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Isolation and Characterization of Extended-Spectrum β-Lactamase Producing Escherichia coli from Pig Farms and Slaughterhouse

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Abstract

Extended-spectrum β-lactamase (ESBL) producing Escherichia coli represents a formidable challenge in the field of microbiology and public health due to its resistance to commonly used antibiotics. These strains pose a serious threat to human and animal health, underscoring the urgency of comprehensive research and surveillance. The ongoing investigation seeks ESBL producing E. coli strains from pig farms and slaughterhouses in West Bengal and Assam, India. A total of 309 samples were collected: nasal swabs (25), rectal swabs (25) from healthy pigs, pig pen soil (45), faeces (55), slaughterhouse effluents (115), and cleaning water (44). In these samples, 154 tested positive for E. coli, indicating a 49.8% prevalence. Among 154 E. coli isolates, 23 (14.9%) produced ESBLs, sourced from pig rectal swabs (7.1%), faeces (10.7%), slaughterhouse effluents (26.1%), and cleaning water (11.7%). Significantly, 4 ESBL E. coli isolates (6.6%) exclusively emerged from pig slaughterhouse effluents, displaying imipenem-resistant properties. The majority of ESBL E. coli primarily produced CTX-M and CMY, with consistent genetic markers blaCTX-M (100%) and blaCMY (82.6%). Remarkably, 2 (8.6%) of 17 ESBL E. coli isolates from pig slaughterhouse effluents carried the genetic marker blaNDM1. These findings stress implementing thorough surveillance in pig farms and local slaughterhouses. This proactive approach is crucial to identify ESBL E. coli strains, enhancing public health protection.

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References

  1. Van Boeckel TP, Brower C, Gilbert M et al (2015) Global trends in antimicrobial use in food animals. Proc Natl Acad Sci USA 112:5649–5654. https://doi.org/10.1073/pnas.1503141112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Mutua F, Sharma G, Grace D et al (2020) A review of animal health and drug use practices in India, and their possible link to antimicrobial resistance. Antimicrob Resist Infect Control 9:1–13

    Article  Google Scholar 

  3. Czekalski N, Berthold T, Caucci S et al (2012) Increased levels of multiresistant bacteria and resistance genes after wastewater treatment and their dissemination into Lake Geneva, Switzerland. Front Microbiol. https://doi.org/10.3389/fmicb.2012.00106

    Article  PubMed  PubMed Central  Google Scholar 

  4. Dcosta VM, King CE, Kalan L et al (2011) Antibiotic resistance is ancient. Nature 477:457–461

    Article  CAS  PubMed  Google Scholar 

  5. Baquero F, Martínez JL, Cantón R (2008) Antibiotics and antibiotic resistance in water environments. Curr Opin Biotechnol 19:260–265

    Article  CAS  PubMed  Google Scholar 

  6. Søraas A, Sundsfjord A, Sandven I et al (2013) Risk factors for community-acquired urinary tract infections caused by ESBL-producing enterobacteriaceae—a case-control study in a low prevalence country. PLoS ONE. https://doi.org/10.1371/journal.pone.0069581

    Article  PubMed  PubMed Central  Google Scholar 

  7. Njage PMK, Buys EM (2015) Pathogenic and commensal Escherichia coli from irrigation water show potential in transmission of extended spectrum and AmpC β-lactamases determinants to isolates from lettuce. Microb Biotechnol 8:462–473. https://doi.org/10.1111/1751-7915.12234

    Article  CAS  PubMed  Google Scholar 

  8. Solà-Ginés M, González-López JJ, Cameron-Veas K et al (2015) Houseflies (Musca domestica) as vectors for extended-spectrum β-lactamase-producing Escherichia coli on Spanish broiler farms. Appl Environ Microbiol 81:3604–3611. https://doi.org/10.1128/AEM.04252-14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. North J (2020) Challenges to tackling antimicrobial resistance. Cambridge University Press, Cambridge

