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Review

Metallo-beta-lactamases: mechanisms, treatment challenges, and future prospects

, &
Pages 189-201 | Received 30 Sep 2023, Accepted 24 Jan 2024, Published online: 01 Feb 2024

References

  • Thakuria B. The Beta Lactam Antibiotics as an Empirical Therapy in a Developing Country: An Update on Their Current Status and Recommendations to Counter the Resistance against Them. JCDR. 2013. doi: 10.7860/JCDR/2013/5239.3052
  • Antimicrobial Resistance C. Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis. Lancet. 2022;399(10325):629–655. doi:10.1016/S0140-6736(21)02724-0
  • Dadgostar P. Antimicrobial Resistance: Implications and Costs. Infect Drug Resist. 2019;12:3903–3910. doi:10.2147/IDR.S234610
  • WHO. 2017. WHO publishes list of bacteria for which new antibiotics are urgently needed. [cited 2023 Sep 26] Available from: https://www.who.int/news/item/27-02-2017-who-publishes-list-of-bacteria-for-which-new-antibiotics-are-urgently-needed
  • WHO. 2021. Global research agenda for antimicrobial resistance in human health. [cited 2023 Sep 26]. Available from: https://www.who.int/publications/m/item/global-research-agenda-for-antimicrobial-resistance-in-human-health
  • De Angelis G, Del Giacomo P, Posteraro B, et al. Molecular mechanisms, epidemiology, and clinical importance of β-lactam resistance in Enterobacteriaceae. Int J Mol Sci. 2020;21(14):5090. doi: 10.3390/ijms21145090
  • Mojica MF, Rossi MA, Vila AJ, et al. The urgent need for metallo-beta-lactamase inhibitors: an unattended global threat. Lancet Infect Dis. 2022;22(1):e28–e34.
  • Diene SM, Pontarotti P, Azza S, et al. Origin, diversity, and multiple roles of enzymes with metallo-β-lactamase Fold from different organisms. Cells. 2023;12(13):1752. doi: 10.3390/cells12131752
  • Ambler RP. The structure of beta-lactamases. Philos Trans R Soc Lond B Biol Sci. 1980;289(1036):321–331.
  • Sheu CC, Chang YT, Lin SY, et al. Infections caused by Carbapenem-Resistant Enterobacteriaceae: an update on therapeutic options. Front Microbiol. 2019;10:80. doi:10.3389/fmicb.2019.00080
  • Bahr G, Gonzalez LJ, Vila AJ. Metallo-beta-lactamases in the age of multidrug resistance: from structure and mechanism to evolution, dissemination, and inhibitor design. Chem Rev. 2021;121(13):7957–8094. doi:10.1021/acs.chemrev.1c00138
  • Mojica MF, Bonomo RA, Fast W. B1-metallo-beta-lactamases: where do we stand? Curr Drug Targets. 2016;17(9):1029–1050. doi:10.2174/1389450116666151001105622
  • Wang Z, Fast W, Valentine AM, et al. Metallo-beta-lactamase: structure and mechanism. Curr Opin Chem Biol. 1999;3(5):614–622. doi:10.1016/S1367-5931(99)00017-4
  • Arer V, Kar D. Biochemical exploration of beta-lactamase inhibitors. Front Genet. 2022;13:1060736. doi:10.3389/fgene.2022.1060736
  • Kanj SS, Bassetti M, Kiratisin P, et al. Clinical data from studies involving novel antibiotics to treat multidrug-resistant Gram-negative bacterial infections. Int J Antimicrob Agents. 2022;60(3):106633. doi: 10.1016/j.ijantimicag.2022.106633
  • Vazquez-Ucha JC, Arca-Suarez J, Bou G, et al. New carbapenemase inhibitors: clearing the way for the β-Lactams. Int J Mol Sci. 2020;21(23):9308. doi: 10.3390/ijms21239308
  • de Sousa Coelho F, Mainardi JL. The multiple benefits of second-generation beta-lactamase inhibitors in treatment of multidrug-resistant bacteria. Infect Dis Now. 2021;51(6):510–517. doi:10.1016/j.idnow.2020.11.007
  • Boyd SE, Livermore DM, Hooper DC, et al. Metallo-beta-lactamases: structure, function, epidemiology, treatment options, and the development pipeline. Antimicrob Agents Chemother. 2020;64(10). doi: 10.1128/AAC.00397-20
