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The present danger of New Delhi metallo-β-lactamase: a threat to public health

    Muhammad Usman Qamar

    *Author for correspondence:

    E-mail Address: musmanqamar@gcuf.edu.pk

    Department of Microbiology, Faculty of Life Sciences, Government College University Faisalabad, 38000, Pakistan

    ,
    Bruno S Lopes

    School of Medicine, Medical Sciences & Nutrition, University of Aberdeen, AB24 3DR, Scotland, UK

    ,
    Brekhna Hassan

    Department of Medical Microbiology & Infectious Diseases, Institute of Infection & Immunity, School of Medicine, Cardiff University, CF10 3AT, Cardiff, UK

    ,
    Mohsin Khurshid

    Department of Microbiology, Faculty of Life Sciences, Government College University Faisalabad, 38000, Pakistan

    ,
    Muhammad Shafique

    Department of Microbiology, Faculty of Life Sciences, Government College University Faisalabad, 38000, Pakistan

    ,
    Muhammad Atif Nisar

    Department of Microbiology, Faculty of Life Sciences, Government College University Faisalabad, 38000, Pakistan

    College of Science and Engineering, Flinders University, 5042, Australia

    ,
    Mashkoor Mohsin

    Institute of Microbiology, University of Agriculture Faisalabad, 38000, Pakistan

    ,
    Zeeshan Nawaz

    Department of Microbiology, Faculty of Life Sciences, Government College University Faisalabad, 38000, Pakistan

    ,
    Saima Muzammil

    Department of Microbiology, Faculty of Life Sciences, Government College University Faisalabad, 38000, Pakistan

    ,
    Bilal Aslam

    Department of Microbiology, Faculty of Life Sciences, Government College University Faisalabad, 38000, Pakistan

    ,
    Hasan Ejaz

    Department of Clinical Laboratory Sciences, College of Applied Medical Sciences, Jouf University, Al Jouf, 72388, Saudi Arabia

    &
    Mark A Toleman

    Department of Medical Microbiology & Infectious Diseases, Institute of Infection & Immunity, School of Medicine, Cardiff University, CF10 3AT, Cardiff, UK

    Published Online:https://doi.org/10.2217/fmb-2020-0069

    The evolution of antimicrobial-resistant Gram-negative pathogens is a substantial menace to public health sectors, notably in developing countries because of the scarcity of healthcare facilities. New Delhi metallo-β-lactamase (NDM) is a potent β-lactam enzyme able to hydrolyze several available antibiotics. NDM was identified from the clinical isolates of Klebsiella pneumoniae and Escherichia coli from a Swedish patient in New Delhi, India. This enzyme horizontally passed on to various Gram-negative bacteria developing resistance against a variety of antibiotics which cause treatment crucial. These bacteria increase fatality rates and play an integral role in the economic burden. The efficient management of NDM-producing isolates requires the coordination between each healthcare setting in a region. In this review, we present the prevalence of NDM in children, fatality and the economic burden of resistant bacteria, the clonal spread of NDM harboring bacteria and modern techniques for the detection of NDM producing pathogens.

    Papers of special note have been highlighted as: • of interest; •• of considerable interest