    Google Scholar 

  10. Gao LL, Tan Y, Zhang XD et al (2015) Emissions of Escherichia coli carrying extended-spectrum β-lactamase resistance from pig farms to the surrounding environment. Int J Environ Res Public Health 12:4203–4213. https://doi.org/10.3390/ijerph120404203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Von Salviati C, Laube H, Guerra B et al (2015) Emission of ESBL/AmpC-producing Escherichia coli from pig fattening farms to surrounding areas. Vet Microbiol 175:77–84. https://doi.org/10.1016/j.vetmic.2014.10.010

    Article  CAS  Google Scholar 

  12. Samanta A, Mahanti A, Chatterjee S et al (2018) Pig farm environment as a source of beta-lactamase or AmpC-producing Klebsiella pneumoniae and Escherichia coli. Ann Microbiol 68:781–791. https://doi.org/10.1007/s13213-018-1387-2

    Article  CAS  Google Scholar 

  13. Chen X, Han W, Patel M et al (2022) Inactivation of a pathogenic NDM-1-positive Escherichia coli strain and the resistance gene blaNDM-1 by TiO2/UVA photocatalysis. Sci Total Environ. https://doi.org/10.1016/j.scitotenv.2022.157369

    Article  PubMed  PubMed Central  Google Scholar 

  14. Deb R, Chaudhary P, De S (2022) CRISPR/cas9 cassette targeting Escherichia coli blaCTX-M specific gene of mastitis cow milk origin can alter the antibiotic resistant phenotype for cefotaxime. Anim Biotechnol. https://doi.org/10.1080/10495398.2022.2053695

    Article  PubMed  Google Scholar 

  15. Wang GCY, Wang Y (1996) The frequency of chimeric molecules as a consequence of PCR co-amplification of 16S rRNA genes from different bacterial species. Microbiology 142:1107–1114. https://doi.org/10.1099/13500872-142-5-1107

    Article  CAS  PubMed  Google Scholar 

  16. Gālina D, Balins A, Valdovska A (2021) The prevalence and characterization of fecal extended-spectrum-beta-lactamase-producing Escherichia coli isolated from pigs on farms of different sizes in Latvia. Antibiotics 10:1099. https://doi.org/10.3390/antibiotics10091099

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  18. Lalzampuia H, Dutta TK, Warjri I, Chandra R (2013) PCR-based detection of extended-spectrum β-lactamases (blaCTX-M-1and blaTEM) in Escherichia coli, Salmonella spp. and Klebsiella pneumoniae Isolated from Pigs in North Eastern India (Mizoram). Indian J Microbiol 53:291–296. https://doi.org/10.1007/s12088-013-0378-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Machado E, Coque TM, Cantón R et al (2008) Antibiotic resistance integrons and extended-spectrum β-lactamases among Enterobacteriaceae isolates recovered from chickens and swine in Portugal. J Antimicrob Chemother 62:296–302. https://doi.org/10.1093/jac/dkn179

    Article  CAS  PubMed  Google Scholar 

  20. Duan RS, Sit THC, Wong SSY et al (2006) Escherichia coli producing CTX-M β-lactamases in food animals in Hong Kong. Microb Drug Resist 12:145–148. https://doi.org/10.1089/mdr.2006.12.145

    Article  CAS  PubMed  Google Scholar 

  21. Geser N, Stephan R, Hächler H (2012) Occurrence and characteristics of extended-spectrum β-lactamase (ESBL) producing Enterobacteriaceae in food producing animals, minced meat and raw milk. BMC Vet Res. https://doi.org/10.1186/1746-6148-8-21

    Article  PubMed  PubMed Central  Google Scholar 

  22. Hiroi M, Yamazaki F, Harada T et al (2012) Prevalence of extended-spectrum β-lactamase-producing Escherichia coli and Klebsiella pneumoniae in food-producing animals. J Vet Med Sci 74:189–195. https://doi.org/10.1292/jvms.11-0372

    Article  CAS  PubMed  Google Scholar 

  23. Mirbagheri SZ, Meshkat Z, Naderinasab M et al (2015) Study on imipenem resistance and prevalence of blaVIM1 and blaVIM2 metallo-beta lactamases among clinical isolates of Pseudomonas aeruginosa from Mashhad, Northeast of Iran. Iran J Microbiol 7:72–78