  • Tang B, Yang A, Liu P, et al. Outer membrane vesicles transmitting bla(NDM-1) mediate the emergence of carbapenem-resistant hypervirulent Klebsiella pneumoniae. Antimicrob Agents Chemother. 2023;67(5):e0144422. doi: 10.1128/aac.01444-22
  • Watanabe M, Iyobe S, Inoue M, et al. Transferable imipenem resistance in Pseudomonas aeruginosa. Antimicrob Agents Chemother. 1991;35(1):147–151. doi:10.1128/AAC.35.1.147
  • Pongchaikul P, Mongkolsuk P. Comprehensive Analysis of Imipenemase (IMP)-type metallo-β-lactamase: a global distribution threatening asia. Antibiotics. 2022;11(2):236. doi: 10.3390/antibiotics11020236
  • Beta-lactamase Database. 2024. [cited 2024 Jan 15]. Available from: http://bldb.eu/BLDB.php?prot=B1#IMP
  • Bush K, Bradford PA. Epidemiology of beta-lactamase-producing pathogens. Clin Microbiol Rev. 2020;33(2). doi: 10.1128/CMR.00047-19
  • Lauretti L, Riccio ML, Mazzariol A, et al. Cloning and characterization of blaVIM, a new integron-borne metallo-beta-lactamase gene from a Pseudomonas aeruginosa clinical isolate. Antimicrob Agents Chemother. 1999;43(7):1584–1590. doi: 10.1128/AAC.43.7.1584
  • Vatopoulos A. High rates of metallo-beta-lactamase-producing Klebsiella pneumoniae in Greece–a review of the current evidence. Euro Surveill. 2008;13(4):7–8. doi: 10.2807/ese.13.04.08023-en
  • Papadimitriou-Olivgeris M, Bartzavali C, Lambropoulou A, et al. Reversal of carbapenemase-producing Klebsiella pneumoniae epidemiology from blaKPC- to blaVIM-harbouring isolates in a Greek ICU after introduction of ceftazidime/avibactam. J Antimicrob Chemother. 2019;74(7):2051–2054. doi: 10.1093/jac/dkz125
  • Kazmierczak KM, Rabine S, Hackel M, et al. Multiyear, multinational survey of the incidence and global distribution of metallo-beta-lactamase-producing enterobacteriaceae and Pseudomonas aeruginosa. Antimicrob Agents Chemother. 2016;60(2):1067–1078. doi: 10.1128/AAC.02379-15
  • 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. 2009;53(12):5046–5054. doi: 10.1128/AAC.00774-09
  • Zowawi HM, Sartor AL, Balkhy HH, et al. Molecular characterization of carbapenemase-producing Escherichia coli and Klebsiella pneumoniae in the countries of the Gulf cooperation council: dominance of OXA-48 and NDM producers. Antimicrob Agents Chemother. 2014;58(6):3085–3090. doi: 10.1128/AAC.02050-13
  • Ma J, Song X, Li M, et al. Global spread of carbapenem-resistant Enterobacteriaceae: Epidemiological features, resistance mechanisms, detection and therapy. Microbiol Res. 2023;266:127249. doi: 10.1016/j.micres.2022.127249
  • CDC. 2022. COVID-19 U.S. impact on antimicrobial resistance. [cited 2023 Sep 26]. Available from: https://www.cdc.gov/drugresistance/pdf/covid19-impact-report-508.pdf
  • Porretta AD, Baggiani A, Arzilli G, et al. Increased risk of acquisition of New Delhi metallo-beta-lactamase-producing carbapenem-resistant enterobacterales (NDM-CRE) among a cohort of COVID-19 patients in a teaching hospital in Tuscany, Italy. Pathogens. 2020;9(8):635. doi: 10.3390/pathogens9080635
  • Caliskan-Aydogan O, Alocilja EC. A review of Carbapenem Resistance in Enterobacterales and its detection techniques. Microorganisms. 2023;11(6):1491. doi: 10.3390/microorganisms11061491
  • Hu Y, Matsui Y, WR L. Risk factors for fecal carriage of drug-resistant Escherichia coli: a systematic review and meta-analysis. Antimicrob Resist Infect Control. 2020;9(1):31. doi:10.1186/s13756-020-0691-3
  • Wailan AM, Paterson DL. The spread and acquisition of NDM-1: a multifactorial problem. Expert Rev Anti Infect Ther. 2014;12(1):91–115.
