Evidence of potentially unrelated AmpC beta-lactamase producing Enterobacteriaceae from cattle, cattle products and hospital environments commonly harboring the blaACC resistance determinant

Keduetswe Matloko; Justine Fri; Tshepiso Pleasure Ateba; Lesego G Molale-Tom; Collins Njie Ateba

doi:10.1371/journal.pone.0253647

Evidence of potentially unrelated AmpC beta-lactamase producing Enterobacteriaceae from cattle, cattle products and hospital environments commonly harboring the blaACC resistance determinant

PLoS One. 2021 Jul 29;16(7):e0253647. doi: 10.1371/journal.pone.0253647. eCollection 2021.

Authors

Keduetswe Matloko¹, Justine Fri^{1

2}, Tshepiso Pleasure Ateba³, Lesego G Molale-Tom⁴, Collins Njie Ateba^{1

2}

Affiliations

¹ Antimicrobial Resistance and Phage Biocontrol Research Group, Department of Microbiology, School of Biological Sciences, Faculty of Natural and Agricultural Sciences, North-West University, Mmabatho, South Africa.
² Food Security and Safety Niche Area, Faculty of Natural and Agricultural Sciences, North-West University, Mmabatho, South Africa.
³ Centre for Animal Health Studies, Faculty of Natural and Agricultural Sciences, North-West University, Mmabatho, South Africa.
⁴ Unit for Environmental Sciences and Management - Microbiology, North-West University, Potchefstroom, South Africa.

Abstract

The occurrence and genetic relatedness of AmpC beta-lactamase producing Enterobacteriaceae isolated from clinical environments, groundwater, beef, human and cattle faeces were investigated. One hundred seventy-seven (177) samples were collected and cultured on MacConkey agar. A total of 203 non-repetitive isolates were characterised using genus/species-specific PCRs and the identified isolates were subjected to antibiotic susceptibility testing. The production of AmpC beta-lactamases was evaluated using cefoxitin disc, confirmed by the D96C detection test and their encoding genes detected by PCR. The D64C extended-spectrum beta-lactamases (ESBL) test was also performed to appraise ESBLs/AmpC co-production. The genetic fingerprints of AmpC beta-lactamase producers were determined by ERIC-PCR. A total of 116 isolates were identified as E. coli (n = 65), Shigella spp. (n = 36) and Klebsiella pneumoniae (n = 15). Ciprofloxacin resistance (44.4-55.4%) was the most frequent and resistance against the Cephem antibiotics ranged from 15-43.1% for E. coli, 25-36.1% for Shigella spp., and 20-40% for K. pneumoniae. On the other hand, these bacteria strains were most sensitive to Amikacin (0%), Meropenem (2.8%) and Piperacillin-Tazobactam (6.7%) respectively. Nineteen (16.4%) isolates comprising 16 E. coli and 3 Shigella spp. were confirmed as AmpC beta-lactamase producers. However, only E. coli isolates possessed the corresponding resistance determinants: blaACC (73.7%, n = 14), blaCIT (26%, n = 5), blaDHA (11%, n = 2) and blaFOX (16%, n = 3). Thirty-four (27.3%) Enterobacteriaceae strains were confirmed as ESBL producers and a large proportion (79.4%, n = 27) harboured the blaTEM gene, however, only two were ESBLs/AmpC co-producers. Genetic fingerprinting of the AmpC beta-lactamase-producing E. coli isolates revealed low similarity between isolates. In conclusion, the findings indicate the presence of AmpC beta-lactamase-producing Enterobacteriaceae from cattle, beef products and hospital environments that commonly harbour the associated resistance determinants especially the blaACC gene, nonetheless, there is limited possible cross-contamination between these environments.

Publication types

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

MeSH terms

Animals
Anti-Bacterial Agents*
Bacteria / genetics
Bacterial Proteins*
Cattle
Microbial Sensitivity Tests
beta-Lactamases*

Substances

Anti-Bacterial Agents
Bacterial Proteins
AmpC beta-lactamases
beta-Lactamases

Grants and funding

The authors are grateful to the National Research Foundation of South Africa for their financial support provided to MK under the DST-NRF Internship Programme (2018 – 2019). The North-West University is highly appreciated for providing the space for bench work. This project was also supported in part by an incentive funding for rated researchers funding (grant UID number 109187) awarded to CNA by the National Research Fund of South Africa.