    PubMed  PubMed Central  Google Scholar 

  24. Nandi SP, Sultana M, Hossain MA (2013) Prevalence and characterization of multidrug-resistant zoonotic Enterobacter spp. in Poultry of Bangladesh. Foodborne Pathog Dis 10:420–427. https://doi.org/10.1089/fpd.2012.1388

    Article  CAS  PubMed  Google Scholar 

  25. Yaici L, Haenni M, Saras E et al (2016) blaNDM-5-carrying IncX3 plasmid in Escherichia coli ST1284 isolated from raw milk collected in a dairy farm in Algeria. J Antimicrob Chemother 71:2671–2672

    Article  CAS  PubMed  Google Scholar 

  26. Fischer J, San José M, Roschanski N et al (2017) Spread and persistence of VIM-1 Carbapenemase-producing Enterobacteriaceae in three German swine farms in 2011 and 2012. Vet Microbiol 200:118–123. https://doi.org/10.1016/j.vetmic.2016.04.026

    Article  PubMed  Google Scholar 

  27. Pruthvishree BS, Vinodh Kumar OR, Sinha DK et al (2017) Spatial molecular epidemiology of carbapenem-resistant and New Delhi metallo beta-lactamase (blaNDM)-producing Escherichia coli in the piglets of organized farms in India. J Appl Microbiol 122:1537–1546. https://doi.org/10.1111/jam.13455

    Article  CAS  PubMed  Google Scholar 

  28. Pulss S, Semmler T, Prenger-Berninghoff E et al (2017) First report of an Escherichia coli strain from swine carrying an OXA-181 carbapenemase and the colistin resistance determinant MCR-1. Int J Antimicrob Agents 50:232–236. https://doi.org/10.1016/j.ijantimicag.2017.03.014

    Article  CAS  PubMed  Google Scholar 

  29. Shi X, Li Y, Yang Y et al (2021) High prevalence and persistence of carbapenem and colistin resistance in livestock farm environments in China. J Hazard Mater. https://doi.org/10.1016/j.jhazmat.2020.124298

    Article  PubMed  PubMed Central  Google Scholar 

  30. Dankittipong N, Fischer EAJ, Swanenburg M et al (2022) Quantitative risk assessment for the introduction of carbapenem-resistant Enterobacteriaceae (CPE) into Dutch Livestock Farms. Antibiotics. https://doi.org/10.3390/antibiotics11020281

    Article  PubMed  PubMed Central  Google Scholar 

  31. Jia B, Raphenya AR, Alcock B et al (2017) CARD 2017: expansion and model-centric curation of the comprehensive antibiotic resistance database. Nucleic Acids Res 45:D566–D573. https://doi.org/10.1093/nar/gkw1004

    Article  CAS  PubMed  Google Scholar 

  32. Ewers C, Bethe A, Semmler T et al (2012) Extended-spectrum β-lactamase-producing and AmpC-producing Escherichia coli from livestock and companion animals, and their putative impact on public health: a global perspective. Clin Microbiol Infect 18:646–655

    Article  CAS  PubMed  Google Scholar 

  33. Hu YY, Cai JC, Zhou HW et al (2013) Molecular typing of CTX-M-producing Escherichia coli isolates from environmental water, swine feces, specimens from healthy humans, and human patients. Appl Environ Microbiol 79:5988–5996. https://doi.org/10.1128/AEM.01740-13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Rodríguez I, Barownick W, Helmuth R et al (2009) Extended-spectrum β-lactamases and AmpC β-lactamases in ceftiofur-resistant Salmonella enterica isolates from food and livestock obtained in Germany during 2003–07. J Antimicrob Chemother 64:301–309. https://doi.org/10.1093/jac/dkp195

    Article  CAS  PubMed  Google Scholar 

  35. Mollenkopf DF, Kleinhenz KE, Funk JA et al (2011) Salmonella enterica and Escherichia coli harboring blaCMY in retail beef and pork products. Foodborne Pathog Dis 8:333–336. https://doi.org/10.1089/fpd.2010.0701

