Prevalence and molecular characterization of Salmonella isolated from wild birds in fresh produce environments

Jared C Smith; Sofia Varriano; Kerrie Roach; Zach Snipes; Joshua L Dawson; Justin Shealy; Laurel L Dunn; William E Snyder; Nikki W Shariat

doi:10.3389/fmicb.2023.1272916

Prevalence and molecular characterization of Salmonella isolated from wild birds in fresh produce environments

Front Microbiol. 2023 Nov 7:14:1272916. doi: 10.3389/fmicb.2023.1272916. eCollection 2023.

Authors

Jared C Smith¹, Sofia Varriano², Kerrie Roach³, Zach Snipes³, Joshua L Dawson⁴, Justin Shealy⁵, Laurel L Dunn^{6

7}, William E Snyder², Nikki W Shariat^{1

7}

Affiliations

¹ Departments of Population Health and Microbiology, University of Georgia, Athens, GA, United States.
² Department of Entomology, University of Georgia, Athens, GA, United States.
³ Department of Plant Industry, Clemson University Extension, Charleston, SC, United States.
⁴ Fort Valley State University Extension, Fort Valley, GA, United States.
⁵ College of Agricultural and Environmental Sciences, University of Georgia Extension, Athens, GA, United States.
⁶ Department of Food Science and Technology, University of Georgia, Athens, GA, United States.
⁷ Center for Food Safety, University of Georgia, Griffin, GA, United States.

Abstract

Wild birds pose a difficult food safety risk to manage because they can avoid traditional wildlife mitigation strategies, such as fences. Birds often use agricultural fields and structures as foraging and nesting areas, which can lead to defecation on crops and subsequent transfer of foodborne pathogens. To assess the food safety risk associated with these events, wild bird feces were collected from produce fields across the southeastern United States during the 2021 and 2022 growing seasons. In total 773 fecal samples were collected from 45 farms across Florida, Georgia, South Carolina, and Tennessee, and 2.1% (n = 16) of samples were Salmonella-positive. Importantly, 75% of Salmonella were isolated from moist feces, showing reduced Salmonella viability when feces dry out. 16S microbiome analysis showed that presence of culturable Salmonella in moist feces correlated to a higher proportion of the Enterobacteriaceae family. From the Salmonella-positive samples, 62.5% (10/16) contained multi-serovar Salmonella populations. Overall, 13 serovars were detected, including six most commonly attributed to human illness (Enteriditis, Newport, Typhimurium, Infantis, Saintpaul, and Muenchen). PCR screening identified an additional 59 Salmonella-positive fecal samples, which were distributed across moist (n = 44) and dried feces (n = 15). On-farm point counts and molecular identification from fecal samples identified 57 bird species, including for 10 Salmonella-positive fecal samples. Overall, there was a low prevalence of Salmonella in fecal samples, especially in dried feces, and we found no evidence of Salmonella transmission to proximal foliage or produce. Fecal samples collected in farms close together shared highly related isolates by whole genome sequencing and also had highly similar Salmonella populations with comparable relative frequencies of the same serovars, suggesting the birds acquired Salmonella from a common source.

Keywords: Salmonella; WGS; food safety; produce; wild birds.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work was supported by a grant from the Center for Produce Safety to NS.