In vitro invasiveness and antimicrobial resistance of Salmonella enterica subspecies isolated from wild and captive reptiles

Andrea McWhorter; Jane Owens; Mary Valcanis; Liberty Olds; Cecilia Myers; Ian Smith; Darren Trott; David McLelland

doi:10.1111/zph.12820

In vitro invasiveness and antimicrobial resistance of Salmonella enterica subspecies isolated from wild and captive reptiles

Zoonoses Public Health. 2021 Aug;68(5):402-412. doi: 10.1111/zph.12820. Epub 2021 Mar 2.

Authors

Andrea McWhorter¹, Jane Owens², Mary Valcanis³, Liberty Olds⁴, Cecilia Myers⁵, Ian Smith⁴, Darren Trott¹, David McLelland⁴

Affiliations

¹ School of Animal and Veterinary Sciences, University of Adelaide, Roseworthy, SA, Australia.
² Faculty of Veterinary and Agricultural Science, University of Melbourne, Parkville, Vic., Australia.
³ Department of Microbiology and Immunology, Peter Doherty Institute for Infection and Immunity, Microbiological Diagnostic Unit-Public Health Laboratory, University of Melbourne, Melbourne, Vic., Australia.
⁴ Adelaide Zoo, Zoos South Australia, SA, Australia.
⁵ Dunkeld Pastoral Co Pty Ltd, Dunkeld, Vic., Australia.

PMID: 33655685
DOI: 10.1111/zph.12820

Abstract

Reptiles are carriers of Salmonella and can intermittently shed bacteria in their faeces. Contact with snakes and lizards is a source of human salmonellosis. Here, two populations of reptiles, wild and captive were surveyed for Salmonella. One hundred thirty wild-caught reptiles were sampled for Salmonella including 2 turtle, 9 snake and 31 lizard species. Fifty-two of 130 (40%) animals were Salmonella positive: one of 5 (20%) turtles, 7 of 14 (50%) snakes and 44 of 111 (39.6%) lizards. One hundred twenty-two reptiles were sampled from a zoo collection including 1 turtle, 6 tortoise, 9 lizard, 14 snake and 1 crocodile species. Forty-two of 122 (34.4%) captive reptiles sampled were Salmonella positive. Salmonella was most commonly isolated from lizards and snakes. Fifteen serotypes were identified from zoo and 19 from wild-caught reptiles and most were members of subspecies enterica (I), salamae (II), arizonae (IIIa) or diarizonae (IIIb). Antimicrobial susceptibility testing was conducted on all Salmonella isolates; only two exhibited resistance, a Salmonella subsp. (II) ser. 21:z₁₀ :z₆ (Wandsbek) isolate cultured from a wild-caught reptile and a Salmonella Typhimurium DT120 isolated from a captive snake. The invasive capacity of reptile-associated Salmonella strains into cultured human intestinal epithelial (Caco2) and mouse macrophages cell lines (J774A.1) was also investigated. All isolates were invasive into both cell lines. Significant (P $\leq$ 0.001) variability in invasiveness into polarized Caco2 cells was observed. Salmonella Eastbourne exhibited the highest invasiveness into Caco2 cells and Salmonella Chester the lowest, with mean per cent recoveries of 19.99 $\pm$ 0.32 and 1.23 $\pm$ 0.30, respectively. Invasion into J774A.1 macrophages was also variable but was not significant. Salmonella subsp. II ser. 17:g,t:- (Bleadon) exhibited the highest invasiveness into J774A.1 with a mean per cent recovery of 10.19 $\pm$ 0.19. Thus, reptile-associated Salmonellae are likely to have different capacities to cause disease in humans.

Keywords: Salmonella; Caco2; J774.A1; invasiveness; reptile.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Animals, Wild*
Animals, Zoo*
Anti-Bacterial Agents / pharmacology*
Australia / epidemiology
Drug Resistance, Bacterial
Reptiles*
Salmonella Infections, Animal / epidemiology
Salmonella Infections, Animal / microbiology*
Salmonella enterica / drug effects
Salmonella enterica / pathogenicity*

Substances

Anti-Bacterial Agents