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Companion Animals Emerged as an Important Reservoir of Carbapenem-Resistant Enterobacteriaceae: A Report from India

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Abstract

The emergence and spread of carbapenem-resistant Enterobacteriaceae (CRE) are perceived as a serious public-health threat world-wide. Despite sporadic reports, no systemic study has been carried out on CRE in companion animals in Indian subcontinent. In total, 237 canine specimens collected from five veterinary polyclinics in and around Kolkata were analyzed for isolation, antimicrobial resistance profiling and molecular characterization of carbapenem-resistant (CR) E. coli. Of the 29 CR isolates, 19 were identified as metallo-β-lactamase producers (MP-CRE) and 10 as metallo-β-lactamase non-producers (MNP-CRE). Eleven of them were extended spectrum β-lactamase and/or AmpC type β-lactamase producers and harboured fluoroquinolone-, tetracycline-, sulfonamide- and aminoglycoside-resistant genes. Beside uropathogenic virulence determinants, they carried the adhesion factors mediating biofilm production which was remarkably higher in 6 MP-CRE and one MNP-CRE isolates. Although the CRE were of diverse origin including the healthy and the diseased dogs, these were more frequently isolated from canine pyometra. The MP-CRE harboured plasmids of IncF and IncA/C types. Phylo-type B1 was observed in 38% of the CR isolates, followed by A0 in 31% and rest were attributed to A1 and D1. The Enterobacterial repetitive intergenic consensus-PCR (ERIC-PCR) revealed that these isolates were genetically diverse and constituted of a heterogenous population. Detection of CRE in pet dogs despite the fact that carbapenems are not used in animals in India emphasizes the need for active surveillance to identify the transmission and dynamics of such pathogens in companion animals.

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References

  1. El-Gamal MI, Brahim I, Hisham N, Aladdin R, Mohammed H, Bahaaeldin A (2017) Recent updates of carbapenem antibiotics. Eur J Med Chem 131:185–195

    CAS  PubMed  Google Scholar 

  2. Nicoletti G, Russo G, Bonfiglio G (2002) Recent developments in carbapenems. Expert Opin Investig Drugs 11:529–544

    PubMed  Google Scholar 

  3. Hawkey PM, Livermore DM (2012) Carbapenem antibiotics for serious infections. BMJ 344:e3236–e3236

    PubMed  Google Scholar 

  4. Nair PK (2013) Prevalence of carbapenem resistant Enterobacteriaceae from a tertiary care hospital in Mumbai, India. J Microbiol Infect Dis 3:207–210

    Google Scholar 

  5. Pagano M, Martins AF, Barth AL (2016) Mobile genetic elements related to carbapenem resistance in Acinetobacter baumannii. Brazilian J Microbiol 47:785

    CAS  Google Scholar 

  6. Yang D, Guo Y, Zhang Z (2009) Combined porin loss and extended spectrum β-lactamase production is associated with an increasing imipenem minimal inhibitory concentration in clinical Klebsiella pneumoniae strains. Curr Microbiol 58:366–370

    CAS  PubMed  Google Scholar 

  7. Ahmad N, Ali SM, Khan AU (2018) Detection of New Delhi metallo-β-lactamase variants NDM-4, NDM-5, and NDM-7 in Enterobacter aerogenes isolated from a neonatal intensive care unit of a north india hospital: a first report. Microb Drug Resist 24:161–165

    CAS  PubMed  Google Scholar 

  8. Bhattacharya D, Thamizhmani R, Bhattacharya H, Sayi DS, Muruganandam N, Roy S, Sugunan AP (2013) Emergence of New Delhi metallo-β-lactamase 1 (NDM-1) producing and multidrug resistant uropathogens causing urinary tract infections in Andaman Islands, India. Microb Drug Resist 19:457–462

    CAS  PubMed  Google Scholar 

  9. Dhanikachalam V, Gowsica BR, Kundu TK, Bhat A, Shome BR, Modak R, Natesan K, Das Mitra S, Bhuvana M, Banerjee A, Shome R, Krishnamoorthy P (2012) Histone H3K14 and H4K8 hyperacetylation is associated with Escherichia coli -induced mastitis in mice. Epigenetics 7:492–501

    PubMed  Google Scholar 

  10. Hindler JA, Humphries RM (2013) Colistin MIC variability by method for contemporary clinical isolates of multidrug-resistant gram-negative bacilli. J Clin Microbiol 51:1678–1684

