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Characterization of blaNDM-harboring, multidrug-resistant Enterobacteriaceae isolated from seafood

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Abstract

Carbapenem-resistant Enterobacteriaceae (CRE) have evolved into a major challenge to antibiotic therapy worldwide. The problem is more confounding when wider dissemination of CRE occurs in the community and the environment. In this study, six blaNDM-harboring Enterobacteriaceae, four Klebsiella pneumoniae, and two Escherichia coli, isolated from seafood, were characterized with respect to their antibiotic resistance and the genetic factors responsible for these resistances. The isolates were resistant to all β-lactam antibiotics, quinolones, trimethoprim–sulfamethoxazole, chloramphenicol, and tetracycline and were susceptible to colistin, polymixin B, fosfomycin, and tigecycline. Four isolates harbored New Delhi metallo β-lactamase (blaNDM-5 genes, while one isolate each harbored blaNDM-1 and blaNDM-2 genes, respectively. The blaNDM genes in all the isolates were flanked by an upstream, truncated ISAba125, and downstream bleMBL-trpF genes. Conjugation experiments showed that the NDM plasmids were readily transmissible. Further, the two blaNDM-positive E. coli isolates belonged to the multidrug-resistant ST131 clone. This study highlights the growing danger of seafood as carriers of multidrug-resistant bacteria leading to their wider dissemination in the community.

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References

  • Ahmad N, Khalid S, Ali SM, Khan AU (2018) Occurrence of bla NDM variants among Enterobacteriaceae from a neonatal intensive care unit in a northern India hospital. Front Microbiol 9:407

    Article  Google Scholar 

  • Biedenbach D, Bouchillon S, Hackel M, Hoban D, Kazmierczak K, Hawser S, Badal R (2015) Dissemination of NDM metallo-β-lactamase genes among clinical isolates of Enterobacteriaceae collected during the SMART global surveillance study from 2008 to 2012. Antimicrob Agents Chemother 59:826–830

    Article  CAS  Google Scholar 

  • Bora A, Ahmed GU, Hazarika NK, Prasad KN, Shukla SK, Randhawa V, Sarma JB (2013) Incidence of bla NDM-1 gene in Escherichia coli isolates at a tertiary care referral hospital in Northeast India. Indian J Med Microbiol 31:250–256

    Article  CAS  Google Scholar 

  • Bush K, Jacoby GA (2010) Updated functional classification of beta-lactamases. Antimicrob Agents Chemother 54:969–976

    Article  CAS  Google Scholar 

  • Clermont O, Dhanji H, Upton M, Gibreel T, Fox A, Boyd D, Mulvey MR, Nordmann P, Ruppe E, Sarthou JL, Frank T, Vimont S, Arlet G, Branger C, Woodford N, Denamur E (2009) Rapid detection of the O25b-ST131 clone of Escherichia coli encompassing the CTX-M-15-producing strains. J Antimicrob Chemother 64:274–277

    Article  CAS  Google Scholar 

  • Clermont O, Glodt J, Burdet C, Pognard D, Lefort A, Branger C, Denamur E, COLIBAFI Group Members (2013) Complexity of Escherichia coli bacteremia pathophysiology evidenced by comparison of isolates from blood and portal of entry within single patients. Int J Med Microbiol 303:529–532

    Article  CAS  Google Scholar 

  • CLSI (2009) Performance standards for antimicrobial susceptibility testing; nineteenth informational supplement M100-S19. Clinical and Laboratory Standards Institute, Wayne

    Google Scholar 

  • Devarajan N, Köhler T, Sivalingam P, van Delden C, Mulaji CK, Mpiana PT, Ibelings BW, Poté J (2017) Antibiotic resistant Pseudomonas spp. in the aquatic environment: a prevalence study under tropical and temperate climate conditions. Water Res 115:256–265

    Article  CAS  Google Scholar 

  • Drawz SM, Papp-Wallace KM, Bonomo RA (2014) New β-lactamase inhibitors: a therapeutic renaissance in an MDR world. Antimicrob Agents Chemother 58:1835–1846

