Genotypic identification of extended spectrum β-lactamase producing Escherichia coli in dairy supply chain


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Authors

  • Amarjeet Kumar ICAR-National Dairy Research Institute
  • Rashmi Hogarehalli Mallappa ICAR-National Dairy Research Institute
  • Avinash Jaswal ICAR-National Dairy Research Institute
  • Brijesh Kumar ICAR-National Dairy Research Institute
  • Naresh Kumar ICAR-National Dairy Research Institute
  • RAGHU HIRIKYATHANAHALLI VISHWESWARAIAH ICAR-National Dairy Research Institute http://orcid.org/0000-0002-4166-0086

Keywords:

E. coli, antibiotic resistance, milk, ESBL

Abstract

Foodborne illnesses due to antibiotic-resistant bacteria represent a major public health problem in both developed and developing countries. Among 190 samples, 139 Escherichia coli positive isolates from raw milk, pasteurized milk, and human handlers were identified by phenotypic methods and genotypic methods. All E. coli isolates were found to be resistant to penicillin, oxacillin, erythromycin, and clindamycin. The dominant type of resistance to cefotaxime and amoxiclav identically detected in 18.7% isolates followed by ampicillin in 17.98%, trimethoprim 15.82%, tetracycline 10.79%, nalidixic acid 7.91%, and piperacillin 7.79%. Four isolates have shown resistance (2.87%) to Ceftriaxone and ceftazidime, Cefotaxime and one isolate has shown resistance to Cefepime. Further, all four isolates were confirmed as extended-spectrum β-lactamase (ESBL) producer by double disc diffusion test and ESBL chromogenic medium. Later, all four isolates were evaluated by PCR and they are observed as carrier of blaCTX M gene which is responsible for ESBL antibiotic resistance in E.coli but blaTEM and blaSHV genes were absent in all four ESBL isolates. Based on the above findings, it is concluded that ESBL antibiotic resistance in E. coli were more prevalent in milk and this may due to the spread and acquirement of antibiotics resistance gene by plasmid and mobile genetic elements.

Author Biographies

  • Amarjeet Kumar, ICAR-National Dairy Research Institute
    National Referral center, Dairy Microbiology Division, ICAR-NDRI, Karnal-132001. Haryana, India
  • Rashmi Hogarehalli Mallappa, ICAR-National Dairy Research Institute
    Scientist (Senior Scale) Molecular Biology Unit, Dairy Microbiology Division, ICAR-NDRI, Karnal-132001
  • Avinash Jaswal, ICAR-National Dairy Research Institute
    PhD Scholar, National Referral centre, Dairy Microbiology Division, ICAR-NDRI, Karnal-132001. Haryana, India
  • Brijesh Kumar, ICAR-National Dairy Research Institute
    PhD Scholar, National Referral centre, Dairy Microbiology Division, ICAR-NDRI, Karnal-132001. Haryana, India
  • Naresh Kumar, ICAR-National Dairy Research Institute
    Principal Scientist and Nodal Officer, National Referral Centre, Dairy Microbiology Division, ICAR-NDRI, Karnal-132001. Haryana, India
  • RAGHU HIRIKYATHANAHALLI VISHWESWARAIAH, ICAR-National Dairy Research Institute
    Scientist (Senior scale) National Referral centre, Dairy Microbiology Division, ICAR-NDRI, Karnal-132001. Haryana, India

References

Adeolu M, Alnajar S, Naushad S, Gupta RS (2016) Genome-based phylogeny and taxonomy of the ‘Enterobacteriales’: proposal for Enterobacterales ord. nov. divided into the families Enterobacteriaceae, Erwiniaceae fam. nov., Pectobacteriaceae fam. nov., Yersiniaceae fam. nov., Hafniaceae fam. nov., Morganellaceae fam. nov., and Budviciaceae fam. nov. Int J Syst Evol Microbiol 66: 5575-5599

Alegría Ã, Arias-Temprano M, Fernández-Natal I, Rodríguez-Calleja JM, García-López ML, Santos Jan (2020) Molecular diversity of ESBL-producing E. coli from foods of animal origin and human patients. Int J Environ Res Public Health 17:1312

