{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,26]],"date-time":"2026-09-26T01:50:32Z","timestamp":1790387432768,"version":"4.1.0"},"reference-count":127,"publisher":"MDPI AG","issue":"6","license":[{"start":{"date-parts":[[2023,6,1]],"date-time":"2023-06-01T00:00:00Z","timestamp":1685577600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Microorganisms"],"abstract":"<jats:p>Anaerobic bacteria are normal inhabitants of the human commensal microbiota and play an important role in various human infections. Tedious and time-consuming, antibiotic susceptibility testing is not routinely performed in all clinical microbiology laboratories, despite the increase in antibiotic resistance among clinically relevant anaerobes since the 1990s. \u03b2-lactam and metronidazole are the key molecules in the management of anaerobic infections, to the detriment of clindamycin. \u03b2-lactam resistance is usually mediated by the production of \u03b2-lactamases. Metronidazole resistance remains uncommon, complex, and not fully elucidated, while metronidazole inactivation appears to be a key mechanism. The use of clindamycin, a broad-spectrum anti-anaerobic agent, is becoming problematic due to the increase in resistance rate in all anaerobic bacteria, mainly mediated by Erm-type rRNA methylases. Second-line anti-anaerobes are fluoroquinolones, tetracyclines, chloramphenicol, and linezolid. This review aims to describe the up-to-date evolution of antibiotic resistance, give an overview, and understand the main mechanisms of resistance in a wide range of anaerobes.<\/jats:p>","DOI":"10.3390\/microorganisms11061474","type":"journal-article","created":{"date-parts":[[2023,6,1]],"date-time":"2023-06-01T01:40:56Z","timestamp":1685583656000},"page":"1474","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":45,"title":["Recent Trends in Antimicrobial Resistance among Anaerobic Clinical Isolates"],"prefix":"10.3390","volume":"11","author":[{"given":"Sophie","family":"Reissier","sequence":"first","affiliation":[{"name":"Rennes University Hospital, Department of Clinical Microbiology, F-35033 Rennes, France"},{"name":"UMR_S1230 BRM, Inserm, University of Rennes, F-35043 Rennes, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Malo","family":"Penven","sequence":"additional","affiliation":[{"name":"Rennes University Hospital, Department of Clinical Microbiology, F-35033 Rennes, France"},{"name":"UMR_S1230 BRM, Inserm, University of Rennes, F-35043 Rennes, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6821-3131","authenticated-orcid":false,"given":"Fran\u00e7ois","family":"Gu\u00e9rin","sequence":"additional","affiliation":[{"name":"Rennes University Hospital, Department of Clinical Microbiology, F-35033 Rennes, France"},{"name":"UMR_S1230 BRM, Inserm, University of Rennes, F-35043 Rennes, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4026-9912","authenticated-orcid":false,"given":"Vincent","family":"Cattoir","sequence":"additional","affiliation":[{"name":"Rennes University Hospital, Department of Clinical Microbiology, F-35033 Rennes, France"},{"name":"UMR_S1230 BRM, Inserm, University of Rennes, F-35043 Rennes, France"},{"name":"CHU de Rennes, Service de Bact\u00e9riologie-Hygi\u00e8ne Hospitali\u00e8re, 2 Rue Henri Le Guilloux, CEDEX 9, F-35033 Rennes, France"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,6,1]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1139","DOI":"10.1016\/j.cmi.2018.02.008","article-title":"How to isolate, identify and determine antimicrobial susceptibility of anaerobic bacteria in routine laboratories","volume":"24","author":"Nagy","year":"2018","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1016\/j.anaerobe.2016.02.007","article-title":"Clinical characteristics associated with mortality of patients with anaerobic bacteremia","volume":"39","author":"Umemura","year":"2016","journal-title":"Anaerobe"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"91","DOI":"10.3947\/ic.2016.48.2.91","article-title":"Anaerobic Bacteremia: Impact of Inappropriate Therapy on Mortality","volume":"48","author":"Kim","year":"2016","journal-title":"Infect. Chemother."