  • Ahammad ZS, Sreekrishnan TR, Hands CL, et al. Increased waterborne blaNDM-1 resistance gene abundances associated with seasonal human pilgrimages to the upper ganges river. Environ Sci Technol. 2014;48(5):3014–3020. doi:10.1021/es405348h
  • WHO. 2023. One health. [cited 2023 Sep 26]. Available from: https://www.who.int/health-topics/one-health#tab=tab_1
  • Mushtaq S, Vickers A, Doumith M, et al. Activity of beta-lactam/taniborbactam (VNRX-5133) combinations against carbapenem-resistant Gram-negative bacteria. J Antimicrob Chemother. 2021;76(1):160–170. doi:10.1093/jac/dkaa391
  • Tsivkovski R, Totrov M, Lomovskaya O. Biochemical characterization of QPX7728, a new ultrabroad-spectrum beta-lactamase inhibitor of serine and metallo-beta-lactamases. Antimicrob Agents Chemother. 2020;64(6). doi: 10.1128/AAC.00130-20
  • Ghazi IM, Crandon JL, Lesho EP, et al. Efficacy of humanized high-dose meropenem, cefepime, and levofloxacin against enterobacteriaceae isolates producing Verona integron-encoded metallo-beta-lactamase (VIM) in a murine thigh infection model. Antimicrob Agents Chemother. 2015;59(11):7145–7147. doi:10.1128/AAC.00794-15
  • MacVane SH, Crandon JL, Nichols WW, et al. Unexpected in vivo activity of ceftazidime alone and in combination with avibactam against New Delhi metallo-beta-lactamase-producing enterobacteriaceae in a murine thigh infection model. Antimicrob Agents Chemother. 2014;58(11):7007–7009. doi:10.1128/AAC.02662-14
  • Walsh TR, Toleman MA, Poirel L, et al. Metallo-beta-lactamases: the quiet before the storm? Clin Microbiol Rev. 2005;18(2):306–325. doi:10.1128/CMR.18.2.306-325.2005
  • Zhao S, Kennedy S, Perry MR, et al. Epidemiology of and risk factors for mortality due to carbapenemase-producing organisms (CPO) in healthcare facilities. J Hosp Infect. 2021;110:184–193. doi: 10.1016/j.jhin.2021.01.028
  • Matar GM. Editorial: Pseudomonas and acinetobacter: from drug resistance to pathogenesis. Front Cell Infect Microbiol. 2018;8:68. doi:10.3389/fcimb.2018.00068
  • Lemos EV, de la Hoz FP, Einarson TR, et al. Carbapenem resistance and mortality in patients with acinetobacter baumannii infection: systematic review and meta-analysis. Clin Microbiol Infect. 2014;20(5):416–423. doi: 10.1111/1469-0691.12363
  • Zavascki AP, Barth AL, Goncalves AL, et al. The influence of metallo-beta-lactamase production on mortality in nosocomial Pseudomonas aeruginosa infections. J Antimicrob Chemother. 2006;58(2):387–392. doi: 10.1093/jac/dkl239
  • Zhang Y, Wang Q, Yin Y, et al. Epidemiology of carbapenem-resistant enterobacteriaceae infections: report from the China CRE network. Antimicrob Agents Chemother. 2018;62(2). doi: 10.1128/AAC.01882-17
  • Falcone M, Tiseo G, Carbonara S, et al. Mortality attributable to bloodstream infections caused by different carbapenem-resistant gram-negative bacilli: results from a nationwide study in Italy (ALARICO network). Clin Infect Dis. 2023;76(12):2059–2069. doi: 10.1093/cid/ciad100
  • Xu L, Sun X, Ma X. Systematic review and meta-analysis of mortality of patients infected with carbapenem-resistant Klebsiella pneumoniae. Ann Clin Microbiol Antimicrob. 2017;16(1):18. doi:10.1186/s12941-017-0191-3
  • Boutzoukas AE, Komarow L, Chen L, et al. International epidemiology of carbapenemase-producing Escherichia coli. Clin Infect Dis. 2023;77(4):499–509. doi: 10.1093/cid/ciad288
  • CLSI Outreach Working Group. 2016. Laboratory detection and reporting of carbapenem-resistant enterobacteriaceae (CRE). [cited Sep 26]. Available from: https://clsi.org/media/1720/script-orwg-cre-laboratory-role.pdf
  • EUCAST. 2017. EUCAST guideline for the detection of resistance mechanisms and specific resistances of clinical and/or epidemiological importance. [cited 2023 Sep 26]. Available from: https://www.eucast.org/resistance_mechanisms
  • Tamma PD, Aitken SL, Bonomo RA, et al. Infectious Diseases Society of America 2023 Guidance on the treatment of antimicrobial resistant gram-negative infections. Clin Infect Dis. 2023. doi: 10.1093/cid/ciad428
  • Tamma PD, Simner PJ, Kraft CS. Phenotypic detection of carbapenemase-producing organisms from clinical isolates. J Clin Microbiol. 2018;56(11). doi: 10.1128/JCM.01140-18
  • Amjad A, Mirza I, Abbasi S, et al. Modified Hodge test: a simple and effective test for detection of carbapenemase production. Iran J Microbiol. 2011;3(4):189–193.
