The DOI matches its Crossref record; 462 of the 464 references it cites were found in a registry or an index.
Three Decades of β-Lactamase Inhibitors
Open accessAbstract
Since the introduction of penicillin, beta-lactam antibiotics have been the antimicrobial agents of choice. Unfortunately, the efficacy of these life-saving antibiotics is significantly threatened by bacterial beta-lactamases. beta-Lactamases are now responsible for resistance to penicillins, extended-spectrum cephalosporins, monobactams, and carbapenems. In order to overcome beta-lactamase-mediated resistance, beta-lactamase inhibitors (clavulanate, sulbactam, and tazobactam) were introduced into clinical practice. These inhibitors greatly enhance the efficacy of their partner beta-lactams (amoxicillin, ampicillin, piperacillin, and ticarcillin) in the treatment of serious Enterobacteriaceae and penicillin-resistant staphylococcal infections. However, selective pressure from excess antibiotic use accelerated the emergence of resistance to beta-lactam-beta-lactamase inhibitor combinations. Furthermore, the prevalence of clinically relevant beta-lactamases from other classes that are resistant to inhibition is rapidly increasing. There is an urgent need for effective inhibitors that can restore the activity of beta-lactams. Here, we review the catalytic mechanisms of each beta-lactamase class. We then discuss approaches for circumventing beta-lactamase-mediated resistance, including properties and characteristics of mechanism-based inactivators. We next highlight the mechanisms of action and salient clinical and microbiological features of beta-lactamase inhibitors. We also emphasize their therapeutic applications. We close by focusing on novel compounds and the chemical features of these agents that may contribute to a "second generation" of inhibitors. The goal for the next 3 decades will be to design inhibitors that will be effective for more than a single class of beta-lactamases.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“Clavulanic acid, a potent β-lactamase inhibitor, was developed to overcome this limitation by binding irreversibly to the active site of β-lactamase enzymes, thereby protecting amoxicillin from enzymatic degradation and restoring its antimicrobial spectrum [3].”
From Clinical Outcomes and Real-World Effectiveness of Amoxicillin-Clavulanic Acid Across Indian Healthcare Settings: A Retrospective Multicenter Study (2026) · cites this paper as [3]
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Extended-Spectrum β-Lactamases: a Clinical Update
Paterson, D. L., & Bonomo, R. A. (2005) · Clinical Microbiology Reviews · doi:10.1128/cmr.18.4.657-686.2005 · Cited by 3,495
Self-citationBradford, P. A. (2001) · Clinical Microbiology Reviews · doi:10.1128/cmr.14.4.933-951.2001 · Cited by 2,646
Carbapenemases: the Versatile β-Lactamases
Queenan, A. M., & Bush, K. (2007) · Clinical Microbiology Reviews · doi:10.1128/cmr.00001-07 · Cited by 2,609
A functional classification scheme for beta-lactamases and its correlation with molecular structure
Bush, K., Jacoby, G. A., & Medeiros, A. A. (1995) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.39.6.1211 · Cited by 2,485
Updated Functional Classification of β-Lactamases
Bush, K., & Jacoby, G. A. (2010) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01009-09 · Cited by 2,367
Federal Funding for the Study of Antimicrobial Resistance in Nosocomial Pathogens: No ESKAPE
Rice, L. B. (2008) · The Journal of Infectious Diseases · doi:10.1086/533452 · Cited by 2,328
Jacoby, G. A. (2009) · Clinical Microbiology Reviews · doi:10.1128/cmr.00036-08 · Cited by 2,277
Extended-spectrum β-lactamase-producing Enterobacteriaceae: an emerging public-health concern
Pitout, J. D. D., & Laupland, K. B. (2008) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(08)70041-0 · Cited by 2,068
The real threat of Klebsiella pneumoniae carbapenemase-producing bacteria
Nordmann, P., Cuzon, G., & Naas, T. (2009) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(09)70054-4 · Cited by 1,619
Prevention of Drug Access to Bacterial Targets: Permeability Barriers and Active Efflux
Nikaido, H. (1994) · Science · doi:10.1126/science.8153625 · Cited by 1,542
Research works printed but not linked: 14
- Danel, F., M. G. Page, and D. M. Livermore. 2007. Class D β-lactamases, p. 163-194. In R. A. Bonomo and M. E. Tolmasky (ed.), Enzyme-mediated resistance to antibiotics: mechanisms, dissemination, and prospects for inhibition. ASM Press, Washington, DC.