    References

    • 1. Aslam B, Wang W, Arshad MI et al. Antibiotic resistance: a rundown of a global crisis. Infect. Drug Resist. 11, 1645–1658 (2018).
    • 2. Li B, Webster TJ. Bacteria antibiotic resistance: new challenges and opportunities for implant-associated orthopedic infections. J. Orthop. Res. 36(1), 22–32 (2018).
    • 3. Munita JM, Arias CA. Mechanisms of antibiotic resistance. Microbiol. Spectr. 4(2), 1–37 (2016).
    • 4. Eichenberger EM, Thaden JT. Epidemiology and mechanisms of resistance of extensively drug resistant Gram-negative bacteria. Antibiotics (Basel) 8(2), 37 (2019).
    • 5. Qamar MU, Walsh TR, Toleman MA et al. Dissemination of genetically diverse NDM-1, -5, -7 producing-Gram-negative pathogens isolated from pediatric patients in Pakistan. Future Microbiol. 14(8), 691–704 (2019). •• This is the first study from Pakistan that highlighted the genotypes of NDM-producing Gram-negative bacteria mainly K. pneumoniae and E. coli clinical isolated from children's samples.
    • 6. Qamar MU, Nahid F, Walsh TR, Kamran R, Zahra R. Prevalence and clinical burden of NDM-1 positive infections in pediatric and neonatal patients in Pakistan. Pediatr. Infect. Dis. J. 34(4), 452–454 (2015).
    • 7. Qamar MU, Saleem S, Toleman MA et al. In vitro and in vivo activity of Manuka honey against NDM-1-producing Klebsiella pneumoniae ST11. Future Microbiol. 13(1), 13–26 (2018). •• In this study, NDM-1 producing K. pneumoniae ST11 strain was treated with Manuka honey in vitro and in vivo. Manuka honey showed promising results against the pathogenic strain.
    • 8. Tagliabue A, Rappuoli R. Changing priorities in vaccinology: antibiotic resistance moving to the top. Front. Immunol. 9, 1068–1068 (2018).
    • 9. CDC. Biggest Threats and Data (2019). www.cdc.gov/drugresistance/biggest-threats.html
    • 10. Laxminarayan R, Duse A, Wattal C et al. Antibiotic resistance-the need for global solutions. Lancet Infect. Dis. 13(12), 1057–1098 (2013).
    • 11. Hannan A, Qamar MU, Usman M, Waheed KAI, Rauf K. Multidrug resistant microorganisms causing neonatal septicemia: in a tertiary care hospital Lahore, Pakistan. Afr. J. Microbiol. Res. 7(19), 1896–1902 (2013).
    • 12. Saleem AF, Ahmed I, Mir F, Ali SR, Zaidi AK. Pan-resistant Acinetobacter infection in neonates in Karachi, Pakistan. J. Infect. Dev. Ctries. 4(1), 30–37 (2009).
    • 13. Khan E, Irfan S, Sultan BA, Nasir A, Hasan R. Dissemination and spread of New Delhi metallo-beta-lactamase-1 superbugs in hospital settings. J. Pak. Med. Assoc. 66(8), 999–1004 (2016).
    • 14. de Kraker MEA, Stewardson AJ, Harbarth S. Will 10 million people die a year due to antimicrobial resistance by 2050? PLoS Med. 13(11), e1002184–e1002184 (2016).
    • 15. Codjoe FS, Donkor ES. Carbapenem resistance: a review. Med. Sci. (Basel) 6(1), 1 (2017).
    • 16. Thomson KS. Extended-spectrum-beta-lactamase, AmpC, and Carbapenemase issues. J. Clin. Microbiol. 48(4), 1019–1025 (2010).
    • 17. van Duin D, Doi Y. The global epidemiology of carbapenemase-producing Enterobacteriaceae. Virulence. 8(4), 460–469 (2017).
    • 18. Naas T, Oueslati S, Bonnin RA et al. Beta-lactamase database (BLDB) – structure and function. J. Enzyme Inhib. Med. Chem. 32(1), 917–919 (2017). •• They developed a database for beta-lactamase enzymes. They update each beta-lactam gene as identified around the globe.
    • 19. Yong D, Toleman MA, Giske CG et al. 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(12), 5046–5054 (2009). • This was the first article on the identification of NDM-1 producing K. pneumoniae and E. coli from a Swedish patient had been hospitalized in New Delhi, India.
    • 20. Johnson AP, Woodford N. Global spread of antibiotic resistance: the example of New Delhi metallo-β-lactamase (NDM)-mediated carbapenem resistance. J. Med. Microbiol. 62(Pt 4), 499–513 (2013).
    • 21. Kumarasamy KK, Toleman MA, Walsh TR et al. Emergence of a new antibiotic resistance mechanism in India, Pakistan, and the UK: a molecular, biological, and epidemiological study. Lancet Infect. Dis. 10(9), 597–602 (2010).
    • 22. Pillai DR, McGeer A, Low DE. New Delhi metallo-β-lactamase-1 in Enterobacteriaceae: emerging resistance. CMAJ. 183(1), 59–64 (2011).
    • 23. Rahman M, Shukla SK, Prasad KN et al. Prevalence and molecular characterisation of New Delhi metallo-β-lactamases NDM-1, NDM-5, NDM-6 and NDM-7 in multidrug-resistant Enterobacteriaceae from India. Int. J. Antimicrob. Agents 44(1), 30–37 (2014).
    • 24. Berrazeg M, Diene S, Medjahed L et al. New Delhi Metallo-beta-lactamase around the world: an eReview using Google Maps. Euro Surveill. 19(20), 20809 (2014).
    • 25. Walsh TR, Weeks J, Livermore DM, Toleman MA. 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(5), 355–362 (2011).
    • 26. Feng H, Liu X, Wang S, Fleming J, Wang D-C, Liu W. The mechanism of NDM-1-catalyzed carbapenem hydrolysis is distinct from that of penicillin or cephalosporin hydrolysis. Nat. Commun. 8(1), 2242 (2017).
    • 27. Liang Z, Li L, Wang Y et al. Molecular basis of NDM-1, a new antibiotic resistance determinant. PLoS ONE 6(8), e23606–e23606 (2011).
    • 28. Lisa M-N, Palacios AR, Aitha M et al. A general reaction mechanism for carbapenem hydrolysis by mononuclear and binuclear metallo-β-lactamases. Nat. Commun. 8(1), 538 (2017).
