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Food safety in India: With focus on antimicrobial resistant bacteria in the dairy and poultry value chains and in traditional fermented food products
Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Biochemistry and Microbiology. (Ake Lundkvist)ORCID iD: 0000-0002-9184-449X
2025 (English)Doctoral thesis, comprehensive summary (Other academic)
Description
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 [en]
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: urn:nbn:se:uu:diva-569747ISBN: 978-91-513-2636-8 (print)OAI: oai:DiVA.org:uu-569747DiVA, id: diva2:2006732
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
List of papers
1. Molecular Characterization of Methicillin-Resistant Staphylococci from the Dairy Value Chain in Two Indian States
Open this publication in new window or tab >>Molecular Characterization of Methicillin-Resistant Staphylococci from the Dairy Value Chain in Two Indian States
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2023 (English)In: Pathogens, E-ISSN 2076-0817, Vol. 12, no 2, article id 344Article in journal (Refereed) Published
Abstract [en]

Bovine milk and milk products may contain pathogens, antimicrobial resistant bacteria, and antibiotic residues that could harm consumers. We analyzed 282 gram-positive isolates from milk samples from dairy farmers and vendors in Haryana and Assam, India, to assess the prevalence of methicillin-resistant staphylococci using microbiological tests, antibiotic susceptibility testing, and genotyping by PCR. The prevalence of genotypic methicillin resistance in isolates from raw milk samples was 5% [95% confidence interval, CI (3-8)], with 7% [CI (3-10)] in Haryana, in contrast to 2% [CI (0.2-6)] in Assam. The prevalence was the same in isolates from milk samples collected from farmers [5% (n = 6), CI (2-11)] and vendors [5% (n = 7), CI (2-10)]. Methicillin resistance was also observed in 15% of the isolates from pasteurized milk [(n = 3), CI (3-38)]. Two staphylococci harboring a novel mecC gene were identified for the first time in Indian dairy products. The only SCCmec type identified was Type V. The staphylococci with the mecA (n = 11) gene in raw milk were commonly resistant to oxacillin [92%, CI (59-100)] and cefoxitin [74%, CI (39-94)], while the isolates with mecC (n = 2) were resistant to oxacillin (100%) only. All the staphylococci with the mecA (n = 3) gene in pasteurized milk were resistant to both oxacillin and cefoxitin. Our results provided evidence that methicillin-resistant staphylococci occur in dairy products in India with potential public health implications. The state with more intensive dairy systems (Haryana) had higher levels of methicillin-resistant bacteria in milk.

Place, publisher, year, edition, pages
MDPI, 2023
Keywords
MRCoNS, MRSA, Methicillin resistance, dairy, farmers, food safety, milk, vendors
National Category
Animal and Dairy Science
Research subject
Microbiology; Molecular Biology
Identifiers
urn:nbn:se:uu:diva-500809 (URN)10.3390/pathogens12020344 (DOI)000941812400001 ()36839616 (PubMedID)
Available from: 2023-04-25 Created: 2023-04-25 Last updated: 2025-10-16Bibliographically approved
2. Analyses of Extended-Spectrum-β-Lactamase, Metallo-β-Lactamase, and AmpC-β-Lactamase Producing Enterobacteriaceae from the Dairy Value Chain in India
Open this publication in new window or tab >>Analyses of Extended-Spectrum-β-Lactamase, Metallo-β-Lactamase, and AmpC-β-Lactamase Producing Enterobacteriaceae from the Dairy Value Chain in India
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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
Keywords
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:nbn:se:uu:diva-512928 (URN)10.3390/antibiotics12091449 (DOI)001093265700001 ()37760745 (PubMedID)
Available from: 2023-09-30 Created: 2023-09-30 Last updated: 2025-10-16Bibliographically approved
3. Antimicrobial resistance in India’s dairy value chain: A multilevel logistic regression analysis of risk factors in Haryana and Assam, India
Open this publication in new window or tab >>Antimicrobial resistance in India’s dairy value chain: A multilevel logistic regression analysis of risk factors in Haryana and Assam, India
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(English)Manuscript (preprint) (Other academic)
Abstract [en]

Antimicrobial resistance (AMR) in livestock is a growing One Health concern in India, where dairy is vital for nutrition and livelihoods. This study examined AMR in bacterial isolates from 256 cow milk samples in Assam and Haryana, including raw and pasteurized milk from farmers and vendors. AMR prevalence was high (90%) with no state-level differences. Dual AMR (Gram-positive and Gram-negative bacteria) occurred in 48% of samples, while multidrug resistance (MDR) was also 48%; dual MDR was less frequent (7%). Pasteurized milk showed significantly higher dual MDR (23%) compared to raw milk (6%, p = 0.023). No associations were found between AMR/MDR and herd size, mastitis history, antibiotic use, or farmer knowledge. These results highlight widespread AMR in milk, including vendor-sourced and pasteurized milk, and suggest complex systemic drivers beyond farm-level practices. Strengthened surveillance, with improved hygiene and handling during and after pasteurization, is critical to reduce AMR risks in the dairy sector.