- Abstr. 47th Intersci. Conf. Antimicrob. Agents Chemother. 2007
- Dubus, A., P. Ledent, J. Lamotte-Brasseur, and J. M. Frere. 1996. The roles of residues Tyr150, Glu272, and His314 in class C β-lactamases. Proteins25:473-485.
- Foulds, G., W. E. Barth, J. R. Bianchine, A. R. English, D. Girard, S. L. Hayes, M. O'Brien, and P. Somani. 1980. Pharmacokinetics of CP-45.899 and pro-drug CP-47.904 in animals and humans, p. 353-356. In J. D. Nelson and C. Grassi (ed.), Current chemotherapy and infectious disease. American Society for Microbiology, Washington DC.
- Galleni, M., and J. M. Frere. 2007. Kinetics of β-lactamases and pencillin-binding proteins, p. 195-213. In R. A. Bonomo and M. E. Tolmasky (ed.), Enzyme-mediated resistance to antibiotics: mechanisms, dissemination, and prospects for inhibition. ASM Press, Washington, DC.
- F1-310. Abstr. 47th Intersci. Conf. Antimicrob. Agents Chemother. 2007
- F1-333a. Abstr. 47th Intersci. Conf. Antimicrob. Agents Chemother. 2007
- Livermore, D. M., M. Akova, P. J. Wu, and Y. J. Yang. 1989. Clavulanate and β-lactamase induction. J. Antimicrob. Chemother.24(Suppl. B):23-33.
- A1-006. Abstr. 49th Intersci. Conf. Antimicrob. Agents Chemother. 2009
- Meroueh, S., J. Cha, and S. Mobashery. 2007. Inhibition of class A β-lactamases, p. 101-114. In R. A. Bonomo and M. E. Tolmasky (ed.), Enzyme-mediated resistance to antibiotics: mechanisms, dissemination, and prospects for inhibition. ASM Press, Washingtion, DC.
- Page, M. G. 2007. Resistance mediated by penicllin-binding proteins, p. 81-99. In R. A. Bonomo and M. E. Tolmasky (ed.), Enzyme-mediated resistance to antibiotics: mechanisms, dissemination, and prospects for Inhibition. ASM Press, Washington, DC.
- F1-311. Abstr. 47th Intersci. Conf. Antimicrob. Agents Chemother. 2007
- F1-0882. Abstr. 47th Intersci. Conf. Antimicrob. Agents Chemother. 2007
- Slocombe, B., A. S. Beale, R. J. Boon, K. E. Griffin, P. J. Masters, R. Sutherland, and A. R. White. 1984. Antibacterial activity in vitro and in vivo of amoxicillin in the presence of clavulanic acid, p. 29-49. InProgress and perspectives on β-lactamase inhibition: a review of Augmentin. Custom Communications: Postgraduate Medicine, New York, NY.
Cited by
Sorted by citations
Items 301–400 of 1,001
Pokhrel, R., Shakya, R., Baral, P., & Chapagain, P. P. (2022) · Journal of Chemical Information and Modeling · doi:10.1021/acs.jcim.2c00437 · Cited by 61
Singh, B., Bhat, A., Dutta, L., Pati, K. R., Korpan, Y. I., & Dahiya, I. (2023) · Biosensors · doi:10.3390/bios13090867 · Cited by 62
Antibiotic Susceptibility of Periodontal Enterococcus faecalis
Rams, T. E., Feik, D., Mortensen, J. E., Degener, J. E., & Winkelhoff, A. J. V. (2012) · Journal of Periodontology · doi:10.1902/jop.2012.120050 · Cited by 62
Chen, C., Yang, X., Yang, K., Zhang, Y., Wang, W., Su, J.-P., Ge, Y., & Liu, Y. (2018) · Chemical Communications · doi:10.1039/c8cc01067f · Cited by 62
Sukhum, K. V., Diorio‐Toth, L., & Dantas, G. A. (2019) · Clinical Pharmacology & Therapeutics · doi:10.1002/cpt.1535 · Cited by 60
Probing the Interaction of Aspergillomarasmine A with Metallo-β-lactamases NDM-1, VIM-2, and IMP-7
Bergström, A., Katko, A., Adkins, Z., Hill, J., Cheng, Z., Burnett, M., Yang, H., Aitha, M., Mehaffey, M. R., Brodbelt, J. S., et al. (2017) · ACS Infectious Diseases · doi:10.1021/acsinfecdis.7b00106 · Cited by 62
Self-citationLiving fabrication of functional semi-interpenetrating polymeric materials