    • 29. Toleman MA, Spencer J, Jones L, Walsh TR. blaNDM-1 is a chimera likely constructed in Acinetobacter baumannii. Antimicrob. Agents Chemother. 56(5), 2773–2776 (2012). •• They reported that the NDM gene is a chimera like constructed in A. baumannii. The first 6 amino acids of NDM and aphA6 are the same.
    • 30. Jones LS, Toleman MA, Weeks JL, Howe RA, Walsh TR, Kumarasamy KK. Plasmid carriage of bla NDM-1 in clinical Acinetobacter baumannii isolates from India. Antimicrob. Agents Chemother. 58(7), 4211–4213 (2014).
    • 31. González LJ, Bahr G, Nakashige TG, Nolan EM, Bonomo RA, Vila AJ. Membrane anchoring stabilizes and favors secretion of New Delhi metallo-β-lactamase. Nat. Chem. Biol. 12(7), 516–522 (2016).
    • 32. Bahr G, Vitor-Horen L, Bethel CR, Bonomo RA, González LJ, Vila AJ. Clinical evolution of New Delhi metallo-β-lactamase (NDM) optimizes resistance under Zn(II) deprivation. Antimicrob. Agents Chemother. 62(1), e01849–01817 (2017).
    • 33. Roy S, Viswanathan R, Singh AK, Das P, Basu S. Sepsis in neonates due to imipenem-resistant Klebsiella pneumoniae producing NDM-1 in India. J. Antimicrob. Chemother. 66(6), 1411–1413 (2011).
    • 34. Seema K, Ranjan Sen M, Upadhyay S, Bhattacharjee A. Dissemination of the New Delhi metallo-β-lactamase-1 (NDM-1) among Enterobacteriaceae in a tertiary referral hospital in north India. J. Antimicrob. Chemother. 66(7), 1646–1647 (2011).
    • 35. Castanheira M, Deshpande LM, Farrell SE, Shetye S, Shah N, Jones RN. Update on the prevalence and genetic characterization of NDM-1-producing Enterobacteriaceae in Indian hospitals during 2010. Diagn. Microbiol. Infect. Dis. 75(2), 210–213 (2013).
    • 36. Kumarasamy K, Kalyanasundaram A. Emergence of Klebsiella pneumoniae isolate co-producing NDM-1 with KPC-2 from India. J. Antimicrob. Chemother. 67(1), 243–244 (2012).
    • 37. Karthikeyan K, Thirunarayan MA, Krishnan P. Coexistence of blaOXA-23 with blaNDM-1 and armA in clinical isolates of Acinetobacter baumannii from India. J. Antimicrob. Chemother. 65(10), 2253–2254 (2010).
    • 38. Grover SS, Doda A, Gupta N et al. New Delhi metallo-β-lactamase-type carbapenemases producing Escherichia coli isolates from hospitalized patients: a pilot study. Indian J. Med. Res. 146(1), 105–110 (2017).
    • 39. Khan AU, Maryam L, Zarrilli R. Structure, genetics and worldwide spread of New Delhi metallo-β-lactamase (NDM): a threat to public health. BMC Microbiol. 17(1), 101 (2017).
    • 40. Mukherjee S, Bhattacharjee A, Naha S et al. Molecular characterization of NDM-1-producing Klebsiella pneumoniae ST29, ST347, ST1224, and ST2558 causing sepsis in neonates in a tertiary care hospital of North-East India. Infect. Genet. Evol. 69, 166–175 (2019).
    • 41. Mittal G, Gaind R, Kumar D et al. Risk factors for fecal carriage of carbapenemase producing Enterobacteriaceae among intensive care unit patients from a tertiary care center in India. BMC Microbiol. 16(1), 138–138 (2016).
    • 42. Batra P, Dwivedi M, Sherwal BL, Dutta R, Gupta S. NDM-1 Infection and colonisation in critically ill patients from Delhi: a glimpse of the community scenario. Indian J. Med. Microbiol. 34(1), 120–121 (2016).
    • 43. Nahid F, Khan AA, Rehman S, Zahra R. Prevalence of metallo-β-lactamase NDM-1-producing multi-drug resistant bacteria at two Pakistani hospitals and implications for public health. J. Infect. Public Health. 6(6), 487–493 (2013).
    • 44. Sartor AL, Raza MW, Abbasi SA et al. Molecular epidemiology of NDM-1-producing Enterobacteriaceae and Acinetobacter baumannii isolates from Pakistan. Antimicrob. Agents Chemother. 58(9), 5589–5593 (2014).
    • 45. Peirano G, Schreckenberger PC, Pitout JDD. Characteristics of NDM-1-producing Escherichia coli isolates that belong to the successful and virulent clone ST131. Antimicrob. Agents Chemother. 55(6), 2986–2988 (2011).
    • 46. Borgia S, Lastovetska O, Richardson D et al. Outbreak of Carbapenem-resistant enterobacteriaceae containing blaNDM-1, Ontario, Canada. Clin. Infect. Dis. 55(11), e109–e117 (2012).
    • 47. Peirano G, Pillai DR, Pitondo-Silva A, Richardson D, Pitout JDD. The characteristics of NDM-producing Klebsiella pneumoniae from Canada. Diagn. Microbiol. Infect. Dis. 71(2), 106–109 (2011).
    • 48. Mulvey MR, Grant JM, Plewes K, Roscoe D, Boyd DA. New Delhi metallo-β-lactamase in Klebsiella pneumoniae and Escherichia coli, Canada. Emerg. Infect. Dis. 17(1), 103–106 (2011).
    • 49. Teo J, Ngan G, Balm M, Jureen R, Krishnan P, Lin R. Molecular characterization of NDM-1 producing Enterobacteriaceae isolates in Singapore hospitals. Western Pac. Surveill. Response J. 3(1), 19–24 (2012).
    • 50. Chew KL, Lin RTP, Teo JWP. Klebsiella pneumoniae in Singapore: hypervirulent infections and the carbapenemase threat. Front. Cell Infect. Microbiol. 7, 515–515 (2017).
    • 51. Lachish T, Elimelech M, Arieli N, Adler A, Rolain J-M, Assous MV. Emergence of New Delhi metallo-β-lactamase in Jerusalem, Israel. Int. J. Antimicrob. Agents. 40(6), 566–567 (2012).
    • 52. Mirovic V, Tomanovic B, Lepsanovic Z, Jovcic B, Kojic M. Isolation of Klebsiella pneumoniae producing NDM-1 metallo-β-lactamase from the urine of an outpatient baby boy receiving antibiotic prophylaxis. Antimicrob. Agents Chemother. 56(11), 6062–6063 (2012).
    • 53. Rimrang B, Chanawong A, Lulitanond A et al. Emergence of NDM-1- and IMP-14a-producing Enterobacteriaceae in Thailand. J. Antimicrob. Chemother. 67(11), 2626–2630 (2012).