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Pierce VM, Simner PJ, Lonsway DR, Roe-Carpenter DE, Johnson JK, Brasso WB, Bobenchik AM, Lockett ZC, Charnot-Katsikas A, Ferraro MJ, Thomson RB, Jenkins SG, Limbago BM, Das S (2017) Modified carbapenem inactivation method for phenotypic detection of carbapenemase production among Enterobacteriaceae. J Clin Microbiol 55:2321–2333

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Pasteran F, Tijet N, Melano RG, Corso A (2015) Simplified protocol for carba NP test for enhanced detection of carbapenemase producers directly from bacterial cultures. J Clin Microbiol 53:3908–3911

    CAS  PubMed  PubMed Central  Google Scholar 

  13. de Oliveira DV, Van Der Sand ST (2016) Phenotypic tests for the detection of β-lactamase-producing Enterobacteriaceae isolated from different environments. Curr Microbiol 73:132–138

    PubMed  Google Scholar 

  14. Koovapra S, Bandyopadhyay S, Das G, Bhattacharyya D, Banerjee J, Mahanti A, Samanta I, Nanda PK, Kumar A, Mukherjee R, Dimri U, Singh RK (2016) Molecular signature of extended spectrum β-lactamase producing Klebsiella pneumoniae isolated from bovine milk in eastern and north-eastern India. Infect Genet Evol 44:395–402

    CAS  PubMed  Google Scholar 

  15. Kern ZT, Jacob ME, Gilbertie JM, Vaden SL, Lyle SK (2018) Characteristics of dogs with biofilm-forming Escherichia coli urinary tract infections. J Vet Intern Med 32:1645–1651

    PubMed  PubMed Central  Google Scholar 

  16. Decré D, Favier C, Arlet G, Da Costa A, Dallenne C (2010) Development of a set of multiplex PCR assays for the detection of genes encoding important β-lactamases in Enterobacteriaceae. J Antimicrob Chemother 65:490–495

    PubMed  Google Scholar 

  17. Parveen RM, Manivannan S, Harish BN, Parija SC (2012) Study of CTX-M type of extended spectrum β-lactamase among nosocomial isolates of Escherichia coli and Klebsiella pneumoniae in South India. Indian J Microbiol 52:35–40

    Google Scholar 

  18. Pitout JDD, Hamilton N, Church DL, Nordmann P, Poirel L (2007) Development and clinical validation of a molecular diagnostic assay to detect CTX-M-type β-lactamases in Enterobacteriaceae. Clin Microbiol Infect 13:291–297

    CAS  PubMed  Google Scholar 

  19. Sharma J, Sharma M, Ray P (2010) Detection of TEM & SHV genes in Escherichia coli & Klebsiella pneumoniae isolates in a tertiary care hospital from India. Indian J Med Res 132:332–336

    CAS  PubMed  Google Scholar 

  20. Ng L-KK, Martin I, Alfa M, Mulvey M (2001) Multiplex PCR for the detection of tetracycline resistant genes. Mol Cell Probes 15:209–215

    CAS  PubMed  Google Scholar 

  21. Rahman M, Mukhopadhyay C, Rai RP, Singh S, Gupta S, Singh A, Pathak A, Prasad KN (2018) Novel variant NDM-11 and other NDM-1 variants in multidrug-resistant Escherichia coli from South India. J Glob Antimicrob Resist 14:154–157

    PubMed  Google Scholar 

  22. Bandyopadhyay S, Banerjee J, Bhattacharyya D, Samanta I, Mahanti A, Dutta TK, Ghosh S, Nanda PK, Dandapat P, Bandyopadhyay S (2018) Genomic identity of fluoroquinolone-resistant bla CTX-M -15 -Type ESBL and pMAmpC β-lactamase producing Klebsiella pneumoniae from buffalo milk, India. Microb Drug Resist 24:1345–1353

    CAS  PubMed  Google Scholar 

  23. Rebelo AR, Bortolaia V, Kjeldgaard JS, Pedersen SK, Leekitcharoenphon P, Hansen IM, Guerra B, Malorny B, Borowiak M, Hammerl JA, Battisti A, Franco A, Alba P, Perrin-Guyomard A, Granier SA, De Frutos Escobar C, Malhotra-Kumar S, Villa L, Carattoli A, Hendriksen RS (2018) Multiplex PCR for detection of plasmid-mediated colistin resistance determinants, mcr-1, mcr-2, mcr-3, mcr-4 and mcr-5 for surveillance purposes. Eurosurveillance 23

  24. Bertini A, Falbo V, Carattoli A, Hopkins KL, Threlfall EJ, Villa L (2005) Identification of plasmids by PCR-based replicon typing. J Microbiol Methods 63:219–228