Dai, Z., Yang, X., Wu, F., Wang, L., Xiang, K., Li, P., Lv, Q., Tang, J., Dohlman, A. B., Dai, L., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-23812-7 · Cited by 61
Faheem, M., Rehman, M. T., Danishuddin, M., & Khan, A. U. (2013) · PLoS ONE · doi:10.1371/journal.pone.0056926 · Cited by 65
Feng, L., Yang, K., Zhou, L., Xiao, J.-M., Yang, X., Zhai, L., Zhang, Y., & Crowder, M. W. (2012) · Bioorganic & Medicinal Chemistry Letters · doi:10.1016/j.bmcl.2012.06.074 · Cited by 61
Semighini, C. P., Averette, A. F., Perfect, J. R., & Heitman, J. (2011) · PLoS Pathogens · doi:10.1371/journal.ppat.1002364 · Cited by 61
Wu, J., Racine, F., Wismer, M. K., Young, K., Carr, D. M., Xiao, J. C., Katwaru, R., Si, Q., Harradine, P. J., Motyl, M. R., et al. (2018) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.02323-17 · Cited by 61
Deng, W., Fu, T., Zhang, Z., Jiang, X. Y., Xie, J., Sun, H., Hu, P., Ren, H., Zhou, P., Liu, Q., et al. (2020) · Emerging Microbes & Infections · doi:10.1080/22221751.2020.1740611 · Cited by 61
Novel Modeling Framework To Guide Design of Optimal Dosing Strategies for β-Lactamase Inhibitors
Bhagunde, P. R., Chang, K., Hirsch, E. B., Ledesma, K. R., Nikolaou, M., & Tam, V. H. (2012) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.06113-11 · Cited by 60
Cao, J., Kürsten, D., Schneider, S., Knauer, A., Günther, P. M., & Köhler, J. M. (2011) · Lab on a Chip · doi:10.1039/c1lc20584f · Cited by 60
Stogios, P. J., Spanogiannopoulos, P., Evdokimova, E., Egorova, O., Shakya, T., Todorovic, N., Capretta, A. A., Wright, G. D., & Savchenko, A. V. (2013) · Biochemical Journal · doi:10.1042/bj20130317 · Cited by 60
King, A. M., King, D. T., French, S., Brouillette, É., Asli, A., Alexander, J. A. N., Vuckovic, M., Maiti, S. N., Parr, T. R., Brown, E. D., et al. (2016) · ACS Chemical Biology · doi:10.1021/acschembio.5b00944 · Cited by 60
Potential therapeutic targets of Klebsiella pneumoniae: a multi-omics review perspective
Ali, S., Alam, M., Hasan, G. M., & Hassan, M. I. (2021) · Briefings in Functional Genomics · doi:10.1093/bfgp/elab038 · Cited by 62
Castanheira, M., Doyle, T. B., Deshpande, L. M., Mendes, R. E., & Sader, H. S. (2021) · International Journal of Antimicrobial Agents · doi:10.1016/j.ijantimicag.2021.106439 · Cited by 59
Dückert, H., Khedkar, V., Waldmann, H., & Kumar, K. (2011) · Chemistry - A European Journal · doi:10.1002/chem.201003572 · Cited by 59
Li, W.-J., Li, D., Hu, Y., Zhang, X., Bi, L., & Wang, D. (2013) · Cell Research · doi:10.1038/cr.2013.53 · Cited by 59
Liu, S., Jing, L., Yu, Z., Wu, C., Zheng, Y., Zhang, E., Chen, Q., Yu, Y., Guo, L., Wu, Y., et al. (2018) · European Journal of Medicinal Chemistry · doi:10.1016/j.ejmech.2018.01.032 · Cited by 59
Barnes, M. D., Taracila, M. A., Good, C. E., Bajaksouzian, S., Rojas, L. J., van Duin, D., Kreiswirth, B. N., Jacobs, M. R., Haldimann, A., Papp‐Wallace, K. M., et al. (2019) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00432-19 · Cited by 62
Self-citationGajdács, M., & Spengler, G. (2019) · Antibiotics · doi:10.3390/antibiotics8040270 · Cited by 61
Kim, S. W., Lee, J., Park, S. B., Lee, A. R., Jung, J. W., Chun, J. H., Lazarte, J. M. S., Kim, J., Seo, J., Kim, J.-H., et al. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21082822 · Cited by 58
Costa, R. C., Bertolini, M., Oliveira, B. E. C., NAGAY, B. E., Dini, C., Benso, B., Klein, M. I., Barão, V. A. R., & Souza, J. G. S. (2022) · Critical Reviews in Microbiology · doi:10.1080/1040841x.2022.2062219 · Cited by 62
