Characterization of diverse Salmonella isolated from surface water of a mixed-use watershed and their comparison to human clinical isolates

Authors: CHO, SOHYUN - Non ARS Employee; Hiott, Lari; House, Sandra; Woodley, Tiffanie; McMillan, Elizabeth; SHARMA, POONAM - Oklahoma State University; BARRETT, JOHN - Retired ARS Employee; Adams, Eric; BRANDENBURG, JOSHUA - Centers For Disease Control And Prevention (CDC) - United States; HISE, KELLEY - Centers For Disease Control And Prevention (CDC) - United States; BATEMAN MCDONALD, JACOB - University Of Georgia; OTTESEN, ELIZABETH - University Of Georgia; LIPP, ERIN - University Of Georgia; Jackson, Charlene; Frye, Jonathan

Submitted to: Applied and Environmental Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/11/2022
Publication Date: 5/9/2022
Citation: Cho, S., Hiott, L.M., House, S.L., Woodley, T.A., Mcmillan, E.A., Sharma, P., Barrett, J.B., Adams, E.S., Brandenburg, J.M., Hise, K.B., Bateman Mcdonald, J.M., Ottesen, E.A., Lipp, E.K., Jackson, C.R., Frye, J.G. 2022. Characterization of diverse Salmonella isolated from surface water of a mixed-use watershed and their comparison to human clinical isolates. Applied and Environmental Microbiology. https://doi.org/10.1128/aem.00393-22.
DOI: https://doi.org/10.1128/aem.00393-22

Interpretive Summary: Salmonella has been traditionally considered a zoonotic foodborne pathogen that is associated with food animals; however, cases associated with contaminated water are on the rise. This study was conducted to address the role of surface water as a reservoir and transmission route of Salmonella. We sampled rivers and streams (n = 688) over a 3-year period (2015-2017) in a mixed-use watershed in Athens, GA, and 70.2% of the total stream samples tested positive for Salmonella. A total of 1,190 Salmonella isolates were recovered and characterized phenotypically and genotypically. A wide range of serotypes was identified, including those commonly associated with humans and animals, and about half (46.1%) of the isolates were genetically indistinguishable from human clinical isolates. Fifty-two isolates (4.4%) were resistant to antimicrobials, out of which 43 isolates were resistant to two or more classes of antimicrobials. Persistent contamination of surface water with a high diversity of Salmonella, some of which are genetically indistinguishable from clinical isolates, supports the role of environmental surface water as a source of Salmonella and possible transmission between the aquatic environment and humans, thus playing a role in the epidemiology of Salmonella infections. Furthermore, the presence of antimicrobial resistant Salmonella shows a potential public health safety risk for those exposed to surface water.

Technical Abstract: As the cases of Salmonella infections associated with contaminated water are increasing, this study was conducted to address the role of surface water as a reservoir of Salmonella. We sampled rivers and streams (n = 688) over a 3-year period (2015-2017) in a mixed-use watershed in Athens, GA, and 70.2% of the total stream samples tested positive for Salmonella. A total of 1,190 isolates were recovered and characterized by serotyping, antimicrobial susceptibility testing, and pulsed-field gel electrophoresis (PFGE). A wide range of serotypes was identified, including those commonly associated with humans and animals, with S. Muenchen being predominant (22.7%) and each serotype exhibiting a high degree of strain diversity by PFGE. About half (46.1%) of the isolates had PFGE patterns indistinguishable from human clinical isolates in the CDC PulseNet database. Fifty-two isolates (4.4%) were resistant to antimicrobials, out of which 43 isolates were multidrug resistant (MDR: resistance to two or more classes of antimicrobials). These 52 resistant Salmonella isolates were screened for the presence of antimicrobial resistance genes, plasmid replicons, and class 1 integrons, out of which four representative MDR isolates were selected for whole genome sequencing analysis. The results showed that 28 MDR isolates resistant to 10 antimicrobials had blacmy-2 on an A/C plasmid. Persistent contamination of surface water with a high diversity of Salmonella, some of which are drug resistant and genetically indistinguishable from clinical isolates, supports a role of environmental surface water as a reservoir for and transmission route of this pathogen.