Shedding of Extended Spectrum β-Lactamase and AmpC-producing Enterobacteriaceae (ESBL/AmpC-E) in Petting Zoos in Israel: a Zoonotic Hazard? -

Anat Shnaiderman Torban ¹ Amir Steinman ¹ Gal Meidan ¹ Yossi Paitan ^2,3 Wiessam Abu Ahmad ⁴ Shiri Navon-Venezia ⁵

¹Koret School of Veterinary Medicine (KSVM), The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Israel
²Clinical Microbiology and Immunology, Sackler Faculty of Medicine, Tel Aviv University, Israel
³Clinical Microbiology Lab, Meir Medical Center, Israel
⁴Hadassah Braun School of Public Health and Community Medicine, Hebrew University of Jerusalem, Israel
⁵Molecular Biology, Faculty of Natural Science, Ariel University, Israel

Background: ESBL/AmpC-E are a concern in human and veterinary medicine. Petting zoos are popular and allow exposure of visitors to diverse animal species. There is a significant concern regarding the zoonotic potential, mainly through oro-fecal route.

Aim: To investigate the prevalence, molecular epidemiology and risk factors for ESBL/AmpC-E shedding in petting zoos.

Methods: A prospective cross-sectional study was performed in eight petting zoos. Samples were enriched, plated (CHROMagarESBL) and sub-cultured. Bacterial species and antibiotic susceptibility profiles were determined (Vitek-2), as well as sequence types (MLST). ESBL and AmpC genes (CTX-M, SHV, TEM, CMY-2) were identified (PCR and sequencing). Owners’ questioners were reviewed for risk factor analysis (SPSS).

Results: ESBL/AmpC-E carriage rate was 12% (n=28/228, 95% CI 8-17%), with 35 recovered bacteria: 77% from feces (n=27/35, 95% CI 60-90%) and 23% from skin/fur/feathers (n=8/35, 95% CI 10-40%). The main species were Enterobacter sp. (55%), Escherichia coli (31%) and Citrobacter sp. (14%). The main ESBL gene was CTX-M-1 group (17%) and 20% of the AmpC-E were CMY-2-positive. MLST revealed eight different E. cloacae STs and six E. coli STs, including ST656 and ST127, of ETEC and UPEC, respectively. In a univariate analysis, carriage was associated with antibiotic therapy (p=0.038 and p=0.011 for feces and skin/fur/feathers, respectively) and with petting permission policy (p=0.023). In a logistic regression model, antimicrobial therapy was identified as a risk factor (OR=7.34).

Conclusion: Petting zoos may serve as a reservoir for ESBL/AmpC-E. Acknowledging the psychological and educational value of petting zoos, we highly recommend promoting hygiene and veterinary guidelines in these facilities.

Significance: We describe a potential zoonosis, which was not reported in petting zoos. The prevalence and risk factors identified in this study reveal the necessity of guidelines and regulations.