    Article  PubMed  Google Scholar 

  36. Heider LC, Hoet AE, Wittum TE et al (2009) Genetic and phenotypic characterization of the blaCMY gene from Escherichia coli and Salmonella enterica isolated from food-producing animals, humans, the environment, and retail meat. Foodborne Pathog Dis 6:1235–1240. https://doi.org/10.1089/fpd.2009.0294

    Article  CAS  PubMed  Google Scholar 

  37. Evans BA, Amyes SGB (2014) OXA β-lactamases. Clin Microbiol Rev 27:241–263. https://doi.org/10.1128/CMR.00117-13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Sugumar M, Kumar KM, Manoharan A et al (2014) Detection of OXA-1 β-lactamase gene of Klebsiella pneumoniae from blood stream infections (BSI) by conventional PCR and in-silico analysis to understand the mechanism of OXA mediated resistance. PLoS One 9:e91800. https://doi.org/10.1371/journal.pone.0091800

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Zhou K, Lokate M, Deurenberg RH et al (2015) Characterization of a CTX-M-15 producing Klebsiella pneumoniae outbreak strain assigned to a novel sequence type (1427). Front Microbiol. https://doi.org/10.3389/fmicb.2015.01250

    Article  PubMed  PubMed Central  Google Scholar 

  40. Mir RA, Weppelmann TA, Johnson JA et al (2016) Identification and characterization of cefotaxime resistant bacteria in beef cattle. PLoS ONE. https://doi.org/10.1371/journal.pone.0163279

    Article  PubMed  PubMed Central  Google Scholar 

  41. Walsh TR, Weeks J, Livermore DM, Toleman MA (2011) Dissemination of NDM-1 positive bacteria in the New Delhi environment and its implications for human health: an environmental point prevalence study. Lancet Infect Dis 11:355–362. https://doi.org/10.1016/S1473-3099(11)70059-7

    Article  PubMed  Google Scholar 

  42. Zhai R, Fu B, Shi X et al (2020) Contaminated in-house environment contributes to the persistence and transmission of NDM-producing bacteria in a Chinese poultry farm. Environ Int. https://doi.org/10.1016/j.envint.2020.105715

    Article  PubMed  Google Scholar 

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Acknowledgements

Authors acknowledge the financial support received from Indian Council of Agricultural Research, New Delhi, India under the project of Indian Network for Fisheries and Animal Antimicrobial Resistance (INFAAR). Authors are thankful to Director, ICAR-National Research Centre on Pig, Guwahati, Assam, India for providing necessary facilities to conduct the experiment.

Funding

Authors acknowledge the financial support received from Indian Council of Agricultural Research, New Delhi, India under the project of Indian Network for Fisheries and Animal Antimicrobial Resistance (INFAAR).

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Authors and Affiliations

  1. ICAR-National Research Centre on Pig, Guwahati, Assam, India

    Jagana Niharika, Rajib Deb, Ranjeet Parihar, Priyanka Kumari Thakur, Gyanendra Singh Sengar, Seema Rani Pegu, Nitin Attupurum, Swaraj Rajkhowa & Vivek Kumar Gupta

  2. All India Institute of Hygiene and Public Health, Kolkata, West Bengal, India

    Jagana Niharika, Ranjeet Parihar & Priyanka Kumari Thakur

  3. College of Veterinary Science and Animal Husbandry, Kamdhenu University, Anand, Gujarat, India

    Pranav Anjaria

  4. ICAR-National Dairy Research Institute, Karnal, Haryana, India

    Parul Chaudhary

  5. Sri Venkateswara Veterinary University, Tirupati, Andhra Pradesh, India

    Naveena Antony

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  1. Jagana Niharika
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Correspondence to Rajib Deb.

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Niharika, J., Deb, R., Parihar, R. et al. Isolation and Characterization of Extended-Spectrum β-Lactamase Producing Escherichia coli from Pig Farms and Slaughterhouse. Indian J Microbiol (2023). https://doi.org/10.1007/s12088-023-01151-z

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