Keywords
Dairy; AMR; food safety; public Health
National Category
Medical Biotechnology Animal and Dairy Science
Identifiers
urn:nbn:se:uu:diva-569423 (URN)
Available from: 2025-10-13 Created: 2025-10-13 Last updated: 2025-10-16
4. Antibiotic Residues and Antimicrobial Resistant bacteria in the Poultry Value Chain of Two Indian States
Open this publication in new window or tab >>Antibiotic Residues and Antimicrobial Resistant bacteria in the Poultry Value Chain of Two Indian States
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(English)Manuscript (preprint) (Other academic)
Abstract [en]

Background: The rapid expansion of the poultry industry has positioned it as a key source of animal protein globally, with India ranking eighth in broiler meat production. However, intensification and increased input reliance have raised concerns over antibiotic overuse and antimicrobial resistance (AMR), particularly in low- and middle-income countries like India.

Methods: This study assessed the prevalence and resistance profiles of non-typhoidal Salmonella (NTS) and Escherichia coli (E. coli) in poultry environments (water, fecal, feed, and litter samples) across two Indian states, Assam and Karnataka. Antibiotic residues in meat and feed samples were also tested.

Results: Of 283 samples, NTS and E. coli were detected in 32% (90/283) and 56% (158/283), respectively. Prevalence varied significantly by region, with Karnataka reporting higher NTS [44% (59/133)] than Assam [21% (31/150)]. Both pathogens were detected in treated water used in poultry, suggesting ineffective sanitation. Predominant Salmonella serovars included Typhimurium, Kentucky, and Infantis, many of which showed multidrug resistance (MDR), including to critical fluoroquinolones. Alarmingly, carbapenem-resistant E. coli strains were also identified.

Larger flock sizes were associated with a higher risk of MDR in both NTS and E. coli, suggesting a possible link between production intensity and resistance, though not statistically significant. Multivariable analysis showed higher odds of resistant Salmonella in Karnataka, and sock samples were particularly effective for detection. E. coli resistance was widespread, with no individual predictor reaching significance in multivariable models. No antibiotic residues were found in tested samples.

Conclusion: This study is among the first in India to report fluoroquinolone resistance and MDR in poultry-associated zoonotic NTS serovars across diverse matrices, with serious implications for food safety and public health. Although limited in scale, the absence of antibiotic residues is reassuring. These findings provide critical insight into the AMR landscape of India’s poultry value chains and underscore the urgent need for integrated, One Health based strategies to address AMR in poultry systems and protect public health and food safety.

Keywords
Poultry Value Chain; Salmonella; Escherichia coli; AMR; MDR; Prevalence; Food Safety; Public Health
National Category
Animal and Dairy Science Veterinary Science
Research subject
Microbiology
Identifiers
urn:nbn:se:uu:diva-513142 (URN)
Available from: 2023-10-03 Created: 2023-10-03 Last updated: 2025-10-16
5. Characterization of Lactic Acid Bacteria and Pathogens Isolated from Traditionally Fermented Foods, In Relation to Food Safety and Antimicrobial Resistance in Tribal Hill Areas of Northeast India
Open this publication in new window or tab >>Characterization of Lactic Acid Bacteria and Pathogens Isolated from Traditionally Fermented Foods, In Relation to Food Safety and Antimicrobial Resistance in Tribal Hill Areas of Northeast India
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2023 (English)In: Journal of Food Quality, ISSN 0146-9428, E-ISSN 1745-4557, Vol. 2023, article id 6687015Article in journal (Refereed) Published
Abstract [en]

Traditional fermented food products are often connected to various indigenous tribes and thus vary due to ethnicity, geography, and natural resource availability. The indigenous tribes from India greatly rely on fermentation processes for food preservation, flavor, and nutrition. Fermented foods can provide health benefits but also pose risks from harmful microbes and contaminants that grow in the food due to poor hygiene. In this study, we identified lactic acid bacteria (LAB) in fermented food collected from Northeast India, assessed their beneficial properties, and highlighted the risk from food pathogens that have antimicrobial resistance traits. A total of 113 different samples of fermented food products were collected from the local markets of five Northeastern Indian states (Nagaland, Manipur, Meghalaya, Arunachal Pradesh, and Sikkim). Standard laboratory methods were used to isolate LAB and determine their probiotic properties, conduct coliform counts, and isolate presumptive staphylococci from the fermented food samples. Antimicrobial susceptibility was determined by using the BD-Phoenix 100 automated system. We isolated 30 LAB with probiotic potential. The average aerobic colony count in different fermented food was 4.4-7.7 log center dot cfu/g, while coliforms were present in 43% (49/113, 95% (CI 34-53)) of the food samples, indicating low-hygiene levels. Additionally, some food samples contained staphylococci with phenotypic antibiotic-resistance markers (MRS, HLMUP, BLACT, and STAMLS). This study indicates that probiotic bacteria could be present in traditional fermented food products of Northeast India, but contamination with staphylococci and other bacterial pathogens with antibiotic resistance traits could put the health of consumers at risk.

Place, publisher, year, edition, pages
John Wiley & SonsWILEY-HINDAWI, 2023
National Category
Food Science Microbiology
Identifiers
urn:nbn:se:uu:diva-505275 (URN)10.1155/2023/6687015 (DOI)001000131600001 ()
Available from: 2023-07-06 Created: 2023-07-06 Last updated: 2025-10-16Bibliographically approved

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