    • 54. Netikul T, Kiratisin P. Genetic characterization of carbapenem-resistant enterobacteriaceae and the spread of carbapenem-resistant Klebsiella pneumonia ST340 at a University Hospital in Thailand. PLoS One. 10(9), e0139116–e0139116 (2015).
    • 55. Poirel L, Revathi G, Bernabeu S, Nordmann P. Detection of NDM-1-producing Klebsiella pneumoniae in Kenya. Antimicrob. Agents Chemother. 55(2), 934–936 (2011).
    • 56. Revathi G, Siu LK, Lu P-L, Huang L-Y. First report of NDM-1-producing Acinetobacter baumannii in East Africa. Int. J. Infect. Dis. 17(12), e1255–e1258 (2013).
    • 57. McGann P, Milillo M, Clifford RJ et al. Detection of New Delhi metallo-β-lactamase (encoded by blaNDM-1) in Acinetobacter schindleri during routine surveillance. J. Clin. Microbiol. 51(6), 1942–1944 (2013).
    • 58. Khan ER, Aung MS, Paul SK et al. 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(10), 1568–1579 (2018).
    • 59. Islam MA, Islam M, Hasan R et al. Environmental spread of New Delhi metallo-β-lactamase-1-producing multidrug-resistant bacteria in Dhaka, Bangladesh. Appl. Environ. Microbiol. 83(15), e00793–00717 (2017).
    • 60. Islam MA, Talukdar PK, Hoque A et al. Emergence of multidrug-resistant NDM-1-producing Gram-negative bacteria in Bangladesh. Eur. J. Clin. Microbiol. Infect. Dis. 31(10), 2593–2600 (2012).
    • 61. Toleman MA, Bugert JJ, Nizam SA. Extensively drug-resistant New Delhi metallo-β-lactamase-encoding bacteria in the environment, Dhaka, Bangladesh, 2012. Emerg. Infect. Dis. 21(6), 1027–1030 (2015).
    • 62. Refath F, Shamsuzzaman SM, Kazi Zulfiquer M. Isolation and molecular characterization of New Delhi metallo-beta-lactamase-1 producing superbug in Bangladesh. J Infect Dev Ctries. 7(3), 161–8 (2013).
    • 63. Liu Z, Gu Y, Li X et al. Identification and characterization of NDM-1-producing hypervirulent (hypermucoviscous) Klebsiella pneumoniae in China. Ann. Lab. Med. 39(2), 167–175 (2019).
    • 64. Zou M-X, Wu J-M, Li J et al. NDM-1-producing Klebsiella pneumoniae in mainland China. Zhongguo Dang Dai Er Ke Za Zhi. 14(8), 616–621 (2012).
    • 65. Zhang X, Li X, Wang M et al. Outbreak of NDM-1-producing Klebsiella pneumoniae causing neonatal infection in a teaching hospital in mainland China. Antimicrob. Agents Chemother. 59(7), 4349–4351 (2015).
    • 66. Bi R, Kong Z, Qian H et al. High prevalence of bla (NDM) variants among carbapenem-resistant Escherichia coli in northern Jiangsu province, China. Front. Microbiol. 9, 2704–2704 (2018).
    • 67. Zhou G, Guo S, Luo Y et al. NDM-1-producing strains, family Enterobacteriaceae, in hospital, Beijing, China. Emerg. Infect. Dis. 20(2), 340–342 (2014).
    • 68. Kaase M, Nordmann P, Wichelhaus TA, Gatermann SG, Bonnin RA, Poirel L. NDM-2 carbapenemase in Acinetobacter baumannii from Egypt. J. Antimicrob. Chemother. 66(6), 1260–1262 (2011).
    • 69. Espinal P, Fugazza G, López Y et al. Dissemination of an NDM-2-producing Acinetobacter baumannii clone in an Israeli rehabilitation center. Antimicrob. Agents Chemother. 55(11), 5396–5398 (2011).
    • 70. Espinal P, Poirel L, Carmeli Y et al. Spread of NDM-2-producing Acinetobacter baumannii in the Middle East. J. Antimicrob. Chemother. 68(8), 1928–1930 (2013).
    • 71. Ghazawi A, Sonnevend Á, Bonnin RA et al. NDM-2 carbapenemase-producing Acinetobacter baumannii in the United Arab Emirates. Clin. Microbiol. Infect. 18(2), E34–E36 (2012).
    • 72. Ismail SJ, Mahmoud SS. First detection of New Delhi metallo-beta-lactamases variants (NDM-1, NDM-2) among Pseudomonas aeruginosa isolated from Iraqi hospitals. Iran J. Microbiol. 10(2), 98–103 (2018).
    • 73. Sjolander I, Hansen F, Elmanama A et al. Detection of NDM-2-producing Acinetobacter baumannii and VIM-producing Pseudomonas aeruginosa in Palestine. J. Glob. Antimicrob. Resist. 2(2), 93–97 (2014).
    • 74. Tada T, Miyoshi-Akiyama T, Shimada K, Kirikae T. Biochemical analysis of metallo-β-Lactamase NDM-3 from a multidrug-resistant Escherichia coli strain isolated in Japan. Antimicrob. Agents Chemother. 58(6), 3538–3540 (2014).
    • 75. Hu X, Xu X, Wang X et al. Diversity of New Delhi metallo-beta-lactamase-producing bacteria in China. Int. J. Infect. Dis. 55, 92–95 (2017).
    • 76. Qamar MU, Walsh TR, Toleman MA, Saleem S, Jahan S. First identification of clinical isolate of a novel “NDM-4” producing Escherichia coli ST405 from urine sample in Pakistan. Braz. J. Microbiol. 49(4), 949–950 (2018). • NDM-4 producing E. coli ST405 was isolated from a urine sample of a 4-year child. The strain was resistant to almost all antibiotics except colistin.
    • 77. Papagiannitsis CC, Studentova V, Chudackova E et al. Identification of a New Delhi metallo-beta-lactamase-4 (NDM-4)-producing Enterobacter cloacae from a Czech patient previously hospitalized in Sri Lanka. Folia Microbiol. (Praha). 58(6), 547–549 (2013).
    • 78. Ahmad N, Ali SM, Khan AU. Detection of New Delhi metallo-beta-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(2), 161–165 (2018).
    • 79. Khan AU, Beg AZ, Verma PK. Draft genome sequence of the first NDM-4-producing Escherichia coli strain (AK1), isolated from sewage water of a north Indian hospital. Genome Announc. 5(50), e01366–17 (2017).
    • 80. Coppo E, Del Bono V, Ventura F et al. Identification of a New Delhi metallo-beta-lactamase-4 (NDM-4)-producing Escherichia coli in Italy. BMC Microbiol. 14, 148 (2014).
    • 81. Le L, Tran LK, Le-Ha TD et al. Coexistence of plasmid-mediated MCR-1 And bla NDM-4 genes in a Klebsiella pneumoniae clinical strain in Vietnam. Infect. Drug Resist. 12, 3703–3707 (2019).