Händel, N., Otte, S., Jonker, M. J., Brul, S., & ter Kuile, B. H. (2015) · PLoS ONE · doi:10.1371/journal.pone.0123039 · Cited by 58
Papp‐Wallace, K. M., Taracila, M. A., Gatta, J. A., Ohuchi, N., Bonomo, R. A., & Nukaga, M. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.458315 · Cited by 58
Self-citationApplying ecological resistance and resilience to dissect bacterial antibiotic responses
Meredith, H. R., Andreani, V., Ma, H. R., Lopatkin, A. J., Lee, A. J., Anderson, D. J., Batt, G., & You, L. (2018) · Science Advances · doi:10.1126/sciadv.aau1873 · Cited by 56
Tremblay, L. W., Xu, H., & Blanchard, J. S. (2010) · Biochemistry · doi:10.1021/bi1015088 · Cited by 58
Du, S., Hu, X., Menéndez‐Arias, L., Zhan, P., & Liu, X. (2024) · Drug Resistance Updates · doi:10.1016/j.drup.2024.101053 · Cited by 61
Vestergaard, M. R., Leng, B., Haaber, J., Bojer, M. S., Vegge, C. S., & Ingmer, H. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.02018 · Cited by 58
Biowaiver Monograph for Immediate-Release Solid Oral Dosage Forms: Amoxicillin Trihydrate
Thambavita, D., Galappatthy, P., Mannapperuma, U., Jayakody, L., Cristofoletti, R., Abrahamsson, B., Groot, D. W., Langguth, P., Mehta, M., Parr, A. F., et al. (2017) · Journal of Pharmaceutical Sciences · doi:10.1016/j.xphs.2017.04.068 · Cited by 57
Mortimer, M., Devarajan, N., Li, D., & Holden, P. A. (2018) · ACS Nano · doi:10.1021/acsnano.7b08977 · Cited by 57
Jin, W., Xu, C., Cheng, Q., Qi, X. L., Gao, W., Zheng, Z., Chan, E. W., Leung, Y., Chan, T. H., Wong, K., et al. (2018) · European Journal of Medicinal Chemistry · doi:10.1016/j.ejmech.2018.06.007 · Cited by 57
Gaibani, P., Lombardo, D., Bussini, L., Bovo, F., Munari, B., Giannella, M., Bartoletti, M., Viale, P., Lazzarotto, T., & Ambretti, S. (2021) · Antibiotics · doi:10.3390/antibiotics10050536 · Cited by 57
McGeary, R. P., Tan, D. T. C., Selleck, C., Pedroso, M. M., Sidjabat, H. E., & Schenk, G. (2017) · European Journal of Medicinal Chemistry · doi:10.1016/j.ejmech.2017.05.061 · Cited by 56
Prospects for circumventing aminoglycoside kinase mediated antibiotic resistance
Shi, K., Caldwell, S. J., Fong, D. H., & Berghuis, A. M. (2013) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2013.00022 · Cited by 56
Inhibition of β-lactamases of mycobacteria by avibactam and clavulanate
Soroka, D., Ourghanlian, C., Compain, F., Fichini, M., Dubée, V., Mainardi, J., Hugonnet, J., & Arthur, M. (2016) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkw546 · Cited by 55
Slater, C., Winogrodzki, J. L., Fraile-Ribot, P. A., Oliver, A., Khajehpour, M., & Mark, B. L. (2020) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00894-20 · Cited by 55
Imipenem/cilastatin/relebactam: A new carbapenem β-lactamase inhibitor combination
Mansour, H., Ouweini, A. E., Chahine, E. B., & Karaoui, L. R. (2021) · American Journal of Health-System Pharmacy · doi:10.1093/ajhp/zxab012 · Cited by 55
Rojas, L. J., Taracila, M. A., Papp‐Wallace, K. M., Bethel, C. R., Caselli, E., Romagnoli, C., Winkler, M., Spellberg, B. J., Prati, F., & Bonomo, R. A. (2016) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.02641-15 · Cited by 54
Self-citationEmerging Strategies to Combat β-Lactamase Producing ESKAPE Pathogens
Vrâncianu, C. O., Gheorghe, I., Dobre, E.-G., Barbu, I. C., Cristian, R.-E., Popa, M., Lee, S. H., Limban, C., Vlad, I. M., & Chifiriuc, M. C. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21228527 · Cited by 55
New β-Lactam/β-Lactamase Inhibitor Combination Antibiotics