},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Gajd\u00e1cs, M., Spengler, G., and Urb\u00e1n, E. (2017). Identification and Antimicrobial Susceptibility Testing of Anaerobic Bacteria: Rubik\u2019s Cube of Clinical Microbiology?. Antibiotics, 6.","DOI":"10.3390\/antibiotics6040025"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"419","DOI":"10.1128\/CMR.00092-13","article-title":"Propionibacterium acnes: From Commensal to Opportunistic Biofilm-Associated Implant Pathogen","volume":"27","author":"Achermann","year":"2014","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1016\/j.jgar.2016.11.007","article-title":"Antimicrobial susceptibility of clinical isolates of Actinomyces and related genera reveals an unusual clindamycin resistance among Actinomyces urogenitalis strains","volume":"8","author":"Barberis","year":"2017","journal-title":"J. Glob. Antimicrob. Resist."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1080\/23744235.2021.1963469","article-title":"Epidemiology and antibiotic susceptibility in anaerobic bacteraemia: A 15-year retrospective study in South-Eastern Hungary","volume":"54","year":"2022","journal-title":"Infect. Dis."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"698","DOI":"10.1093\/cid\/ciu395","article-title":"Antimicrobial Resistance and Susceptibility Testing of Anaerobic Bacteria","volume":"59","author":"Schuetz","year":"2014","journal-title":"Clin. Infect. Dis."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"523","DOI":"10.1097\/QCO.0000000000000595","article-title":"Anaerobic resistance: Should we be worried?","volume":"32","author":"Cooley","year":"2019","journal-title":"Curr. Opin. Infect. Dis."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"S387","DOI":"10.1093\/clinids\/16.Supplement_4.S387","article-title":"Antibiotic Susceptibility of Anaerobic Bacteria in Europe","volume":"16","author":"Nord","year":"1993","journal-title":"Clin. Infect. Dis."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"371","DOI":"10.1111\/j.1469-0691.2010.03256.x","article-title":"Antimicrobial susceptibility of Bacteroides fragilis group isolates in Europe: 20 years of experience","volume":"17","author":"Nagy","year":"2011","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1247","DOI":"10.1128\/AAC.05823-11","article-title":"Prevalence of Antimicrobial Resistance among Clinical Isolates of Bacteroides fragilis Group in Canada in 2010\u20132011: CANWARD Surveillance Study","volume":"56","author":"Karlowsky","year":"2012","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1093\/jac\/dkt344","article-title":"Fourth Belgian multicentre survey of antibiotic susceptibility of anaerobic bacteria","volume":"69","author":"Wybo","year":"2014","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1016\/j.anaerobe.2016.07.003","article-title":"Changes in the antibiotic susceptibility of anaerobic bacteria from 2007\u20132009 to 2010\u20132012 based on the CLSI methodology","volume":"42","author":"Hastey","year":"2016","journal-title":"Anaerobe"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1452","DOI":"10.1089\/mdr.2019.0462","article-title":"Trends and Impact in Antimicrobial Resistance Among Bacteroides and Parabacteroides Species in 2007\u20132012 Compared to 2013\u20132017","volume":"26","author":"Kierzkowska","year":"2020","journal-title":"Microb. Drug Resist."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"931","DOI":"10.1016\/j.jiac.2021.03.010","article-title":"Change in antimicrobial susceptibility of pathogens isolated from surgical site infections over the past decade in Japanese nation-wide surveillance study","volume":"27","author":"Ueda","year":"2021","journal-title":"J. Infect. Chemother."