    PubMed  Google Scholar 

  25. Carlos C, Pires MM, Stoppe NC, Hachich EM, Sato MIZ, Gomes TAT, Amaral LA, Ottoboni LMM (2010) Escherichia coli phylogenetic group determination and its application in the identification of the major animal source of fecal contamination. BMC Microbiol 10:161

    PubMed  PubMed Central  Google Scholar 

  26. Agostinho JMA, de Souza A, Schocken-Iturrino RP, Beraldo LG, Borges CA, Ávila FA, Marin JM (2014) Escherichia coli strains isolated from the uteri horn, mouth, and rectum of bitches suffering from pyometra: virulence factors, antimicrobial susceptibilities, and clonal relationships among strains. Int J Microbiol 2014:1–8

    Google Scholar 

  27. Kar D, Bandyopadhyay S, Bhattacharyya D, Samanta I, Mahanti A, Nanda PK, Mondal B, Dandapat P, Das AK, Dutta TK, Bandyopadhyay S, Singh RK (2015) Molecular and phylogenetic characterization of multidrug resistant extended spectrum beta-lactamase producing Escherichia coli isolated from poultry and cattle in Odisha, India. Infect Genet Evol 29:82–90

    CAS  PubMed  Google Scholar 

  28. Reynolds ME, Phan HTT, George S, Hubbard ATM, Stoesser N, Maciuca IE, Crook DW, Timofte D (2019) Occurrence and characterization of Escherichia coli ST410 co-harbouring blaNDM-5, blaCMY-42 and blaTEM-190 in a dog from the UK. J Antimicrob Chemother 74:1207–1211

    CAS  PubMed  Google Scholar 

  29. Mollenkopf DF, Stull JW, Mathys DA, Bowman AS, Feicht SM, Grooters SV, Daniels JB, Wittum TE (2016) Carbapenemase-producing Enterobacteriaceae recovered from the environment of a swine farrow-to-finish operation in the United States. Antimicrob Agents Chemother. https://doi.org/10.1128/AAC.01298-16

    Article  Google Scholar 

  30. Yousfi M, Touati A, Mairi A, Brasme L, Gharout-Sait A, Guillard T, De Champs C (2016) Emergence of carbapenemase-producing Escherichia coli isolated from companion animals in Algeria. Microb Drug Resist 22:342–346

    CAS  PubMed  Google Scholar 

  31. Aung MS, San N, Maw WW, San T, Urushibara N, Kawaguchiya M, Sumi A, Kobayashi N (2018) Prevalence of extended-spectrum beta-lactamase and carbapenemase genes in clinical isolates of Escherichia coli in Myanmar: dominance of bla NDM-5 and emergence of bla OXA-181. Microb Drug Resist 24:1333–1344

    CAS  PubMed  Google Scholar 

  32. Khan ER, Aung MS, Paul SK, Ahmed S, Haque N, Ahamed F, Sarkar SR, Roy S, Rahman MM, Mahmud MC, Hossain MA, Urushibara N, Kawaguchiya M, Sumi A, Kobayashi N (2018) Prevalence and molecular epidemiology of clinical isolates of Escherichia coli and Klebsiella pneumoniae harboring extended-spectrum beta-lactamase and carbapenemase genes in Bangladesh. Microb Drug Resist 24:1568–1579

    CAS  PubMed  Google Scholar 

  33. Feng Y, Yang P, Xie Y, Wang X, McNally A, Zong Z (2015) Escherichia coli of sequence type 3835 carrying blaNDM-1, blaCTX-M-15, blaCMY-42 and blaSHV-12. Sci Rep 5:12275

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Grönthal T, Österblad M, Eklund M, Jalava J, Nykäsenoja S, Pekkanen K, Rantala M (2018) Sharing more than friendship – transmission of NDM-5 ST167 and CTX-M-9 ST69 Escherichia coli between dogs and humans in a family, Finland, 2015. Eurosurveillance 23:1700497

    PubMed Central  Google Scholar 

  35. Po KHL, Chan EWC, Chen S (2017) Functional characterization of CTX-M-14 and CTX-M-15 β-lactamases by in vitro DNA shuffling. Antimicrob Agents Chemother 61:e00891-e917

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Poulou A, Grivakou E, Vrioni G, Koumaki V, Pittaras T, Pournaras S, Tsakris A (2014) Modified CLSI extended-spectrum -β-lactamase (ESBL) confirmatory test for phenotypic detection of ESBLs among Enterobacteriaceae producing various β-lactamases. J Clin Microbiol 52:1483–1489