Σαργιάνου, Μ., Stathopoulos, P., Vrysis, C., Tzvetanova, I. D., & Falagas, M. E. (2025) · Pathogens · doi:10.3390/pathogens14040307 · Cited by 54
The synthesis and antibacterial activity of pyrazole-fused tricyclic diterpene derivatives
Yu, L., Ni, T., Gao, W., He, Y., Wang, Y., Cui, H., Yang, C., & Qiu, W. (2014) · European Journal of Medicinal Chemistry · doi:10.1016/j.ejmech.2014.11.015 · Cited by 54
Mistranslation drives the evolution of robustness in TEM-1 β-lactamase
Bratulić, S., Gerber, F., & Wagner, A. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1510071112 · Cited by 54
Evren, E., Azap, Ö. K., Çolakoğlu, Ş., & Arslan, H. (2013) · Diagnostic Microbiology and Infectious Disease · doi:10.1016/j.diagmicrobio.2013.04.004 · Cited by 54
Yang, S.-K., Kang, J. S., Oelschlaeger, P., & Yang, K. (2015) · ACS Medicinal Chemistry Letters · doi:10.1021/ml500534c · Cited by 54
Azam, M., Jan, A. T., & Haq, Q. M. R. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.00176 · Cited by 54
A Self‐Immobilizing and Fluorogenic Probe for β‐Lactamase Detection
Mao, W., Xia, L., Wang, Y., & Xie, H. (2016) · Chemistry - An Asian Journal · doi:10.1002/asia.201601344 · Cited by 54
Davies, T. J., Stoesser, N. E., Sheppard, A. E., AbuOun, M., Fowler, P. W., Swann, J., Quan, T. P., Griffiths, D., Vaughan, A., Morgan, M. R., et al. (2020) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.02026-19 · Cited by 54
Self-citationModular, stereocontrolled C β –H/C α –C activation of alkyl carboxylic acids
Shang, M., Feu, K. S., Vantourout, J. C., Barton, L. M., Osswald, H. L., Kato, N., Gagaring, K., McNamara, C. W., Chen, G., Hu, L., et al. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1903048116 · Cited by 53
Magkoufopoulou, C., Claessen, S. M. H., Jennen, D. G. J., Kleinjans, J. C. S., & van Delft, J. H. M. (2011) · Mutagenesis · doi:10.1093/mutage/ger021 · Cited by 55
The Role of the Ω-Loop in Regulation of the Catalytic Activity of TEM-Type β-Lactamases
Egorov, A. M., Rubtsova, M. Y., Григоренко, В. Г., Uporov, I. V., & Veselovsky, A. V. (2019) · Biomolecules · doi:10.3390/biom9120854 · Cited by 54
Wang, T., Zhang, P., Lv, H., Deng, X., & Wang, J. (2020) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2020.00330 · Cited by 53
Heinz, E. (2018) · Microbial Genomics · doi:10.1099/mgen.0.000214 · Cited by 52
A novel flow cytometric assay for rapid detection of extended-spectrum beta-lactamases
Faria‐Ramos, I., Espinar, M. J., Rocha, R., Santos‐Antunes, J., Rodrigues, A. G., Cantón, R., & Pina‐Vaz, C. (2012) · Clinical Microbiology and Infection · doi:10.1111/j.1469-0691.2012.03986.x · Cited by 52
Papp‐Wallace, K. M., Taracila, M. A., Smith, K. M., Xu, Y., & Bonomo, R. A. (2012) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.05769-11 · Cited by 52
Self-citationPulmonary Penetration of Piperacillin and Tazobactam in Critically Ill Patients
Felton, T., McCalman, K., Malagon, I. L., Isalska, B. J., Whalley, S., Goodwin, J., Bentley, A. M., & Hope, W. W. (2014) · Clinical Pharmacology & Therapeutics · doi:10.1038/clpt.2014.131 · Cited by 52
Ke, W., Bethel, C. R., Papp‐Wallace, K. M., Pagadala, S. R. R., Nottingham, M., Fernández, D., Buynak, J. D., Bonomo, R. A., & van den Akker, F. (2012) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.06099-11 · Cited by 52
Self-citationThe global need for effective antibiotics—A summary of plenary presentations
Alván, G., Edlund, C., & Heddini, A. (2011) · Drug Resistance Updates · doi:10.1016/j.drup.2011.01.007 · Cited by 52