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"102173","DOI":"10.1016\/j.anaerobe.2020.102173","article-title":"Surveillance of antimicrobial resistance in recent clinical isolates of Gram-negative anaerobic bacteria in a Greek University Hospital","volume":"62","author":"Maraki","year":"2020","journal-title":"Anaerobe"},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"K\u00f6nig, E., Ziegler, H.P., Tribus, J., Grisold, A.J., Feierl, G., and Leitner, E. (2021). Surveillance of Antimicrobial Susceptibility of Anaerobe Clinical Isolates in Southeast Austria: Bacteroides fragilis Group Is on the Fast Track to Resistance. Antibiotics, 10.","DOI":"10.3390\/antibiotics10050479"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"102446","DOI":"10.1016\/j.anaerobe.2021.102446","article-title":"Etiology and antimicrobial susceptibility profiles of anaerobic bacteria isolated from clinical samples in a university hospital in Madrid, Spain","volume":"72","author":"Morosini","year":"2021","journal-title":"Anaerobe"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"64","DOI":"10.1016\/j.anaerobe.2017.04.007","article-title":"Evaluation of the routine antimicrobial susceptibility testing results of clinically significant anaerobic bacteria in a Slovenian tertiary-care hospital in 2015","volume":"47","author":"Jeverica","year":"2017","journal-title":"Anaerobe"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"190","DOI":"10.3343\/alm.2019.39.2.190","article-title":"Antimicrobial Susceptibility Patterns of Anaerobic Bacterial Clinical Isolates From 2014 to 2016, Including Recently Named or Renamed Species","volume":"39","author":"Byun","year":"2019","journal-title":"Ann. Lab. Med."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"102386","DOI":"10.1016\/j.anaerobe.2021.102386","article-title":"Antimicrobial susceptibility profiles of invasive isolates of anaerobic bacteria from a large Canadian reference laboratory: 2012\u20132019","volume":"70","author":"Forbes","year":"2021","journal-title":"Anaerobe"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"837","DOI":"10.1016\/j.jiac.2019.07.018","article-title":"Antimicrobial susceptibility surveillance of obligate anaerobic bacteria in the Kinki area","volume":"25","author":"Shimura","year":"2019","journal-title":"J. Infect. Chemother."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1016\/j.anaerobe.2013.03.001","article-title":"The prevalence of antibiotic resistance genes in Bacteroides fragilis group strains isolated in different European countries","volume":"21","author":"Eitel","year":"2013","journal-title":"Anaerobe"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"4","DOI":"10.1016\/j.anaerobe.2014.05.004","article-title":"Recent evolution of antibiotic resistance in the anaerobes as compared to previous decades","volume":"31","author":"Boyanova","year":"2015","journal-title":"Anaerobe"},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Wolf, L.J., and Stingu, C.-S. (2022). Antimicrobial Susceptibility Profile of Rare Anaerobic Bacteria. Antibiotics, 12.","DOI":"10.3390\/antibiotics12010063"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"102497","DOI":"10.1016\/j.anaerobe.2021.102497","article-title":"Antimicrobial susceptibility patterns of anaerobic bacteria at an Irish University Hospital over a ten-year period (2010\u20132020)","volume":"73","author":"Ali","year":"2022","journal-title":"Anaerobe"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"120","DOI":"10.1016\/j.anaerobe.2014.05.015","article-title":"Antimicrobial susceptibility of clinical isolates of anaerobic bacteria in Ontario, 2010\u20132011","volume":"28","author":"Rawte","year":"2014","journal-title":"Anaerobe"},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Gu\u00e9rin, F., Dejoies, L., Degand, N., Guet-Revillet, H., Janvier, F., Corvec, S., Barraud, O., Guillard, T., Walewski, V., and Gallois, E. (2021). In Vitro Antimicrobial Susceptibility Profiles of Gram-Positive Anaerobic Cocci Responsible for Human Invasive Infections. Microorganisms, 9.","DOI":"10.3390\/microorganisms9081665"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1016\/j.anaerobe.2019.05.007","article-title":"Antimicrobial susceptibility and clinical findings of significant anaerobic bacteria in southern