    Article  CAS  Google Scholar 

  • Edelstein M, Pimkin M, Palagin I, Edelstein I, Stratchounski L (2003) Prevalence and molecular epidemiology of CTX-M extended-spectrum beta-lactamase-producing Escherichia coli and Klebsiella pneumoniae in Russian hospitals. Antimicrob Agents Chemother 47:3724–3732

    Article  CAS  Google Scholar 

  • Fiett J, Baraniak A, Izdebski R, Sitkiewicz I, Żabicka D, Meler A, Filczak K, Hryniewicz W, Gniadkowski M (2014) The first NDM metallo-β-lactamase-producing Enterobacteriaceae isolate in Poland: evolution of IncFII-type plasmids carrying the bla (NDM-1) gene. Antimicrob Agents Chemother 58:1203–1207

    Article  CAS  Google Scholar 

  • Frère J-M, Galleni M, Bush K, Dideberg O (2005) Is it necessary to change the classification of {beta}-lactamases? J Antimicrob Chemother 55:1051–1053

    Article  CAS  Google Scholar 

  • Ghatak S, Singha A, Sen A, Guha C, Ahuja A, Bhattacharjee U, Das S, Pradhan NR, Puro K, Jana C, Dey TK, Prashantkumar KL, Das A, Shakuntala I, Biswas U, Jana PS (2013) Detection of New Delhi metallo-beta-lactamase and extended-spectrum beta-lactamase genes in Escherichia coli isolated from mastitic milk samples. Transbound Emerg Dis 60:385–389

    Article  CAS  Google Scholar 

  • Hornsey M, Phee L, Wareham DW (2011) A novel variant, NDM-5, of the New Delhi metallo-β-lactamase in a multidrug-resistant Escherichia coli ST648 isolate recovered from a patient in the United Kingdom. Antimicrob Agents Chemother 55:5952–5954

    Article  CAS  Google Scholar 

  • Huang T-W, Wang J-T, Lauderdale T-L, Liao TL, Lai JF, Tan MC, Lin AC, Chen YT, Tsai SF, Chang SC (2013) Complete sequences of two plasmids in a bla NDM-1-positive Klebsiella oxytoca isolate from Taiwan. Antimicrob Agents Chemother 57:4072–4076

    Article  CAS  Google Scholar 

  • Inamasu J, Ishikawa K, Oheda M, Nakae S, Hirose Y, Yoshida S (2016) Intrathecal administration of colistin for meningitis due to New Delhi metallo-β-lactamase 1(NDM-1)-producing Klebsiella pneumoniae. J Infect Chemother Off J Jpn Soc Chemother 22:184–186

    Article  CAS  Google Scholar 

  • Isozumi R, Yoshimatsu K, Yamashiro T, Hasebe F, Nguyen BM, Ngo TC, Yasuda SP, Koma T, Shimizu K, Arikawa J (2012) bla (NDM-1)-positive Klebsiella pneumoniae from environment, Vietnam. Emerg Infect Dis 18:1383–1385

    Article  Google Scholar 

  • Khajuria A, Praharaj AK, Kumar M, Grover N (2013) Emergence of NDM-1 in the clinical isolates of Pseudomonas aeruginosa in India. J Clin Diagn Res JCDR 7:1328–1331

    Google Scholar 

  • Khalifa HO, Soliman AM, Ahmed AM et al (2016) NDM-4- and NDM-5-producing Klebsiella pneumoniae coinfection in a 6-month-old infant. Antimicrob Agents Chemother 60:4416–4417

    Article  Google Scholar 

  • Khan AU, Maryam L, Zarrilli R (2017) Structure, genetics and worldwide spread of New Delhi Metallo-β-lactamase (NDM): a threat to public health. BMC Microbiol 17:101

    Article  CAS  Google Scholar 

  • Kumarasamy KK, Toleman MA, Walsh TR, Bagaria J, Butt F, Balakrishnan R, Chaudhary U, Doumith M, Giske CG, Irfan S, Krishnan P, Kumar AV, Maharjan S, Mushtaq S, Noorie T, Paterson DL, Pearson A, Perry C, Pike R, Rao B, Ray U, Sarma JB, Sharma M, Sheridan E, Thirunarayan MA, Turton J, Upadhyay S, Warner M, Welfare W, Livermore DM, Woodford N (2010) Emergence of a new antibiotic resistance mechanism in India, Pakistan, and the UK: a molecular, biological, and epidemiological study. Lancet Infect Dis 10:597–602