Zhang, J., Wang, S., Wei, Q., Guo, Q., Bai, Y., Yang, S., Song, F., Zhang, L., & Lei, X. (2017) · Bioorganic & Medicinal Chemistry · doi:10.1016/j.bmc.2017.07.025 · Cited by 52
Sheu, C., Lin, S., Chang, Y.-T., Lee, C.-Y., Chen, Y., & Hsueh, P. (2018) · Expert Review of Anti-infective Therapy · doi:10.1080/14787210.2018.1436966 · Cited by 53
Peng, L., Xiao, L., Ding, Y., Xiang, Y., & Tong, A. (2018) · Journal of Materials Chemistry B · doi:10.1039/c8tb00414e · Cited by 52
Resveratrol enhances the efficacy of aminoglycosides against Staphylococcus aureus
Nøhr-Meldgaard, K., Ovsepian, A., Ingmer, H., & Vestergaard, M. R. (2018) · International Journal of Antimicrobial Agents · doi:10.1016/j.ijantimicag.2018.06.005 · Cited by 55
Moyá, B., Barceló, I. M., Cabot, G., Torrens, G., Palwe, S. R., Joshi, P., Umarkar, K., Takalkar, S., Periasamy, H., Bhagwat, S., et al. (2019) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00128-19 · Cited by 52
Antibiotic Resistance and the MRSA Problem
Vestergaard, M. R., Frees, D., & Ingmer, H. (2019) · ASM Press eBooks · doi:10.1128/9781683670131.ch47 · Cited by 53
β-Lactamase Inhibitors: An Update
Chen, J., Shang, X., Hu, F., Lao, X., Gao, X., Zheng, H., & Yao, W. (2013) · Mini-Reviews in Medicinal Chemistry · doi:10.2174/13895575113139990074 · Cited by 51
Total Synthesis and Structural Reassignment of Aspergillomarasmine A
Liao, D., Yang, S., Wang, J., Zhang, J., Hong, B., Wu, F., & Lei, X. (2015) · Angewandte Chemie International Edition · doi:10.1002/anie.201509960 · Cited by 51
In vitro evaluation of metal chelators as potential metallo- β -lactamase inhibitors
Azumah, R., Dutta, J., Somboro, A. M., Ramtahal, M. A., Chonco, L., Parboosing, R., Bester, L. A., Kruger, H. G., Naicker, T., Essack, S. Y., et al. (2016) · Journal of Applied Microbiology · doi:10.1111/jam.13085 · Cited by 51
Gordon, E. M., Duncton, M. A. J., & Gallop, M. A. (2018) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.8b01389 · Cited by 51
A systematic review and meta-analysis of antimicrobial resistance in paediatric acute otitis media
Mather, M. W., Drinnan, M. J., Perry, J. D., Powell, S. M., Wilson, J. A., & Powell, J. (2019) · International Journal of Pediatric Otorhinolaryngology · doi:10.1016/j.ijporl.2019.04.041 · Cited by 51
Kotsakis, S. D., Miriagou, V., Tzelepi, Ε., & TZOUVELEKIS, L. S. (2010) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00771-10 · Cited by 51
Salimraj, R., Hinchliffe, P., Kosmopoulou, M. N., Tyrrell, J. M., Brem, J., van Berkel, S. S., Verma, A. K., Owens, R. J., McDonough, M. A., Walsh, T. R., et al. (2018) · FEBS Journal · doi:10.1111/febs.14695 · Cited by 50
Reappraising the use of β-lactams to treat tuberculosis
Kurz, S. G., & Bonomo, R. A. (2012) · Expert Review of Anti-infective Therapy · doi:10.1586/eri.12.96 · Cited by 50
Self-citationTargeting Class A and C Serine β-Lactamases with a Broad-Spectrum Boronic Acid Derivative
Tondi, D., Venturelli, A., Bonnet, R., Pozzi, C., Shoichet, B. K., & Costi, M. P. (2014) · Journal of Medicinal Chemistry · doi:10.1021/jm5006572 · Cited by 50
Exploring the Role of Residue 228 in Substrate and Inhibitor Recognition by VIM Metallo-β-lactamases
Mojica, M. F., Mahler, G., Bethel, C. R., Taracila, M. A., Kosmopoulou, M. N., Papp‐Wallace, K. M., Llarrull, L. I., Wilson, B. M., Marshall, S. H., Wallace, C. J., et al. (2015) · Biochemistry · doi:10.1021/acs.biochem.5b00106 · Cited by 50
Self-citationWhat Approaches to Thwart Bacterial Efflux Pumps-Mediated Resistance?
