Investigating Clinically Important Antimicrobial Resistant Bacteria in Australian Wildlife

Xing Li

doi:10.60867/00000168

Antimicrobial resistance (AMR) is a growing One Health concern, challenging human, animal, and environmental health. Despite increasing reports of AMR in wildlife globally, little is known regarding antimicrobial resistant bacteria circulating in Australian wildlife. Using culture-based methods and whole genome sequencing (WGS), this study investigated the occurrence, AMR profiles, genomic characteristics, and potential transmission risks of clinically important bacteria in six representative Australian wildlife species, including western grey kangaroo (Macropus fuliginosus), quenda (Isoodon fusciventer), pelican (Pelecanus conspicillatus), galah (Eolophus roseicapilla), shingleback skink (Tiliqua rugosa), and long-necked turtle (Chelodina colliei). Skin, nasal, and cloacal samples were collected from 180 animals (30 of each species) on admission to the WA Wildlife Hospital, Western Australia, and 97 animals after seven days of hospitalisation. Staphylococcus aureus was isolated from 11.7% (95% CI: 7.4%-17.3%) of the animals on admission and 16.5% (95% CI: 9.7%-25.4%) after seven days of hospitalisation. In a diversity of S. aureus lineages, multiple virulence factors, including the human-specific immune evasion cluster (IEC), and AMR genes, including aac(6’)-aph(2''), blaZ, erm(T), and tet(L), were identified. Notably, two mecA-positive methicillin-resistant S. aureus (MRSA) were isolated from two pelicans after seven days of hospitalisation. The two MRSA were identified as ST1- IV and ST93-IV, two community-associated MRSA clones frequently identified in Australia, suggesting possible anthroponotic transmission. In the same investigation of MRSA, methicillin-resistant coagulase-negadve staphylococci (MRCoNS) were isolated from 7.2% (95% CI: 3.9%-12.0%) of the animals on admission and 17.5% (95% CI: 10.6%-26.6%) after seven days of hospitalisation. The odds of detecting MRCoNS were significantly higher after seven days of hospitalisation (OR=2.72, 95% CI: 1.18- 6.41, p<0.05). The mecA gene was identified in various staphylococcal species, including S. haemolyticus, S. saprophyticus, S. hominis, S. epidermidis, and S. warneri, and mecC was identified in S. xylosus. Diverse staphylococcal cassette chromosome mec (SCCmec) elements were identified. The findings highlight wildlife as a potential reservoir of methicillin resistance. In addition to MRCoNS, methicillin-resistant Mammaliicoccus sciuri (MRMS) was isolated from 4.4% (95% CI: 1.9%-8.6%) of the animals on admission and 23.7% (95% CI: 15.7%-33.4%) after seven days of hospitalisation. The odds of detecting MRMS were significantly higher after seven days of hospitalisation (OR: 6.63, 95% CI: 2.71-17.97, p<0.001). The mecA gene, located on a SCCmec type III (3A), was identified in the ST81 and ST337 isolates. The ST321 isolates harboured mecA and mecC, which were located on a SCCmec-mecC hybrid, consisting of a SCCmec type III (3A) element fused to a class E mec complex (blaZ-mecC-mecR1-mecI). To the best of our knowledge, this is the first report of a SCCmec-mecC hybrid in Australia. Enterococcus faecium was isolated from 8.9% (16/180, 95% CI: 5.2%-14.0%) of the animals on admission and 15.5% (15/97, 95% CI: 8.9%-24.2%) after seven days of hospitalisation. Identified AMR genes included ant(6)-Ia, aph(3')-IIIa, cat, dfrG, erm(B), lnu(B), lnu(G), lsa(E), sat4, spw, tet(L), and tet(M). Vancomycin resistance genes were not detected. Extended-spectrum β-lactamase (ESBL)/AmpC-producing Escherichia coli was isolated from 6.1% (11/180, 95% CI: 3.1%-10.7%) of the animals on admission, and 18.6% (18/97, 95% CI: 11.4%-27.7%) after seven days of hospitalisation. The odds of detecting ESBL/AmpCproducing E. coli were significantly higher after seven days of hospitalisation (OR: 3.48, 95% CI: 1.48-8.58, p<0.01). ESBL/AmpC-encoding genes blaCTX-M-15, blaCTX-M-27, blaCTX-M-55, blaCTX-M- 65, blaCMY-2, blaCMY-42, and blaDHA-1 were identified. In addition, the carbapenemase-encoding gene blaOXA-181 was identified from six animals after seven days of hospitalisation, which, to our knowledge, has not previously been reported in Australian wildlife. An epidemiological review of risk factors found antimicrobial resistant bacteria were detected in the urban areas, as well as regional and remote towns. Clustering was observed in pelicans from the Rockingham/Penguin Island area. The detection of MRCoNS and MRMS in the animals after seven days of hospitalisation was significantly associated with the use of amoxicillin-clavulanic acid during hospitalisation. Collectively, Australian wildlife may be an overlooked reservoir of antimicrobial resistant bacteria, highlighting the importance of incorporating wildlife into AMR surveillance with a One Health approach. In addition, wildlife rescue settings may be an under-recognised human-wildlife-environment interface facilitating the acquisition and transmission of clinically significant antimicrobial resistant bacteria.

Investigating Clinically Important Antimicrobial Resistant Bacteria in Australian Wildlife

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