    Article  CAS  Google Scholar 

  • Lekshmi M, Ammini P, Kumar S, Varela MF (2017) The food production environment and the development of antimicrobial resistance in human pathogens of animal origin. Microorganisms 5. https://doi.org/10.3390/microorganisms5010011

  • Liu Z, Li J, Wang X, Liu D, Ke Y, Wang Y, Shen J (2018) Novel variant of New Delhi Metallo-β-lactamase, NDM-20, in Escherichia coli. Front Microbiol 9:248

    Article  Google Scholar 

  • Mabilat C, Goussard S (1993) PCR detection and identification of genes for extended spectrum beta-lactamase. In: Persing DH, Smith TF, Tenover FC, White TJ (eds) Diagnostic molecular microbiology: principles and applications. American Society for Microbiology, pp 553–563, Washington, DC

  • Nakano R, Nakano A, Hikosaka K, Kawakami S, Matsunaga N, Asahara M, Ishigaki S, Furukawa T, Suzuki M, Shibayama K, Ono Y (2014) First report of metallo-β-lactamase NDM-5-producing Escherichia coli in Japan. Antimicrob Agents Chemother 58:7611–7612

    Article  CAS  Google Scholar 

  • Nordmann P, Poirel L (2005) Emergence of plasmid-mediated resistance to quinolones in Enterobacteriaceae. J Antimicrob Chemother 56:463–469. https://doi.org/10.1093/jac/dki245

    Article  CAS  Google Scholar 

  • Nordmann P, Naas T, Poirel L (2011a) Global spread of carbapenemase-producing Enterobacteriaceae. Emerg Infect Dis 17:1791–1798

    Article  CAS  Google Scholar 

  • Nordmann P, Poirel L, Carrër A et al (2011b) How to detect NDM-1 producers. J Clin Microbiol 49:718–721

    Article  Google Scholar 

  • Nordmann P, Poirel L, Walsh TR, Livermore DM (2011c) The emerging NDM carbapenemases. Trends Microbiol 19:588–595

    Article  CAS  Google Scholar 

  • Poirel L, Benouda A, Hays C, Nordmann P (2011a) Emergence of NDM-1-producing Klebsiella pneumoniae in Morocco. J Antimicrob Chemother 66:2781–2783

    Article  CAS  Google Scholar 

  • Poirel L, Dortet L, Bernabeu S, Nordmann P (2011b) Genetic features of bla NDM-1-positive Enterobacteriaceae. Antimicrob Agents Chemother 55:5403–5407

    Article  CAS  Google Scholar 

  • Queenan AM, Bush K (2007) Carbapenemases: the versatile beta-lactamases. Clin Microbiol Rev 20:440–458

    Article  CAS  Google Scholar 

  • Rasheed JK, Jay C, Metchock B, Berkowitz F, Weigel L, Crellin J, Steward C, Hill B, Medeiros AA, Tenover FC (1997) Evolution of extended-spectrum beta-lactam resistance (SHV-8) in a strain of Escherichia coli during multiple episodes of bacteremia. Antimicrob Agents Chemother 41:647–653

    Article  CAS  Google Scholar 

  • Robicsek A, Strahilevitz J, Sahm DF, Jacoby GA, Hooper DC (2006) qnr prevalence in ceftazidime-resistant Enterobacteriaceae isolates from the United States. Antimicrob Agents Chemother 50:2872–2874

    Article  CAS  Google Scholar 

  • Rogers BA, Sidjabat HE, Paterson DL (2011) Escherichia coli O25b-ST131: a pandemic, multiresistant, community-associated strain. J Antimicrob Chemother 66:1–14

    Article  CAS  Google Scholar 

  • Sambrook J, Fritsch E, Maniatis T (2001) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory, NY

    Google Scholar 

  • Singh AS, Lekshmi M, Nayak BB, Kumar SH (2016) Isolation of Escherichia coli harboring bla NDM-5 from fresh fish in India. J Microbiol Immunol Infect 49:822–823