Ali AA, Abdelgadir WS (2011) Incidence of Escherichia coli in raw cow’s milk in Khartoum state, British. J Dairy Sci 2:23–26

Badri AM, Ibrahim IT, Mohamed SG, Garbi MI, Kabbashi AS (2017) Prevalence of Extended Spectrum â-Lactamase (ESBL) Producing E. coli and Klebsiella pneumonia Isolated from Raw Milk Samples in Al Jazirah State, Sudan. Mol Biol 7: 2

Batabyal K, Banerjee A, Pal S, Dey S, Joardar SN, Samanta I, Isore DP, Singh AD (2018) Detection, characterization, and antibiogram of extended-spectrum â-lactamase E. coli isolated from bovine milk samples in West Bengal, India. Vet World 10:1423

Batchelor M, Hopkins K, Threlfall EJ, Clifton-Hadley FA, Stallwood AD, Davies RH, Liebana E (2005) blaCTX-M genes in clinical Salmonella isolates recovered from humans in England and Wales from 1992 to 2003. Antimicrob Agents Chemother 49: 1319-1322

Bauer AW, Kirby WMM, Sherris JC, Turck M (1966) Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol 45: 493-496

CLSI (2007 Performance standards. In: Institute CaLS, editor. M100-S17. vol. ISBN 1-56238-625-5, 1 edn. 940 West Valley Road, Suite 1400, Wayne 19087-1898 USA; 2007.

CLSI (2012) Performance standards for antimicrobial susceptibility testing. Clinical and Laboratory Standards Institute (M100eS22). 2012 (s22nd Informational Supplement)

Dhara L, Tripathi A (2014) Genetic and structural insights into plasmid-mediated extended-spectrum â-lactamase activity of CTX-M and SHV variants among pathogenic Enterobacteriaceae infecting Indian patients. Int J Antimicrob Agents 43: 518-26

Drieux L, Brossier F, Sougakoff W, Jarlier V (2008) Phenotypic detection of extended spectrum â lactamase production in Enterobacteriaceae: review and bench guide. Clin Microbiol Infect 14: 90-103

Duan RS, Sit TH, Wong SS, Wong RC, Chow KH, Mak GC, Ho PL (2006) Escherichia coli producing CTX-M â-lactamases in food animals in Hong Kong. Microb Drug Resist 12: 145-148

EFSA (2011) BIOHAZ Panel Scientific Opinion on the public health risks of bacterial strains producing extended-spectrum â-lactamases and/or AmpC â-lactamases in food and food-producing animals. EFSA J 9: 2322

EFSA (2019) ECDC. The European union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2017. EFSA J 17: 5598

Ghatak S, Singha A, Sen A, Guha C, Ahuja A, Bhattacharjee U, Das S, Pradhan NR, Puro K, Jana C, Dey TK (2013) Detection of New Delhi Metallo â Lactamase and Extended Spectrum â Lactamase genes in E. coli isolated from mastitic milk amples. Transbound Emerg Dis 60: 385-389

Godambe LP, Bandekar J, Shashidhar R (2017) Species specific PCR based detection of Escherichia coli from Indian foods. 3 Biotech 7: 1–5

Gundogan N, Avci E (2013) Prevalence and antibiotic resistance of extended-spectrum â-lactamase (ESBL) producing E. coli and Klebsiella species isolated from foods of animal origin in Turkey. Afr J Microbiol Res 7: 4059-4064

Jarlier V, Nicolas MH, Fournier G, Philippon A (1988) Extended broad-spectrum â-lactamases conferring transferable resistance to newer â-lactam agents in Enterobacteriaceae: hospital prevalence and susceptibility patterns. Clin Infect Dis 10: 867-878

Karczmarczyk M, Abbott Y, Walsh C, Leonard N, Fanning S (2011) Characterization of multidrug-resistant Escherichia coli isolates from animals presenting at a university veterinary hospital. Appl Environ Microbiol 77: 7104-7112

Kucukbasmaci O, Ciftcioglu G, Midilli K, Issa G (2008) Detection of extended spectrum â-lactamase producing Enterobacteriaceae from food animals In Turkey. Revue Méd Vét 159: 586-592