  • Ghebremedhin B, Halstenbach A, Smiljanic M, et al. MALDI-TOF MS based carbapenemase detection from culture isolates and from positive blood culture vials. Ann Clin Microbiol Antimicrob. 2016;15(5). doi: 10.1186/s12941-016-0120-x
  • Lahiri S, Venkataraman R, Jagan A, et al. Evaluation of LAMP-based assays for carbapenemase genes. J Med Microbiol. 2019;68(10):1431–1437. doi: 10.1099/jmm.0.001050
  • Motro Y, Moran-Gilad J. Next-generation sequencing applications in clinical bacteriology. Biomol Detect Quantif. 2017;14:1–6. doi:10.1016/j.bdq.2017.10.002
  • Su M, Satola SW, Read TD, et al. Genome-based prediction of bacterial antibiotic resistance. J Clin Microbiol. 2019;57(3). doi: 10.1128/JCM.01405-18
  • Nordmann P, Sadek M, Demord A, et al. NitroSpeed-carba NP test for rapid detection and differentiation between different classes of carbapenemases in Enterobacterales. J Clin Microbiol. 2020;58(9). doi: 10.1128/JCM.00932-20
  • Dortet L, Poirel L, Errera C, et al. CarbAcineto NP test for rapid detection of carbapenemase-producing acinetobacter spp. J Clin Microbiol. 2014;52(7):2359–2364. doi:10.1128/JCM.00594-14
  • Uechi K, Tada T, Shimada K, et al. A modified carbapenem inactivation method, CIMTris, for carbapenemase production in acinetobacter and pseudomonas species. J Clin Microbiol. 2017;55(12):3405–3410. doi: 10.1128/JCM.00893-17
  • Pasteran F, Gonzalez LJ, Albornoz E, et al. Triton hodge test: improved protocol for modified hodge test for enhanced detection of NDM and other carbapenemase producers. J Clin Microbiol. 2016;54(3):640–649. doi:10.1128/JCM.01298-15
  • Garcia-Fernandez S, Morosini MI, Marco F, et al. Evaluation of the eazyplex(R) SuperBug CRE system for rapid detection of carbapenemases and ESBLs in clinical Enterobacteriaceae isolates recovered at two Spanish hospitals. J Antimicrob Chemother. 2015;70(4):1047–1050. doi: 10.1093/jac/dku476
  • Cuzon G, Naas T, Bogaerts P, et al. Evaluation of a DNA microarray for the rapid detection of extended-spectrum beta-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. 2012;67(8):1865–1869. doi:10.1093/jac/dks156
  • Prat C, Lacoma A. Bacteria in the respiratory tract-how to treat? Or do not treat? Int J Infect Dis. 2016;51:113–122. doi:10.1016/j.ijid.2016.09.005
  • Nicolle LE, Gupta K, Bradley SF, et al. Clinical practice guideline for the management of Asymptomatic Bacteriuria: 2019 update by the infectious diseases society of America. Clin Infect Dis. 2019;68(10):e83–e110. doi: 10.1093/cid/ciz021
  • Zakhour J, Haddad SF, Kerbage A, et al. Diagnostic stewardship in infectious diseases: a continuum of antimicrobial stewardship in the fight against antimicrobial resistance. Int J Antimicrob Agents. 2023;62(1):106816. doi: 10.1016/j.ijantimicag.2023.106816
  • Mitchell BG, Fasugba O, Gardner A, et al. Reducing catheter-associated urinary tract infections in hospitals: study protocol for a multi-site randomised controlled study. BMJ Open. 2017;7(11):e018871. doi: 10.1136/bmjopen-2017-018871
  • Kenaa B, Richert ME, Claeys KC, et al. Ventilator-associated pneumonia: diagnostic test stewardship and relevance of culturing practices. Curr Infect Dis Rep. 2019;21(12):50. doi: 10.1007/s11908-019-0708-3
  • Tamma PD, Bergman Y, Jacobs EB, et al. Comparing the activity of novel antibiotic agents against carbapenem-resistant Enterobacterales clinical isolates. Infect Control Hosp Epidemiol. 2023;44(5):762–767. doi: 10.1017/ice.2022.161
  • Agarwal A, Srivastava J, Maheshwari U, et al. Molecular characterization and antimicrobial susceptibility profile of New Delhi metallo-beta-lactamase-1-producing Escherichia coli among hospitalized patients. J Lab Physicians. 2018;10(2):149–154. doi:10.4103/JLP.JLP_76_17
  • Fomda BA, Khan A, Zahoor D. NDM-1 (New Delhi metallo beta lactamase-1) producing Gram-negative bacilli: emergence & clinical implications. Indian J Med Res. 2014;140(5):672–678.