Seukep, A. J., Mbuntcha, H. G., Kuete, V., Chu, Y., Fan, E., & Guo, M. (2022) · Antibiotics · doi:10.3390/antibiotics11101287 · Cited by 50
Page, M. G. P., Dantier, C., Desarbre, E., Gaucher, B., Gebhardt, K., & Schmitt‐Hoffmann, A. H. (2011) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01370-10 · Cited by 49
Drawz, S. M., Taracila, M. A., Caselli, E., Prati, F., & Bonomo, R. A. (2011) · Protein Science · doi:10.1002/pro.612 · Cited by 49
Self-citationThe development of efflux pump inhibitors to treat Gram-negative infections
Blanco, P., Sanz‐García, F., Hernando‐Amado, S., Martínez, J. L., & Alcalde‐Rico, M. (2018) · Expert Opinion on Drug Discovery · doi:10.1080/17460441.2018.1514386 · Cited by 49
Noman, E. A., Al-Gheethi, A. A. S., Talip, B. A., Mohamed, R. M. S. R., & Kassim, A. H. M. (2019) · PLoS ONE · doi:10.1371/journal.pone.0221522 · Cited by 50
Identifying Oxacillinase-48 Carbapenemase Inhibitors Using DNA-Encoded Chemical Libraries
Taylor, D. M., Anglin, J. L., Park, S., Ucisik, M. N., Faver, J. C., Simmons, N., Jin, Z., Palaniappan, M., Nyshadham, P., Li, F., et al. (2020) · ACS Infectious Diseases · doi:10.1021/acsinfecdis.0c00015 · Cited by 49
A Clinical Review and Critical Evaluation of Imipenem-Relebactam: Evidence to Date
Campanella, T. A., & Gallagher, J. C. (2020) · Infection and Drug Resistance · doi:10.2147/idr.s224228 · Cited by 48
Hirvonen, V. H. A., SPENCER, J. M., & van der Kamp, M. W. (2021) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00184-21 · Cited by 48
Kuo, S., Lee, Y., Lauderdale, T.-L. Y., Huang, W., Chuang, M.-F., Chen, C.-P., Su, S.-C., Lee, K., & Chen, T.-L. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2015.00231 · Cited by 48
β-Lactam Antibiotics Renaissance
Qin, W., Panunzio, M., & Biondi, S. (2014) · Antibiotics · doi:10.3390/antibiotics3020193 · Cited by 49
Molecular Mechanisms of Substrate Recognition and Specificity of New Delhi Metallo-β-Lactamase
Chiou, J. A., Leung, T. Y.-C., & Chen, S. (2014) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01977-13 · Cited by 48
Zhang, D., Wang, Y., Lu, J. L., & Pang, Y. (2015) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01035-15 · Cited by 48
Copper Ions and Coordination Complexes as Novel Carbapenem Adjuvants
Djoko, K. Y., Achard, M. E. S., Phan, M., Lo, A. W. H., Miraula, M., Prombhul, S., Hancock, S. J., Peters, K. M., Sidjabat, H. E., Harris, P. N. A., et al. (2017) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.02280-17 · Cited by 48
2D-MoS2-Based β-Lactamase Inhibitor for Combination Therapy against Drug-Resistant Bacteria
Ali, S. R., Pandit, S., & De, M. (2018) · ACS Applied Bio Materials · doi:10.1021/acsabm.8b00105 · Cited by 48
Liu, X., Xu, T., Jiang, C., Li, Y., Su, B., Zhao, W., & Zhao, C. (2022) · Biomacromolecules · doi:10.1021/acs.biomac.2c00583 · Cited by 48
Pereira, J. H. O. S., Reis, A. C., Homem, V., Silva, J. A., Alves, A., Borges, M.-T., Boaventura, R. A. R., Vilar, V. J. P., & Nunes, O. C. (2014) · Water Research · doi:10.1016/j.watres.2014.07.037 · Cited by 47
Arjomandi, O. K., Hussein, W. M., Vella, P., Yusof, Y., Sidjabat, H. E., Schenk, G., & McGeary, R. P. (2016) · European Journal of Medicinal Chemistry · doi:10.1016/j.ejmech.2016.03.017 · Cited by 47