Liebana E, Carattoli A, Coque TM, Hasman H, Magiorakos AP, Mevius D, Peixe L, Poirel L, Schuepbach-Regula G, Torneke K (2013) Public health risks of enterobacterial isolates producing extended-spectrum â-lactamases or AmpC â-lactamases in food and food producing animals: An EU perspective of epidemiology, analytical methods, risk factors, and control options. Clin Infect Dis 56: 1030-1037

NCCLS (National Committee for Clinical Laboratory Standards) (1993) Tentative Guidelines, M26-TNCCLS. Villanova, PA: 1993. Methods for determining bactericidal activity of antimicrobial agents

Odenthal S, Akineden Ö, Usleber E (2016) Extended-spectrum â-lactamase producing Enterobacteriaceae in bulk tank milk from German dairy farms. Int J Food Microbiol 238: 72–78

Olesen I, Hasman H, Møller Aarestrup F (2004) Prevalence of â-lactamases among ampicillin-resistant E. coli and Salmonella isolated from food animals in Denmark. Microb Drug Resist 10: 334-340

Rasheed MU, Thajuddin N, Ahamed P, Teklemariam Z, Jamil K (2014) Antimicrobial drug resistance in strains of E.coli isolated from food sources. Rev Inst Med Trop Sao Paulo 56: 341-346

Shome BR, Das Mitra S, Bhuvana M, Krithiga N, Velu D, Shome R, Isloor S, Barbuddhe SB, Rahman H (2011) Multiplex PCR assay for species identification of bovine mastitis pathogens. J Appl Microbiol 111: 1349-1356

Singh R, Schroeder CM, Meng J, White DG, McDermott PF, Wagner DD, Yang H, Simjee S, DebRoy C, Walker RD, Zhao S (2005) Identification of antimicrobial resistance and class 1 integrons in Shiga toxin-producing E. coli recovered from humans and food animals. J Antimicrob Chem 56:216-219

Soomro AH, Arain MA, Khaskheli M, Bhutto B (2002) Isolation of E. coli from raw milk and milk products in relation to public health sold under market conditions at Tandojam. Pak J Nutr 1: 151-152

Tadesse DA, Zhao S, Tong E, Ayers S, Singh A, Bartholomew MJ, McDermott PF (2012) Antimicrobial drug resistance in E. coli from humans and food animals, United States, 1950–2002. Emerg Infect Dis 18: 741

Thaker HC, Brahmbhatt MN, Nayak JB, Thaker HC (2013) Isolation and identification of Staphylococcus aureus from milk and milk products and their drug resistance patterns in Anand, Gujarat. Vet World 6: 10-13

Torpdahl M, Nielsen EM, Scheutz F, Olesen B, Hansen DS, Hasman H (2013) Detection of a Shiga toxin- and extended-spectrum-â-lactamase-producing E. coli O157:H7 human clinical isolate. J Antimicrob Chemother 68: 1203–1204

Van Hoek AHAM, Veenman C, van Overbeek WM, Lynch G, de Roda Husman AM, Blaak H (2015) Prevalence and characterization of ESBL- and AmpC-producing Enterobacteriaceae on retail vegetables. Int J Food Microbiol 204: 1–8

Weill FX, Demartin M, Tandé D, Espié E, Rakotoarivony I, Grimont PA (2004) SHV-12-like extended-spectrum-â-lactamase-producing strains of Salmonella enterica serotypes Babelsberg and Enteritidis isolated in France among infants adopted from Mali. J clin Microbiol 42: 2432-2437

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Submitted

2020-11-09

Published

2021-04-04

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Section

DAIRY PROCESSING

How to Cite

Kumar, A., Mallappa, R. H., Jaswal, A., Kumar, B., Kumar, N., & VISHWESWARAIAH, R. H. (2021). Genotypic identification of extended spectrum β-lactamase producing Escherichia coli in dairy supply chain. Indian Journal of Dairy Science, 74(1). https://epubs.icar.org.in/index.php/IJDS/article/view/107092