    • 82. Nordmann P, Boulanger AE, Poirel L. NDM-4 metallo-beta-lactamase with increased carbapenemase activity from Escherichia coli. Antimicrob. Agents Chemother. 56(4), 2184–2186 (2012).
    • 83. Khalifa HO, Soliman AM, Ahmed AM, Shimamoto T, Shimamoto T. NDM-4- and NDM-5-producing Klebsiella pneumoniae coinfection in a 6-month-old infant. Antimicrob. Agents Chemother. 60(7), 4416–4417 (2016).
    • 84. Kim JS, Hong CK, Park SH et al. Emergence of NDM-4 and OXA-181 carbapenemase-producing Klebsiella pneumoniae. J. Glob. Antimicrob. Resist. 20, 332–333 (2020).
    • 85. Tian D, Wang B, Zhang H et al. Dissemination of the bla NDM-5 gene via IncX3-type plasmid among Enterobacteriaceae in children. mSphere. 5(1), (2020).
    • 86. Liu Z, Xiao X, Liu Y, Li R, Wang Z. Recombination of NDM-5-producing plasmids mediated by IS26 among Escherichia coli. Int. J. Antimicrob. Agents. 55(1), 105815 (2020).
    • 87. Xu L, Wang P, Cheng J, Qin S, Xie W. Characterization of a novel bla NDM-5-harboring IncFII plasmid and an MCR-1-bearing IncI2 plasmid in a single Escherichia coli ST167 clinical isolate. Infect. Drug Resist. 12, 511–519 (2019).
    • 88. Kong Z, Cai R, Cheng C et al. First reported nosocomial outbreak Of NDM-5-producing Klebsiella pneumoniae In a neonatal unit in China. Infect. Drug Resist. 12, 3557–3566 (2019).
    • 89. Sun L, Xu J, He F. Draft genome sequence of an NDM-5, CTX-M-15 and OXA-1 co-producing Escherichia coli ST167 clinical strain isolated from a urine sample. J. Glob. Antimicrob Resist. 14, 284–286 (2018).
    • 90. Flerlage T, Brazelton de Cardenas JN, Garner CD et al. Multiple NDM-5-expressing Escherichia coli isolates from an immunocompromised pediatric host. Open Forum Infect. Dis. 7(2), 1–7 (2020).
    • 91. Hasassri ME, Boyce TG, Norgan AP et al. Correction for Hasassri et al. An immunocompromised child with bloodstream infection caused by two Escherichia coli Strains, one harboring NDM-5 and the other harboring OXA-48-like carbapenemase. Antimicrob. Agents Chemother. 60(8), 5108 (2016).
    • 92. Baek JY, Cho SY, Kim SH et al. Plasmid analysis of Escherichia coli isolates from South Korea co-producing NDM-5 and OXA-181 carbapenemases. Plasmid. 104, 102417 (2019).
    • 93. Yousfi M, Mairi A, Bakour S et al. First report of NDM-5-producing Escherichia coli ST1284 isolated from dog in Bejaia, Algeria. New Microbes New Infect. 8, 17–18 (2015).
    • 94. Giufre M, Errico G, Accogli M et al. Emergence of NDM-5-producing Escherichia coli sequence type 167 clone in Italy. Int. J. Antimicrob. Agents. 52(1), 76–81 (2018).
    • 95. Nukui Y, Ayibieke A, Taniguchi M et al. Whole-genome analysis of EC129, an NDM-5-, CTX-M-14-, OXA-10- and MCR-1-co-producing Escherichia coli ST167 strain isolated from Japan. J. Glob. Antimicrob. Resist. 18, 148–150 (2019).
    • 96. Bahramian A, Shariati A, Azimi T et al. First report of New Delhi metallo-beta-lactamase-6 (NDM-6) among Klebsiella pneumoniae ST147 strains isolated from dialysis patients in Iran. Infect. Genet. Evol. 69, 142–145 (2019).
    • 97. Ali A, Gupta D, Srivastava G, Sharma A, Khan AU. Molecular and computational approaches to understand resistance of New Delhi metallo beta-lactamase variants (NDM-1, NDM-4, NDM-5, NDM-6, NDM-7)-producing strains against carbapenems. J. Biomol. Struct. Dyn. 37(8), 2061–2071 (2019). •• The study was initiated to clone NDM variants followed by overexpression of the recombinant proteins to check their hydrolytic properties against β-lactam antibiotics. The MIC of carbapenems antibiotics for blaNDM-5 clone was found fourfold increased as compared with other variants.
    • 98. Cuzon G, Bonnin RA, Nordmann P. First identification of novel NDM carbapenemase, NDM-7, in Escherichia coli in France. PLoS One. 8(4), e61322 (2013).
    • 99. Gottig S, Hamprecht AG, Christ S, Kempf VA, Wichelhaus TA. Detection of NDM-7 in Germany, a new variant of the New Delhi metallo-beta-lactamase with increased carbapenemase activity. J. Antimicrob. Chemother. 68(8), 1737–1740 (2013).
    • 100. Lazaro-Perona F, Sarria-Visa A, Ruiz-Carrascoso G, Mingorance J, Garcia-Rodriguez J, Gomez-Gil R. Klebsiella pneumoniae co-producing NDM-7 and OXA-48 carbapenemases isolated from a patient with prolonged hospitalisation. Int. J. Antimicrob. Agents. 49(1), 112–113 (2017).
    • 101. Seara N, Oteo J, Carrillo R et al. Interhospital spread of NDM-7-producing Klebsiella pneumoniae belonging to ST437 in Spain. Int. J. Antimicrob. Agents. 46(2), 169–173 (2015).
    • 102. Xu J, He F. Characterization of a NDM-7 carbapenemase-producing Escherichia coli ST410 clinical strain isolated from a urinary tract infection in China. Infect. Drug Resist. 12, 1555–1564 (2019).
    • 103. Wang LH, Liu PP, Wei DD et al. Clinical isolates of uropathogenic Escherichia coli ST131 producing NDM-7 metallo-beta-lactamase in China. Int. J. Antimicrob. Agents. 48(1), 41–45 (2016).
    • 104. Hao Y, Shao C, Bai Y, Jin Y. Genotypic and phenotypic characterization of IncX3 plasmid carrying bla NDM-7 in Escherichia coli sequence type 167 isolated from a patient with urinary tract infection. Front. Microbiol. 9, 2468 (2018).
    • 105. Hammerum AM, Littauer P, Hansen F. Detection of Klebsiella pneumoniae co-producing NDM-7 and OXA-181, Escherichia coli producing NDM-5 and Acinetobacter baumannii producing OXA-23 in a single patient. Int. J. Antimicrob. Agents. 46(5), 597–598 (2015).