    Article  Google Scholar 

  • Singh AS, Lekshmi M, Prakasan S et al (2017) Multiple antibiotic-resistant, extended spectrum-β-lactamase (ESBL)-producing Enterobacteria in fresh seafood. Microorganisms 5(3). https://doi.org/10.3390/microorganisms5030053

  • Teo J, Ngan G, Balm M, Jureen R, Krishnan P, Lin R (2012) Molecular characterization of NDM-1 producing Enterobacteriaceae isolates in Singapore hospitals. West Pac Surveill Response J WPSAR 3:19–24

    Article  Google Scholar 

  • Tran JH, Jacoby GA (2002) Mechanism of plasmid-mediated quinolone resistance. Proc Natl Acad Sci U S A 99:5638–5642

    Article  CAS  Google Scholar 

  • Ulu AC, Gökmen TG, Kibar F et al (2017) Molecular epidemiology of carbapenem-resistant Klebsiella pneumonia at a Turkish Center: is the increase of resistance a threat for Europe? J Glob Antimicrob Resist 11:10–16. https://doi.org/10.1016/j.jgar.2017.06.012

    Article  Google Scholar 

  • Vincent C, Boerlin P, Daignault D, Dozois CM, Dutil L, Galanakis C, Reid-Smith RJ, Tellier PP, Tellis PA, Ziebell K, Manges AR (2010) Food reservoir for Escherichia coli causing urinary tract infections. Emerg Infect Dis 16:88–95

    Article  CAS  Google Scholar 

  • Wailan AM, Paterson DL, Kennedy K et al (2015) Genomic characteristics of NDM-producing Enterobacteriaceae isolates in Australia and their bla NDM genetic contexts. Antimicrob Agents Chemother 60:136–141

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Wang Y, Wu C, Zhang Q, Qi J, Liu H, Wang Y, He T, Ma L, Lai J, Shen Z, Liu Y, Shen J (2012) Identification of New Delhi metallo-β-lactamase 1 in Acinetobacter lwoffii of food animal origin. PLoS One 7:e37152

    Article  CAS  Google Scholar 

  • Wei W-J, Yang H-F, Ye Y, Li J-B (2015) New Delhi metallo-β-lactamase-mediated carbapenem resistance: origin, diagnosis, treatment and public health concern. Chin Med J 128:1969–1976

    Article  Google Scholar 

  • Yong D, Toleman MA, Giske CG, Cho HS, Sundman K, Lee K, Walsh TR (2009) Characterization of a new metallo-beta-lactamase gene, bla (NDM-1), and a novel erythromycin esterase gene carried on a unique genetic structure in Klebsiella pneumoniae sequence type 14 from India. Antimicrob Agents Chemother 53:5046–5054

    Article  CAS  Google Scholar 

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Acknowledgements

Authors thank the Director of ICAR-CIFE Mumbai for help and support. Authors are grateful to Prof. George A. Jacoby and Dr. Xavier Alexander for E. coli J53 strain used in this study and to Dr. Manuel F. Varela, ENMU, Portales, USA, for the kind help with the manuscript.

Funding

This research was funded by an institutional research grant CIFE-2012/9.

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Authors and Affiliations

  1. QC Laboratory, Post Harvest Technology Department, ICAR-Central Institute of Fisheries Education (CIFE), Mumbai, 400061, India

    Uday Narayan Das, Asem Sanjit Singh, Manjusha Lekshmi, Binaya Bhusan Nayak & Sanath Kumar

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  1. Uday Narayan Das
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  2. Asem Sanjit Singh
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  3. Manjusha Lekshmi
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  4. Binaya Bhusan Nayak
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Correspondence to Sanath Kumar.

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Das, U.N., Singh, A.S., Lekshmi, M. et al. Characterization of blaNDM-harboring, multidrug-resistant Enterobacteriaceae isolated from seafood. Environ Sci Pollut Res 26, 2455–2463 (2019). https://doi.org/10.1007/s11356-018-3759-3

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  • DOI: https://doi.org/10.1007/s11356-018-3759-3

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