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 environment in bird faeces will help provide crucial missing information necessary to calculate spillover probability. Addressing these essential knowledge gaps will support policy to reduce enteric pathogen spillover to humans and enhance bird conservation efforts that are currently undermined by unsupported fears of pathogen spillover from wild birds.

Keywords: Campylobacter spp.; E. coli; Salmonella spp.; agroecology; enteric illness; food safety; wild birds.

Figure 1

(A) Conceptual diagram outlining steps from bacterial acquisition to human infection. Icons below flow chart show a bird being exposed to E. coli at a bird feeder, E. coli replicating within a bird host, a bird defecating E. coli on a broccoli plant, and a hospital sign to indicate human enteric illness. (B) Percentage of studies included in meta‐analysis that reported data pertaining to exposure, reservoir competence, contact, and bacterial survival and transmission. (C) Percentage of studies that reported data on 0, 1, 2, 3, or 4 of the aspects in the conceptual diagram (exposure, reservoir competence, contact, and bacterial survival and transmission).

Figure 2

Conceptual diagram of likelihood of Campylobacter spp. spillover from mallards (MALL) to humans. (A) Campylobacter spp. prevalence in mallards estimated from meta‐analysis (26%) on left and prevalence of Campylobacter isolates matched with human disease cases estimated from Colles et al. (2011) (26% prevalence of which 0.9% of isolates are known to cause human disease) on right. (B) Estimated prevalence of mallards in farmland from Smith et al. (2019) farm bird database (8.3% of points) on left and area likely to have mallards with human isolates on left (about 2 in 10000). (C) Estimated survival time of Campylobacter spp. in mallard faeces modified from Canada goose faeces study in Moriarty et al. (2012). (D) Flow chart to determine whether spillover will occur.

Figure 3

Scatterplot showing the percentage of pathogen observations (obs) belonging to each taxonomic order versus the % of eBird observations (eBird.org) each taxon comprises (Sullivan et al., 2009). (A), (C) and (E) show all orders. (B), (D) and (F) show orders that comprise less than 10% of pathogen observations and less than 10% of eBird observations (boxed regions in A, C and E, respectively).

Figure 4

Pie charts showing (A, C) the proportion of species or (B, D) relative abundances for which enough observations exist to estimate pathogen prevalence for Campylobacter spp., pathogenic E. coli and Salmonella spp. (purple), two of the three pathogens (dark blue), one of these three pathogens (blue), species with some data but insufficient numbers to determine prevalence (green), and no observations (yellow). (A) North American (NA) breeding bird species found in the North American Breeding Bird Survey (Sauer et al., 2017), (B) eBird (ebird.org) relative abundances (Sullivan et al., 2009), (C) West Coast farm bird species observed by Smith et al. (2019), and (D) farm bird species relative abundances from the database in Smith et al. (2019). Path = pathogens.

Figure 5

Flow chart suggesting directions for future research.

Figure 6

Comparison of estimated Salmonella spp. prevalence (+SE) by substance tested for the three species with data from the most individual studies. (A) European starling, (B) house sparrow, and (C) rock pigeon. Different letters indicate significant differences using pairwise Tukey HSD tests.

Figure 7

Estimated prevalence (+SE) of enteric pathogens by (B–D) diet guild and (F–H) foraging strata, and number of species within each diet guild (A) and foraging strata (E). In A and E, pattern indicates insufficient observations to determine prevalence for any of the three pathogens while white indicates species for which enough observations were available to determine prevalence for one or more pathogens. (B, F) Campylobacter spp., (C, G) pathogenic E. coli, and (D, H) Salmonella spp. for each diet guild or each foraging strata. Colour indicates proportion of positive individuals for each estimate from each taxonomic order. Pattern indicates insufficient observations to determine prevalence within an order. Spaces with no error bars indicate no observations in the literature.