    • 106. Nuesch-Inderbinen M, Zurfluh K, Stevens MJA, Stephan R. Complete and assembled genome sequence of an NDM-9- and CTX-M-15-producing Klebsiella pneumoniae ST147 wastewater isolate from Switzerland. J. Glob. Antimicrob. Resist. 13, 53–54 (2018).
    • 107. Wang X, Li H, Zhao C et al. Novel NDM-9 metallo-beta-lactamase identified from a ST107 Klebsiella pneumoniae strain isolated in China. Int. J. Antimicrob. Agents. 44(1), 90–91 (2014).
    • 108. Liu BT, Song FJ, Zou M, Hao ZH, Shan H. Emergence of colistin resistance gene MCR-1 in Cronobacter sakazakii producing NDM-9 and in Escherichia coli from the same animal. Antimicrob. Agents Chemother. 61(2), e01444–16 (2017).
    • 109. Lai CC, Chuang YC, Chen CC, Tang HJ. Coexistence of MCR-1 and NDM-9 in a clinical carbapenem-resistant Escherichia coli isolate. Int. J. Antimicrob. Agents. 49(4), 517–518 (2017).
    • 110. Di DY, Jang J, Unno T, Hur HG. Emergence of Klebsiella variicola positive for NDM-9, a variant of New Delhi metallo-beta-lactamase, in an urban river in South Korea. J. Antimicrob. Chemother. 72(4), 1063–1067 (2017).
    • 111. Khajuria A, Praharaj AK, Kumar M, Grover N. Presence of a novel variant NDM-10, of the New Delhi metallo-beta-lactamase in a Klebsiella pneumoniae isolate. Indian J. Med. Microbiol. 34(1), 121–123 (2016).
    • 112. Rahman M, Mukhopadhyay C, Rai RP et al. Novel variant NDM-11 and other NDM-1 variants in multidrug-resistant Escherichia coli from south India. J. Glob. Antimicrob. Resist. 14, 154–157 (2018).
    • 113. Tada T, Shrestha B, Miyoshi-Akiyama T et al. NDM-12, a novel New Delhi metallo-beta-lactamase variant from a carbapenem-resistant Escherichia coli clinical isolate in Nepal. Antimicrob. Agents Chemother. 58(10), 6302–6305 (2014).
    • 114. Shrestha B, Tada T, Miyoshi-Akiyama T et al. Identification of a novel NDM variant, NDM-13, from a multidrug-resistant Escherichia coli clinical isolate in Nepal. Antimicrob. Agents Chemother. 59(9), 5847–5850 (2015).
    • 115. Kim JS, Jin YH, Park SH et al. Emergence of a multidrug-resistant clinical isolate of Escherichia coli ST8499 strain producing NDM-13 carbapenemase in the Republic of Korea. Diagn. Microbiol. Infect. Dis. 94(4), 410–412 (2019).
    • 116. Zou D, Huang Y, Zhao X et al. A novel New Delhi metallo-beta-lactamase variant, NDM-14, isolated in a Chinese Hospital possesses increased enzymatic activity against carbapenems. Antimicrob. Agents Chemother. 59(4), 2450–2453 (2015).
    • 117. Mitra S, Mukherjee S, Naha S, Chattopadhyay P, Dutta S, Basu S. Evaluation of co-transfer of plasmid-mediated fluoroquinolone resistance genes and blaNDM gene in Enterobacteriaceae causing neonatal septicaemia. Antimicrob. Resist. Infect. Control 8(1), 46 (2019).
    • 118. Li X, Mu X, Zhang P et al. Detection and characterization of a clinical Escherichia coli ST3204 strain coproducing NDM-16 and MCR-1. Infect. Drug Resist. 11, 1189–1195 (2018).
    • 119. Liu Z, Wang Y, Walsh TR et al. Plasmid-mediated novel bla(NDM-17) gene encoding a carbapenemase with enhanced activity in a sequence type 48 Escherichia coli strain. Antimicrob. Agents Chemother. 61(5), e02233–02216 (2017).
    • 120. Ntshobeni NB, Allam M, Ismail A, Amoako DG, Essack SY, Chenia HY. Draft genome sequence of Providencia rettgeri APW139_S1, an NDM-18-producing clinical strain originating from hospital effluent in South Africa. Microbiol. Resour. Announc. 8(21), e00259–19 (2019).
    • 121. Mancini S, Keller PM, Greiner M, Bruderer V, Imkamp F. Detection of NDM-19, a novel variant of the New Delhi metallo-beta-lactamase with increased carbapenemase activity under zinc-limited conditions, in Switzerland. Diagn. Microbiol. Infect. Dis. 95(3), 114851 (2019).
    • 122. Liu Z, Li J, Wang X et al. Novel variant of New Delhi metallo-beta-lactamase, NDM-20, in Escherichia coli. Front. Microbiol. 9, 248 (2018).
    • 123. Liu L, Feng Y, McNally A, Zong ZY. bla (NDM-21), a new variant of bla(NDM) in an Escherichia coli clinical isolate carrying bla(CTX-M-55) and rmtB. J. Antimicrob. Chemother. 73(9), 2336–2339 (2018).
    • 124. Logan LK, Weinstein RA. The epidemiology of carbapenem-resistant Enterobacteriaceae: the impact and evolution of a global menace. J. Infect. Dis. 215(suppl_1), S28–S36 (2017).
    • 125. McDermott H, Morris D, McArdle E et al. Isolation of NDM-1-producing Klebsiella pnemoniae in Ireland, July 2011. Euro Surveill. 17(7), 20087 (2012).
    • 126. Walsh TR, Toleman MA. The emergence of pan-resistant Gram-negative pathogens merits a rapid global political response. J. Antimicrob. Chemoth. 67(1), 1–3 (2011).
    • 127. Wailan AM, Sartor AL, Zowawi HM, Perry JD, Paterson DL, Sidjabat HE. Genetic contexts of blaNDM-1 in patients carrying multiple NDM-producing strains. Antimicrob. Agents Chemother. 59(12), 7405–7410 (2015).
    • 128. Patel G, Bonomo RA. “Stormy waters ahead”: global emergence of carbapenemases. Front. Microbiol. 4, 48–48 (2013).
    • 129. Poirel L, Dortet L, Bernabeu S, Nordmann P. Genetic features of blaNDM-1-positive Enterobacteriaceae. Antimicrob. Agents Chemother. 55(11), 5403–5407 (2011).
    • 130. Tamma PD, Simner PJ. Phenotypic detection of carbapenemase-producing organisms from clinical isolates. J. Clin. Microbiol. 56(11), e01140–01118 (2018).