  • 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. 2010;10(9):597–602. doi: 10.1016/S1473-3099(10)70143-2
  • Mataseje LF, Abdesselam K, Vachon J, et al. Results from the Canadian nosocomial infection surveillance program on carbapenemase-producing Enterobacteriaceae, 2010 to 2014. Antimicrob Agents Chemother. 2016;60(11):6787–6794. doi: 10.1128/AAC.01359-16
  • Jayol A, Nordmann P, Poirel L, et al. Ceftazidime/avibactam alone or in combination with aztreonam against colistin-resistant and carbapenemase-producing Klebsiella pneumoniae. J Antimicrob Chemother. 2018;73(2):542–544. doi:10.1093/jac/dkx393
  • Falcone M, Daikos GL, Tiseo G, et al. Efficacy of ceftazidime-avibactam plus Aztreonam in patients with bloodstream infections caused by metallo-beta-lactamase-producing enterobacterales. Clin Infect Dis. 2021;72(11):1871–1878. doi: 10.1093/cid/ciaa586
  • Mauri C, Maraolo AE, Di Bella S, et al. The revival of Aztreonam in combination with avibactam against Metallo-β-Lactamase-Producing Gram-Negatives: a systematic review of in vitro studies and clinical cases. Antibiotics. 2021;10(8):1012. doi: 10.3390/antibiotics10081012
  • Karakonstantis S, Kritsotakis EI, Gikas A. Treatment options for K. pneumoniae, P. aeruginosa and A. baumannii co-resistant to carbapenems, aminoglycosides, polymyxins and tigecycline: an approach based on the mechanisms of resistance to carbapenems. Infection. 2020;48(6):835–851. doi:10.1007/s15010-020-01520-6
  • Timsit JF, Paul M, Shields RK, et al. Cefiderocol for the treatment of infections due to metallo-B-lactamase-producing pathogens in the CREDIBLE-CR and APEKS-NP phase 3 randomized studies. Clin Infect Dis. 2022;75(6):1081–1084. doi: 10.1093/cid/ciac078
  • CDC. 2023. Outbreak of extensively drug-resistant Pseudomonas aeruginosa associated with artificial tears. [cited 2023 Sep 26]. Available from: https://www.cdc.gov/hai/outbreaks/crpa-artificial-tears.html
  • Tiseo G, Suardi LR, Leonildi A, et al. Meropenem/Vaborbactam plus aztreonam for the treatment of New Delhi metallo-beta-lactamase-producing Klebsiella pneumoniae infections. J Antimicrob Chemother. 2023;78(9):2377–2379. doi:10.1093/jac/dkad206
  • Maraki S, Mavromanolaki VE, Moraitis P, et al. Ceftazidime-avibactam, meropenen-vaborbactam, and imipenem-relebactam in combination with aztreonam against multidrug-resistant, metallo-beta-lactamase-producing Klebsiella pneumoniae. Eur J Clin Microbiol Infect Dis. 2021;40(8):1755–1759. doi: 10.1007/s10096-021-04197-3
  • Yaghoubi S, Zekiy AO, Krutova M, et al. Tigecycline antibacterial activity, clinical effectiveness, and mechanisms and epidemiology of resistance: narrative review. Eur J Clin Microbiol Infect Dis. 2022;41(7):1003–1022. doi: 10.1007/s10096-020-04121-1
  • Morrissey I, Olesky M, Hawser S, et al. In vitro activity of eravacycline against gram-negative bacilli isolated in clinical laboratories worldwide from 2013 to 2017. Antimicrob Agents Chemother. 2020;64(3). doi: 10.1128/AAC.01699-19
  • Ni W, Han Y, Liu J, et al. Tigecycline Treatment for Carbapenem-Resistant Enterobacteriaceae Infections: A Systematic Review and Meta-Analysis. Medicine (Baltimore). 2016;95(11):e3126. doi: 10.1097/MD.0000000000003126