Lewandowski, E. M., Szczupak, Ł., Wong, S., Skiba, J., Guśpiel, A., Solecka, J., Vrček, V., Kowalski, K., & Chen, Y. (2017) · Organometallics · doi:10.1021/acs.organomet.6b00888 · Cited by 47
Calvopiña, K., Hinchliffe, P., Brem, J., Heesom, K. J., Johnson, S., Cain, R. M., Lohans, C. T., Fishwick, C. W. G., Schofield, C. J., SPENCER, J. M., et al. (2017) · Molecular Microbiology · doi:10.1111/mmi.13831 · Cited by 47
Smith, C. C., Srygley, R. B., Healy, F. G., Swaminath, K., & Mueller, U. G. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.00801 · Cited by 46
Idowu, T., Ammeter, D., Arthur, G., Zhanel, G. G., & Schweizer, F. (2019) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkz228 · Cited by 47
Winkler, M., Rodkey, E. A., Taracila, M. A., Drawz, S. M., Bethel, C. R., Papp‐Wallace, K. M., Smith, K. M., Xu, Y., Dwulit‐Smith, J. R., Romagnoli, C., et al. (2012) · Journal of Medicinal Chemistry · doi:10.1021/jm301490d · Cited by 45
Self-citationStructural and Kinetic Studies on Metallo-β-lactamase IMP-1
Griffin, D. H., Richmond, T. K., Sanchez, C., Moller, A., Breece, R. M., Tierney, D. L., Bennett, B., & Crowder, M. W. (2011) · Biochemistry · doi:10.1021/bi200839h · Cited by 45
Systematic Analysis of Metallo-β-Lactamases Using an Automated Database
Widmann, M., Pleiss, J., & Oelschlaeger, P. (2012) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00255-12 · Cited by 45
Metadata
- Authors
- Drawz, S. M., & Bonomo, R. A.
- Affiliations
- Departments of Pathology
- United States Department of Veterans Affairs (US)
- Corresponding author
- Bonomo, Robert A.
- ORCID
- Bonomo, Robert A.
- Venue
- Clinical Microbiology Reviews
- Publisher
- American Society for Microbiology
- Published
- 2010-01
- Volume
- 23
- Issue
- 1
- Pages
- 160-201
- ISSN
- 0893-8512 (ISSN-L)
- 1098-6618
- PMC
- PMC2806661
- OpenAlex
- W1895007034
- Cited by
- 1,709
- References
- 464
- Citations by year
- 2026: 83 · 2025: 100 · 2024: 87 · 2023: 86 · 2022: 106 · 2021: 126 · 2020: 151 · 2019: 130 · 2018: 131 · 2017: 119 · 2016: 120 · 2015: 108 · 2014: 93 · 2013: 88 · 2012: 81
- FWCI
- 4.26
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Clinical Microbiology Reviews (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- U.S. Public Health Service (1R01A1063517-01)
- National Institute of General Medical Sciences (T32GM007250, T32GM07250)
- Topics
- Health Sciences › Medicine › Microbiology (medical) › Antibiotic Resistance in Bacteria
- Health Sciences › Medicine › Pharmacology (medical) › Antibiotics Pharmacokinetics and Efficacy
- Physical Sciences › Chemistry › Organic Chemistry › Synthesis of β-Lactam Compounds
- Keywords
- beta-lactamase inhibitors, beta-lactamase, beta-lactam resistance, clavulanic acid, sulbactam, tazobactam, mechanism-based inactivators, carbapenemase inhibitors, extended-spectrum cephalosporin resistance, Enterobacteriaceae, penicillin-resistant staphylococci
- MeSH terms
- Bacteria, Bacterial Infections, Bacterial Proteins, beta-Lactamases, Enzyme Inhibitors, Humans, beta-Lactam Resistance, beta-Lactamase Inhibitors
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review