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Analyses of Extended-Spectrum-β-Lactamase, Metallo-β-Lactamase, and AmpC-β-Lactamase Producing Enterobacteriaceae from the Dairy Value Chain in India
Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Biochemistry and Microbiology. Department of Biosciences, International Livestock Research Institute, Nairobi 00100, Kenya; ICAR-National Institute of Veterinary Epidemiology and Disease Informatics, Bengaluru 560064, India.ORCID iD: 0000-0002-9184-449X
Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Biochemistry and Microbiology. Department of Biosciences, International Livestock Research Institute, Nairobi 00100, Kenya; Department of Clinical Sciences, Swedish University of Agricultural Sciences, 75007 Uppsala, Sweden.ORCID iD: 0000-0002-1175-0398
Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Biochemistry and Microbiology.ORCID iD: 0000-0001-8608-6551
Department of Biosciences, International Livestock Research Institute, Nairobi 00100, Kenya;Food and Markets Department, Natural Resources Institute, Chatham Maritime ME4 4TB, UK.ORCID iD: 0000-0002-0195-9489
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2023 (English)In: Antibiotics, E-ISSN 2079-6382, Vol. 12, no 9, article id 1449Article in journal (Refereed) Published
Abstract [en]

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 blaCMY, blaMOX, blaFOX, blaEBC, and blaDHA, associated with AmpC production. Additionally, blaCTX-M1, blaSHV, and blaTEM were detected as ESBL producers, while blaVIM, blaIMP, blaSPM, blaSIM, and blaGIM 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.

Place, publisher, year, edition, pages
MDPI, 2023. Vol. 12, no 9, article id 1449
Keywords [en]
antimicrobial resistance, AMR, enterobacteriaceae, β-lactamase, ESBL, MBL, AmpC, dairy milk, intensification, food safety
National Category
Public Health, Global Health and Social Medicine
Research subject
Microbiology
Identifiers
URN: urn:nbn:se:uu:diva-512928DOI: 10.3390/antibiotics12091449ISI: 001093265700001PubMedID: 37760745OAI: oai:DiVA.org:uu-512928DiVA, id: diva2:1801369
Available from: 2023-09-30 Created: 2023-09-30 Last updated: 2025-10-16Bibliographically approved
In thesis
1. Food safety in India: With focus on antimicrobial resistant bacteria in the dairy and poultry value chains and in traditional fermented food products
Open this publication in new window or tab >>Food safety in India: With focus on antimicrobial resistant bacteria in the dairy and poultry value chains and in traditional fermented food products
2025 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Food safety remains a pressing concern in densely populated countries like India, where contaminated food poses serious health risks, especially to vulnerable groups such as children, the elderly, pregnant women, and immunocompromised individuals. The emergence and spread of antimicrobial resistance (AMR) in food-producing animals and food products further exacerbate these risks, representing a silent but significant threat to public health.

This thesis investigates AMR across dairy and poultry value chains, as well as in traditional fermented food, in diverse Indian regions, using both phenotypic and genotypic analyses. Risk assessments were conducted to evaluate the public health risks associated with AMR in these food systems.

In the dairy chains of Assam and Haryana, methicillin-resistant and β-lactamase-producing bacteria were widely detected. The samples exhibited multidrug-resistant (MDR) strains in milk isolates, with pasteurized milk showing unexpectedly more prevalence of MDR strains, suggesting post-pasteurization contamination due to poor handling. No significant farm-level risk factors, such as herd size or farmer knowledge, could be associated with the presence of AMR.

In poultry from Karnataka and Assam, non-typhoidal Salmonella (NTS) and E. coli were highly prevalent, with Karnataka showing notably higher resistance rates. MDR was common in Salmonella enterica serovars Choleraesuis, Infantis, and Kentucky, posing serious zoonotic risks. Contamination with AMR bacteria in treated water used for feeding birds may indicate biosecurity lapses. Risk modelling confirmed that sampling matrices and regional differences influenced the likelihood of detecting resistant pathogens.

Traditional fermented food products from the North-eastern states of India revealed the presence of lactic acid bacteria (LAB) with probiotic potential in some food products. However, many samples lacked LAB and instead contained pathogenic bacteria, including multi-resistant staphylococci, highlighting hygiene-related risks. This study emphasized the potential for these food products to transmit AMR if consumed without adequate processing.

Collectively, these findings underscore the urgent need for effective pasteurization, improved hygienic handling, rational antibiotic use, and robust biosecurity in food production. The results advocate for integrated food safety strategies, systematic AMR monitoring, and studies in expanded geographical areas to inform public health policies and safeguard India’s food supply.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2025. p. 73
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Medicine, ISSN 1651-6206 ; 2203
Keywords
Food safety, AMR, One Health, Dairy, Poultry, fermented foods, Methicillin, β-lactamase, Non-typhoidal Salmonella, Lactic acid bacteria, MDR, milk, poultry, hygiene, surveillance
National Category
Medical Bioscience Clinical Science Animal and Dairy Science
Identifiers
urn:nbn:se:uu:diva-569747 (URN)978-91-513-2636-8 (ISBN)
Public defence
2025-12-03, A1:107, IMBIM, Husargatan 3, Uppsala, 09:00 (English)
Opponent
Supervisors
Available from: 2025-11-10 Created: 2025-10-16 Last updated: 2025-11-10

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Kumar Dey, TusharLindahl, Johanna FridaLundkvist, ÅkeSharma, Garima

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