  • Pogue JM, Neelakanta A, Mynatt RP, et al. Carbapenem-resistance in gram-negative bacilli and intravenous minocycline: an antimicrobial stewardship approach at the detroit medical center. Clin Infect Dis. 2014;59(Suppl 6):S388–393. doi:10.1093/cid/ciu594
  • Wang J, Shah BK, Zhao J, et al. Comparative study of polymyxin B and colistin sulfate in the treatment of severe comorbid patients infected with CR-GNB. BMC Infect Dis. 2023;23(1):351. doi:10.1186/s12879-023-08339-0
  • Ruedas-Lopez A, Alonso-Garcia I, Lasarte-Monterrubio C, et al. Selection of AmpC beta-Lactamase Variants and Metallo-beta-Lactamases Leading to Ceftolozane/Tazobactam and Ceftazidime/Avibactam Resistance during Treatment of MDR/XDR Pseudomonas aeruginosa Infections. Antimicrob Agents Chemother. 2022;66(2):e0206721. doi: 10.1128/aac.02067-21
  • Voor in ‘t Holt, A. F, Severin, J. A. Hagenaars MBH, et al. VIM-positive Pseudomonas aeruginosa in a large tertiary care hospital: matched case-control studies and a network analysis. Antimicrob Resist Infect Control. 2018;7(1):32. doi: 10.1186/s13756-018-0325-1
  • Haddad SF, Allaw F, Kanj SS. Duration of antibiotic therapy in Gram-negative infections with a particular focus on multidrug-resistant pathogens. Curr Opin Infect Dis. 2022;35(6):614–620. doi:10.1097/QCO.0000000000000861
  • Sanders NH, Hannibal T. An outbreak of New Delhi metallo-beta-lactamase among intensive care unit patients in an acute care hospital. American Journal Of Infection Control. 2022;50(7):S27–S28. doi: 10.1016/j.ajic.2022.03.038
  • Koo VS, O’Neill P, Elves A. Multidrug-resistant NDM-1 Klebsiella outbreak and infection control in endoscopic urology. BJU Int. 2012;110(11 Pt C):E922–926. doi:10.1111/j.1464-410X.2012.11556.x
  • Bruins MJ, Ter Heege AH K, van den Bos-KromhoutMI, et al. VIM-carbapenemase-producing Escherichia coli in a residential care home in the Netherlands. J Hosp Infect. 2020;104(1):20–26. doi:10.1016/j.jhin.2019.08.012
  • Tischendorf J, de Avila RA, Safdar N. Risk of infection following colonization with carbapenem-resistant enterobactericeae: a systematic review. Am J Infect Control. 2016;44(5):539–543. doi:10.1016/j.ajic.2015.12.005
  • Richter SS, Marchaim D. Screening for carbapenem-resistant enterobacteriaceae: who, when, and how? Virulence. 2017;8(4):417–426. doi:10.1080/21505594.2016.1255381
  • Pirzadian J, Voor in ‘t Holt AF, Hossain M, et al. Limiting spread of VIM-positive Pseudomonas aeruginosa from colonized sink drains in a tertiary care hospital: a before-and-after study. PloS One. 2023;18(3):e0282090. doi: 10.1371/journal.pone.0282090
  • Liu B, Trout REL, Chu GH, et al. Discovery of taniborbactam (VNRX-5133): a broad-spectrum serine- and metallo-beta-lactamase inhibitor for carbapenem-resistant bacterial infections. J Med Chem. 2020;63(6):2789–2801. doi: 10.1021/acs.jmedchem.9b01518
  • Hecker SJ, Reddy KR, Lomovskaya O, et al. Discovery of cyclic boronic acid QPX7728, an ultrabroad-spectrum inhibitor of serine and metallo-beta-lactamases. J Med Chem. 2020;63(14):7491–7507. doi: 10.1021/acs.jmedchem.9b01976
  • Khairnar K, Raut MP, Chandekar RH, et al. Novel bacteriophage therapy for controlling metallo-beta-lactamase producing Pseudomonas aeruginosa infection in catfish. BMC Vet Res. 2013;9(1):264. doi: 10.1186/1746-6148-9-264

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