate the template for sequencing.

Figure 1: Point prevalence of avian influenza virus in individual bird species sampled and total sample population.

Discussion

To our knowledge, the pilot work presented herein is the first to examine hunter-harvested birds from a subsistence First Nation community. Globally, surveillance and reporting of avian influenza remains weak^16,17, and the community-level data presented here is the first step towards mapping risk and exposure by identifying which bird species may be acting as reservoirs or pathogen vectors¹⁸. Others have successfully used surveillance data to assess risk from avian influenza^19,20 and similar application of this data could provide added security to subsistence hunting communities.

HPAI remains a concern globally, and those who hunt and handle birds may be at additional risk. However, no HPAI subtypes were identified in any of the samples collected by community members of Fort Albany First Nation; only low pathogenic AIV was found. The H3 and H4 low pathogenic AIV subtypes are most commonly found among dabbling ducks⁸, and this was represented in this study. Ferro et al. found that dabbling ducks and snow geese had lower prevalences of AIV (10.9% and 0%, respectively) in hunter-harvested waterfowl from the Texas coast²¹ when compared to our study (28.6% for mallard duck only and 6.3%, respectively). AIV prevalence within dabbling ducks varies, and others have reported a 24.3% prevalence in mallard ducks, which is similar to our value²². Stallknecht et al. found that prevalence of AIV varied by season²³, and others have noted that age, species, location, and number of birds harvested all cause variation in AIV prevalence^7,8,24. While it is possible that we did not capture true prevalence of all birds from the Fort Albany community, the majority of the samples were collected during the two main hunting seasons (spring and autumn) and this represents the highest potential hazard period for hunters. Additionally, research suggests that northern breeding grounds in colder environments may act as reservoirs for some types of AIV, even though they might seem unfavorable²⁵.

Conclusions

Community-level surveillance of AIV in remote subsistence hunting communities is an important aspect of identifying risks and working to control a potential outbreak that may otherwise lead to adverse social and economic effects²⁶. While general Canadian pandemic plans²⁷ and recommendations for First Nations communities²⁸ have been developed, data such as that presented here can help address monitoring gaps and improve hunter education. This is an important first step to assessing risk as Aboriginal (First Nations, Inuit, and Metis} people have had the highest rate of H1N1 worldwide²⁹ and a HPAI outbreak in a remote community would have significant adverse consequences. Although only low pathogenic AIV was found in the 304 cloacal swab samples tested herein, ongoing monitoring of birds from areas with potentially high exposure groups such as subsistence hunters is recommended.

Acknowledgements

We wish to thank the hunters of Fort Albany First Nation who participated in this research project. Funding was provided by Health Canada's Regional First Nations Environmental Contaminants Program and a Ryerson University Faculty of Community Services Seed Grant.

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