    • 131. Wareham DW, Abdul Momin MHF. Rapid detection of carbapenemases in Enterobacteriaceae: evaluation of the resist-3 O.K.N. (OXA-48, KPC, NDM) lateral flow multiplexed assay. J. Clin. Microbiol. 55(4), 1223–1225 (2017).
    • 132. Hamprecht A, Vehreschild JJ, Seifert H, Saleh A. Rapid detection of NDM, KPC and OXA-48 carbapenemases directly from positive blood cultures using a new multiplex immunochromatographic assay. PLoS One. 13(9), e0204157 (2018).
    • 133. Weinstein MP, Lewis JS, Bobenchik AM et al. M100 Performance Standards for Antimicrobial Susceptibility Testing. Clinical Laboratory Standards Institute, 1–332 (2020).
    • 134. The European Committee on Antimicrobial Susceptibility Testing. Breakpoint tables for interpretation of MICs and zone diameters, version 10.0 (2020). www.eucast.org/clinical_breakpoints/
    • 135. Dortet L, Poirel L, Nordmann P. Worldwide dissemination of the NDM-type carbapenemases in Gram-negative bacteria. Biomed. Res. Int. 2014, 249856–249856 (2014).
    • 136. Girlich D, Poirel L, Nordmann P. Value of the modified Hodge test for detection of emerging carbapenemases in Enterobacteriaceae. J. Clin. Microbiol. 50(2), 477–479 (2012).
    • 137. Pasteran F, Gonzalez LJ, Albornoz E, Bahr G, Vila AJ, Corso A. Triton Hodge test: improved protocol for modified hodge test for enhanced detection of NDM and other carbapenemase producers. J. Clin. Microbiol. 54(3), 640–649 (2016).
    • 138. Poirel L, Nordmann P. Rapidec carba NP test for rapid detection of carbapenemase producers. J. Clin. Microbiol. 53(9), 3003–3008 (2015).
    • 139. Yu J, Liu J, Li Y et al. Rapid detection of carbapenemase activity of Enterobacteriaceae isolated from positive blood cultures by MALDI-TOF MS. Ann. Clin. Microbiol. Antimicrob. 17(1), 22 (2018).
    • 140. Walsh TR, Bolmström A, Qwärnström A, Gales A. Evaluation of a new Etest for detecting metallo-β-lactamases in routine clinical testing. J. Clin. Microbiol. 40(8), 2755–2759 (2002).
    • 141. Hansen F, Hammerum AM, Skov R, Haldorsen B, Sundsfjord A, Samuelsen O. Evaluation of the total MBL confirm kit (ROSCO) for detection of metallo-β-lactamases in Pseudomonas aeruginosa and Acinetobacter baumannii. Diagn. Microbiol. Infect. Dis. 79(4), 486–488 (2014).
    • 142. Al Tamimi M, Al Salamah A, Al Khulaifi M, Al Ajlan H. Comparison of phenotypic and PCR methods for detection of carbapenemases production by Enterobacteriaceae. Saudi J. Biol. Sci. 24(1), 155–161 (2017).
    • 143. Subirats J, Royo E, Balcázar JL, Borrego CM. Real-time PCR assays for the detection and quantification of carbapenemase genes (bla (KPC), bla (NDM), and bla (OXA-48)) in environmental samples. Environ. Sci. Pollut. Res. 24(7), 6710–6714 (2017).
    • 144. Cuzon G, Naas T, Bogaerts P, Glupczynski Y, Nordmann P. Evaluation of a DNA microarray for the rapid detection of extended-spectrum β-lactamases (TEM, SHV and CTX-M), plasmid-mediated cephalosporinases (CMY-2-like, DHA, FOX, ACC-1, ACT/MIR and CMY-1-like/MOX) and carbapenemases (KPC, OXA-48, VIM, IMP and NDM). J. Antimicrob. Chemother. 67(8), 1865–1869 (2012).
    • 145. Peyclit L, Baron SA, Rolain J-M. Drug repurposing to fight colistin and carbapenem-resistant bacteria. Front. Cell Infect. Microbiol. 9(193), (2019).
    • 146. Rogers BA, Sidjabat HE, Silvey A et al. Treatment options for New Delhi metallo-beta-lactamase-harboring Enterobacteriaceae. Microb. Drug Resist. (Larchmont, N.Y.). 19(2), 100–103 (2013).
    • 147. Poirel L, Jayol A, Nordmann P. Polymyxins: antibacterial activity, susceptibility testing, and resistance mechanisms encoded by plasmids or chromosomes. Clin. Microbiol. Rev. 30(2), 557–596 (2017).
    • 148. Dalfino L, Puntillo F, Mosca A et al. High-dose, extended-interval colistin administration in critically ill patients: is this the right dosing strategy? A preliminary study. Clin. Infect. Dis. 54(12), 1720–1726 (2012).
    • 149. Peterson LR. A review of tigecycline – the first glycylcycline. Int. J. Antimicrob. Agents. 32, S215–S222 (2008).
    • 150. Falagas ME, Vouloumanou EK, Samonis G, Vardakas KZ. Fosfomycin. Clin. Microbiol. Rev. 29(2), 321–347 (2016).
    • 151. Dijkmans AC, Zacarías NVO, Burggraaf J et al. Fosfomycin: pharmacological, clinical and future perspectives. Antibiotics (Basel). 6(4), 24 (2017).
    • 152. King AM, Reid-Yu SA, Wang W et al. Aspergillomarasmine A overcomes metallo-β-lactamase antibiotic resistance. Nature. 510(7506), 503–506 (2014).
    • 153. Kalan L, Wright GD. Antibiotic adjuvants: multicomponent anti-infective strategies. Expert Rev. Mol. Med. 13, e5–e5 (2011).
    • 154. MacVane SH, Crandon JL, Nichols WW, Nicolau DP. Unexpected in vivo activity of ceftazidime alone and in combination with avibactam against New Delhi metallo-β-lactamase-producing Enterobacteriaceae in a murine thigh infection model. Antimicrob. Agents Chemother. 58(11), 7007–7009 (2014).
    • 155. Honore PM, Jacobs R, Lochy S et al. Acute respiratory muscle weakness and apnea in a critically ill patient induced by colistin neurotoxicity: key potential role of hemoadsorption elimination during continuous venovenous hemofiltration. Int. J. Nephrol. Renovasc. Dis. 6, 107–111 (2013).
    • 156. Mushtaq S, Irfan S, Sarma JB et al. Phylogenetic diversity of Escherichia coli strains producing NDM-type carbapenemases. J. Antimicrob. Chemother. 66(9), 2002–2005 (2011).
    • 157. Woodford N, Turton JF, Livermore DM. Multiresistant Gram-negative bacteria: the role of high-risk clones in the dissemination of antibiotic resistance. FEMS Microbiol. Rev. 35(5), 736–755 (2011).
