Analyses of Extended-Spectrum-β-Lactamase, Metallo-β-Lactamase, and AmpC-β-Lactamase Producing Enterobacteriaceae from the Dairy Value Chain in India

Tushar Kumar Dey; Johanna Frida Lindahl; Åke Lundkvist; Delia Grace; Ram Pratim Deka; Rajeswari Shome; Samiran Bandyopadhyay; Naresh Kumar Goyal; Garima Sharma; Bibek Ranjan Shome

doi:10.3390/antibiotics12091449

Analyses of Extended-Spectrum-β-Lactamase, Metallo-β-Lactamase, and AmpC-β-Lactamase Producing Enterobacteriaceae from the Dairy Value Chain in India

Antibiotics (Basel). 2023 Sep 14;12(9):1449. doi: 10.3390/antibiotics12091449.

Authors

Tushar Kumar Dey^{1

2

3}, Johanna Frida Lindahl^{1

2

4}, Åke Lundkvist², Delia Grace^{1

5}, Ram Pratim Deka⁶, Rajeswari Shome³, Samiran Bandyopadhyay⁷, Naresh Kumar Goyal⁸, Garima Sharma^{1

2}, Bibek Ranjan Shome³

Affiliations

¹ Department of Biosciences, International Livestock Research Institute, Nairobi 00100, Kenya.
² Zoonosis Science Center, Department of Medical Biochemistry and Microbiology, Uppsala University, 75123 Uppsala, Sweden.
³ ICAR-National Institute of Veterinary Epidemiology and Disease Informatics, Bengaluru 560064, India.
⁴ Department of Clinical Sciences, Swedish University of Agricultural Sciences, 75007 Uppsala, Sweden.
⁵ Food and Markets Department, Natural Resources Institute, Chatham Maritime ME4 4TB, UK.
⁶ International Livestock Research Institute, Regional Office for South Asia, New Delhi 110012, India.
⁷ Eastern Regional Station, ICAR-Indian Veterinary Research Institute, Kolkata 700037, India.
⁸ Dairy Microbiology Division, National Dairy Research Institute, Karnal 132001, India.

Abstract

The consumption of milk contaminated with antibiotic-resistant bacteria poses a significant health threat to humans. This study aimed to investigate the prevalence of Enterobacteriaceae producing β-lactamases (ESBL, MBL, and AmpC) in cow and buffalo milk samples from two Indian states, Haryana and Assam. A total of 401 milk samples were collected from dairy farmers and vendors in the specified districts. Microbiological assays, antibiotic susceptibility testing, and PCR-based genotyping were employed to analyze 421 Gram-negative bacterial isolates. The overall prevalence of β-lactamase genes was 10% (confidence interval (CI) (7-13)), with higher rates in Haryana (13%, CI (9-19)) compared to Assam (7%, CI (4-11)). The identified β-lactamase genes in isolates were bla_CMY, bla_MOX, bla_FOX, bla_EBC, and bla_DHA, associated with AmpC production. Additionally, bla_CTX-M1, bla_SHV, and bla_TEM were detected as ESBL producers, while bla_VIM, bla_IMP, bla_SPM, bla_SIM, and bla_GIM were identified as MBL producers. Notably, Shigella spp. were the dominant β-lactamase producers among identified Enterobacteriaceae. This study highlights the presence of various prevalent β-lactamase genes in milk isolates, indicating the potential risk of antimicrobial-resistant bacteria in dairy products. The presence of β-lactam resistance raises concern as this could restrict antibiotic options for treatment. The discordance between genotypic and phenotypic methods emphasizes the necessity for comprehensive approaches that integrate both techniques to accurately assess antibiotic resistance. Urgent collaborative action incorporating rational and regulated use of antibiotics across the dairy value chain is required to address the global challenge of β-lactam resistance.

Keywords: AMR; AmpC; ESBL; MBL; antimicrobial resistance; dairy milk; enterobacteriaceae; food safety; intensification; β-lactamase.

Grants and funding

ICAR & CGIAR/This research was funded by the Indian Council of Agricultural Research (ICAR), the CGIAR Research Programme on Agriculture for Nutrition and Health, and the CGIAR research initiative One Health.