    PubMed  PubMed Central  Google Scholar 

  37. Bajpai T, Pandey M, Varma M, Bhatambare G (2017) Prevalence of TEM, SHV, and CTX-M beta-lactamase genes in the urinary isolates of a tertiary care hospital. Avicenna J Med 7:12

    PubMed  PubMed Central  Google Scholar 

  38. Chen Y (2003) Uropathogenic virulence factors in isolates of Escherichia coli from clinical cases of canine pyometra and feces of healthy bitches. Vet Microbiol 94:57–69

    PubMed  Google Scholar 

  39. Siqueira AK, Ribeiro MG, da Leite D, Tiba MR, de Moura C, Lopes MD, Prestes NC, Salerno T, da Silva AV (2009) Virulence factors in Escherichia coli strains isolated from urinary tract infection and pyometra cases and from feces of healthy dogs. Res Vet Sci 86:206–210

    CAS  PubMed  Google Scholar 

  40. Zou H, Jia X, Liu H, Li S, Wu X, Huang S (2020) Emergence of NDM-5-producing Escherichia coli in a teaching hospital in Chongqing, China: IncF-type plasmids may contribute to the prevalence of blaNDM–5. Front Microbiol 11:334

    PubMed  PubMed Central  Google Scholar 

  41. Wailan AM, Sidjabat HE, Yam WK, Alikhan N-F, Petty NK, Sartor AL, Williamson DA, Forde BM, Schembri MA, Beatson SA, Paterson DL, Walsh TR, Partridge SR (2016) Mechanisms involved in acquisition of bla NDM genes by IncA/C 2 and IncFII plasmids. Antimicrob Agents Chemother 60:4082–4088

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Zhao W-H, Hu Z-Q (2013) Epidemiology and genetics of CTX-M extended-spectrum β-lactamases in Gram-negative bacteria. Crit Rev Microbiol 39:79–101

    CAS  PubMed  Google Scholar 

  43. Ali T, Rahman S, Zhang L, Shahid M, Han D, Gao J, Zhang S, Ruegg PL, Saddique U, Han B (2017) Characteristics and genetic diversity of multi-drug resistant extended-spectrum beta-lactamase (ESBL)-producing Escherichia coli isolated from bovine mastitis. Oncotarget 8:90144–90163

    PubMed  PubMed Central  Google Scholar 

  44. Müştak HK, Günaydin E, Kaya İB, Salar MÖ, Babacan O, Önat K, Ata Z, Diker KS (2015) Phylo-typing of clinical Escherichia coli isolates originating from bovine mastitis and canine pyometra and urinary tract infection by means of quadruplex PCR. Vet Q 35:194–199

    PubMed  Google Scholar 

  45. Dadi BR, Abebe T, Zhang L, Mihret A, Abebe W, Amogne W (2020) Distribution of virulence genes and phylogenetics of uropathogenic Escherichia coli among urinary tract infection patients in Addis Ababa, Ethiopia. BMC Infect Dis 20:108

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Akhtardanesh B, Ghanbarpour R, Ganjalikhani S, Gazanfari P (2016) Determination of antibiotic resistance genes in relation to phylogenetic background in Escherichia coli isolates from fecal samples of healthy pet cats in Kerman city. Vet Res forum 7:301–308

    PubMed  PubMed Central  Google Scholar 

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Acknowledgement

The authors are thankful to the Director, ICAR-IVRI, Izatnagar (U.P.), for providing necessary facilities.

Funding

Funding was provided by Department of Biotechnology, Ministry of Science and Technology (Grant No. 711/CRC-PMU/TANUVAS/2018).

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Authors and Affiliations

  1. ICAR-Indian Veterinary Research Institute, Eastern Regional Station, 37 Belgachia Road, Kolkata, 700 037, India

    Samiran Bandyopadhyay, Jaydeep Banerjee, Debaraj Bhattacharyya, Premanshu Dandapat, Pramod K. Nanda, Arun K. Das & Bimalendu Mondal

  2. West Bengal University of Animal and Fishery Sciences, 37 & 68 K B Sarani, Kolkata, India

    Rahul Tudu, Indranil Samanta & Subhasis Batabyal

  3. CAU, Selesiah, Aizwal, India

    Tapan K. Dutta

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  1. Samiran Bandyopadhyay
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Correspondence to Samiran Bandyopadhyay.

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Bandyopadhyay, S., Banerjee, J., Bhattacharyya, D. et al. Companion Animals Emerged as an Important Reservoir of Carbapenem-Resistant Enterobacteriaceae: A Report from India. Curr Microbiol 78, 1006–1016 (2021). https://doi.org/10.1007/s00284-021-02355-6

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