    • 158. Wang Y, Wu C, Zhang Q et al. Identification of New Delhi metallo-β-lactamase 1 in Acinetobacter lwoffii of food animal origin. PLoS One. 7(5), e37152–e37152 (2012).
    • 159. Umair M, Mohsin M, Ali Q et al. Prevalence and genetic relatedness of extended spectrum-β-lactamase-producing Escherichia coli among humans, cattle, and poultry in Pakistan. Microb. Drug Resist. 25(9), 1374–1381 (2019). •• The authors reported the prevalence of ESBL producing E. coli from humans and animals. Most of the E. coli displayed resistance to commonly used antibiotics including colistin and they have carried ESBL genes on transmissible plasmids.
    • 160. Yu J, Tan K, Rong Z et al. Nosocomial outbreak of KPC-2- and NDM-1-producing Klebsiella pneumoniae in a neonatal ward: a retrospective study. BMC Infect. Dis. 16(1), 563–563 (2016).
    • 161. Zhang X, Li X, Wang M et al. Outbreak of NDM-1-producing Klebsiella pneumoniae causing neonatal infection in a teaching hospital in mainland China. Antimicrob. Agents Chemother. 59(7), 4349–4351 (2015).
    • 162. Zheng R, Zhang Q, Guo Y et al. Outbreak of plasmid-mediated NDM-1-producing Klebsiella pneumoniae ST105 among neonatal patients in Yunnan, China. Ann. Clin. Microbiol. Antimicrob. 15, 10–10 (2016).
    • 163. Ho P-L, Li Z, Lai EL, Chiu SS, Cheng VCC. Emergence of NDM-1-producing Enterobacteriaceae in China. J. Antimicrob. Chemoth. 67(6), 1553–1555 (2012).
    • 164. Zhu J, Sun L, Ding B et al. Outbreak of NDM-1-producing Klebsiella pneumoniae ST76 and ST37 isolates in neonates. Eur. J. Clin. Microbiol. Infect. Dis. 35(4), 611–618 (2016).
    • 165. Jin Y, Shao C, Li J, Fan H, Bai Y, Wang Y. Outbreak of multidrug resistant NDM-1-producing Klebsiella pneumoniae from a neonatal unit in Shandong Province, China. PLoS One. 10(3), e0119571–e0119571 (2015).
    • 166. Salloum T, Arabaghian H, Alousi S, Abboud E, Tokajian S. Genome sequencing and comparative analysis of an NDM-1-producing Klebsiella pneumoniae ST15 isolated from a refugee patient. Pathog. Glob. Health. 111(4), 166–175 (2017).
    • 167. Green DA, Srinivas N, Watz N, Tenover FC, Amieva M, Banaei N. A pediatric case of New Delhi metallo-β-lactamase-1-producing Enterobacteriaceae in the United States. Pediatr. Infect. Dis. J. 32(11), 1291–1294 (2013).
    • 168. Pannaraj PS, Bard JD, Cerini C, Weissman SJ. Pediatric carbapenem-resistant Enterobacteriaceae in Los Angeles, California, a high-prevalence region in the United States. Pediatr. Infect. Dis. J. 34(1), 11–16 (2015).
    • 169. Chereau F, Herindrainy P, Garin B et al. Colonization of extended-spectrum-β-lactamase- and NDM-1-producing Enterobacteriaceae among pregnant women in the community in a low-income country: a potential reservoir for transmission of multiresistant Enterobacteriaceae to neonates. Antimicrob. Agents Chemother. 59(6), 3652–3655 (2015).
    • 170. Barrios H, Silva-Sanchez J, Reyna-Flores F et al. Detection of a NDM-1-producing Klebsiella pneumoniae (ST22) clinical isolate at a pediatric hospital in Mexico. Pediatr. Infect. Dis. J. 33(3), 335–335 (2014).
    • 171. Drew RJ, Turton JF, Hill RLR et al. Emergence of carbapenem-resistant Enterobacteriaceae in a UK paediatric hospital. J. Hosp. Infect. 84(4), 300–304 (2013).
    • 172. Datta S, Roy S, Chatterjee S et al. A five-year experience of carbapenem resistance in Enterobacteriaceae causing neonatal septicaemia: predominance of NDM-1. PLoS One 9(11), e112101–e112101 (2014).
    • 173. Datta S, Mitra S, Chattopadhyay P, Som T, Mukherjee S, Basu S. Spread and exchange of bla (NDM-1) in hospitalized neonates: role of mobilizable genetic elements. Eur. J. Clin. Microbiol. Infect. Dis. 36(2), 255–265 (2017).
    • 174. Jamal WY, Albert MJ, Rotimi VO. High prevalence of New Delhi metallo-β-lactamase-1 (NDM-1) producers among Carbapenem-Resistant Enterobacteriaceae in Kuwait. PLoS One 11(3), e0152638–e0152638 (2016).
    • 175. Hasassri ME, Boyce TG, Norgan AP et al. An Immunocompromised child with bloodstream infection caused by two Escherichia coli strains, one harboring NDM-5 and the other harboring OXA-48-like carbapenemase. Antimicrob. Agents Chemother. 60(6), 3270–3275 (2016).
    • 176. Birgy A, Doit C, Mariani-Kurkdjian P et al. Early detection of colonization by VIM-1-producing Klebsiella pneumoniae and NDM-1-producing Escherichia coli in two children returning to France. J. Clin. Microbiol. 49(8), 3085–3087 (2011).
    • 177. Novovic K, Vasiljevic Z, Kuzmanovic M et al. Novel E. coli ST5123 Containing bla(NDM-1) carried by IncF plasmid isolated from a pediatric patient in Serbia. Microb. Drug Resist. (Larchmont, N.Y.). 22(8), 707–711 (2016).
    • 178. Karaaslan A, Soysal A, Altinkanat Gelmez G, Kepenekli Kadayifci E, Söyletir G, Bakir M. Molecular characterization and risk factors for carbapenem-resistant Gram-negative bacilli colonization in children: emergence of NDM-producing Acinetobacter baumannii in a newborn intensive care unit in Turkey. J. Hosp. Infect. 92(1), 67–72 (2016).
    • 179. Bhattacharya D, Dey S, Kadam S et al. Isolation of NDM-1-producing multidrug-resistant Pseudomonas putida from a paediatric case of acute gastroenteritis, India. New Microbes New Infect. 5, 5–9 (2015).
    • 180. Huang J, Wang M, Ding H et al. New Delhi metallo-β-lactamase-1 in carbapenem-resistant Salmonella strain, China. Emerg. Infect. Dis. 19(12), 2049–2051 (2013).