Are we overestimating risk of enteric pathogen spillover from wild birds to humans?

Abstract

Enteric illnesses remain the second largest source of communicable diseases worldwide, and wild birds are suspected sources for human infection. This has led to efforts to reduce pathogen spillover through deterrence of wildlife and removal of wildlife habitat, particularly within farming systems, which can compromise conservation efforts and the ecosystem services wild birds provide. Further, Salmonella spp. are a significant cause of avian mortality, leading to additional conservation concerns. Despite numerous studies of enteric bacteria in wild birds and policies to discourage birds from food systems, we lack a comprehensive understanding of wild bird involvement in transmission of enteric bacteria to humans. Here, we propose a framework for understanding spillover of enteric pathogens from wild birds to humans, which includes pathogen acquisition, reservoir competence and bacterial shedding, contact with people and food, and pathogen survival in the environment. We place the literature into this framework to identify important knowledge gaps. Second, we conduct a meta-analysis of prevalence data for three human enteric pathogens, Campylobacter spp., E. coli, and Salmonella spp., in 431 North American breeding bird species. Our literature review revealed that only 3% of studies addressed the complete system of pathogen transmission. In our meta-analysis, we found a Campylobacter spp. prevalence of 27% across wild birds, while prevalence estimates of pathogenic E. coli (20%) and Salmonella spp. (6.4%) were lower. There was significant bias in which bird species have been tested, with most studies focusing on a small number of taxa that are common near people (e.g. European starlings Sturnus vulgaris and rock pigeons Columba livia) or commonly in contact with human waste (e.g. gulls). No pathogen prevalence data were available for 65% of North American breeding bird species, including many commonly in contact with humans (e.g. black-billed magpie Pica hudsonia and great blue heron Ardea herodias), and our metadata suggest that some under-studied species, taxonomic groups, and guilds may represent equivalent or greater risk to human infection than heavily studied species. We conclude that current data do not provide sufficient information to determine the likelihood of enteric pathogen spillover from wild birds to humans and thus preclude management solutions. The primary focus in the literature on pathogen prevalence likely overestimates the probability of enteric pathogen spillover from wild birds to humans because a pathogen must survive long enough at an infectious dose and be a strain that is able to colonize humans to cause infection. We propose that future research should focus on the large number of under-studied species commonly in contact with people and food production and demonstrate shedding of bacterial strains pathogenic to humans into the environment where people may contact them. Finally, studies assessing the duration and intensity of bacterial shedding and survival of bacteria in the environme...

Agricultural intensification heightens food safety risks posed by wild birds

“…prevalence in both our environmental faecal samples (13.1%) and mist-net samples (10.2%) than Smith, Snyder, et al (2020) found in their meta-analysis collating prevalence estimates across species (27%), including their estimate for passerines (28%), which formed the majority of our samples. The estimate reported by Smith, Snyder, et al (2020) was likely inflated due to the majority of past research focusing on a small number of synanthropic species. For example, Hald et al (2016) found an overall Campylobacter spp.…”

“…These 'buyer agreements' are assumed to improve food safety but are based on few data, including a few sensationalized outbreaks linked to wildlife (Beretti & Stuart, 2008;Gardner et al, 2011;Karp et al, 2015;Smith, Snyder, et al, 2020). Importantly, our finding that Campylobacter spp.…”

“…greater contact with conspecific faeces; Barron, Gervasi, Pruitt, & Martin, 2015;Carlson et al, 2011;Gaulker et al, 2012;Heisterberg et al, 1984;Ostfeld et al, 2014;Rodewald, 2015;Smith et al, 2019;Smith, Snyder, et al, 2020 (Rothstein, Verner, & Steven, 1984).…”

“…Therefore, birds inhabiting farms embedded within landscapes with greater environmental pathogen prevalence, such as those with high contamination of livestock waste, may be more likely to encounter foodborne pathogens ( Figure 1a; Hald et al, 2016;Hernandez et al, 2016). At the same time, landscapes with high densities of livestock may attract more competent reservoir host species (Figure 1a,b;Smith, Snyder, et al, 2020). Additionally, on-farm crop-livestock integration could increase the likelihood of spillover by both increasing the overall bird community competence and by altering contact rates between birds, livestock hosts and produce (Figure 1c Here, we examine the roles of landscape context and on-farm crop-livestock integration in the likelihood of spillover of foodborne pathogens from birds to humans in brassica production.…”

European Starlings (Sturnus vulgaris) as Vectors and Reservoirs of Pathogens Affecting Humans and Domestic Livestock

“…It is responsible for disease in humans and many mammalian and avian livestock species, including cows, pigs, goats, sheep, and poultry of all types. Concerns about starlings focus mainly on the spread of Salmonella among livestock and poultry, though direct transmission to humans via fecal matter in human food crops [ 28 ] or urban areas is also a potential concern [ 46 ]. For livestock, the concern is both economic loss due to animal illness, and secondarily, transmission to humans via contaminated products (meat, eggs, dairy products, etc.).…”