Spain","volume":"59","author":"Cobo","year":"2019","journal-title":"Anaerobe"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"102245","DOI":"10.1016\/j.anaerobe.2020.102245","article-title":"Antimicrobial susceptibility patterns of clinically significant Gram-positive anaerobic bacteria in a Greek tertiary-care hospital, 2017\u20132019","volume":"64","author":"Maraki","year":"2020","journal-title":"Anaerobe"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"221","DOI":"10.1093\/cid\/ciy057","article-title":"Eggerthella lenta Bloodstream Infections Are Associated With Increased Mortality Following Empiric Piperacillin-Tazobactam (TZP) Monotherapy: A Population-based Cohort Study","volume":"67","author":"Gillrie","year":"2018","journal-title":"Clin. Infect. Dis."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"284","DOI":"10.1016\/j.jiac.2022.11.011","article-title":"Prevalence of antimicrobial resistant genes in Bacteroides spp. isolated in Oita Prefecture, Japan","volume":"29","author":"Hashimoto","year":"2023","journal-title":"J. Infect. Chemother."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1156.e9","DOI":"10.1016\/j.cmi.2019.02.017","article-title":"Prevalence of antimicrobial resistance genes in Bacteroides spp. and Prevotella spp. Dutch clinical isolates","volume":"25","author":"Veloo","year":"2019","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"4376","DOI":"10.1128\/jb.176.14.4376-4384.1994","article-title":"Insertional activation of cepA leads to high-level beta-lactamase expression in Bacteroides fragilis clinical isolates","volume":"176","author":"Rogers","year":"1994","journal-title":"J. Bacteriol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"942","DOI":"10.1093\/jac\/dkn347","article-title":"Genetic determinants for cfxA expression in Bacteroides strains isolated from human infections","volume":"62","author":"Lorenzo","year":"2008","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"2492","DOI":"10.1093\/jac\/dkr339","article-title":"Molecular analysis of the effector mechanisms of cefoxitin resistance among Bacteroides strains","volume":"66","author":"Gonzalez","year":"2011","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"328","DOI":"10.1016\/j.jgar.2021.01.007","article-title":"Diversity of antimicrobial resistance genes in Bacteroides and Parabacteroides strains isolated in Germany","volume":"24","author":"Rong","year":"2021","journal-title":"J. Glob. Antimicrob. Resist."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1584","DOI":"10.1099\/jmm.0.031336-0","article-title":"Differentiation of division I (cfiA-negative) and division II (cfiA-positive) Bacteroides fragilis strains by matrix-assisted laser desorption\/ionization time-of-flight mass spectrometry","volume":"60","author":"Nagy","year":"2011","journal-title":"J. Med. Microbiol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"1961","DOI":"10.1128\/JCM.02321-10","article-title":"Differentiation of cfiA -Negative and cfiA -Positive Bacteroides fragilis Isolates by Matrix-Assisted Laser Desorption Ionization\u2013Time of Flight Mass Spectrometry","volume":"49","author":"Wybo","year":"2011","journal-title":"J. Clin. Microbiol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"102448","DOI":"10.1016\/j.anaerobe.2021.102448","article-title":"Rapid detection and surveillance of cfiA-positive Bacteroides fragilis using matrix-assisted laser desorption ionization time-of-flight mass spectrometry","volume":"72","author":"Kawamoto","year":"2021","journal-title":"Anaerobe"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"552","DOI":"10.1016\/j.ijantimicag.2017.05.007","article-title":"Prevalence of antimicrobial resistance and the cfiA resistance gene in Danish Bacteroides fragilis group isolates since 1973","volume":"50","author":"Sydenham","year":"2017","journal-title":"Int. J. Antimicrob. Agents"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1016\/j.anaerobe.2019.01.011","article-title":"High prevalence of division II (cfiA positive) isolates among blood stream Bacteroides fragilis in Slovenia as determined by MALDI-TOF MS","volume":"58","author":"Jeverica","year":"2019","journal-title":"Anaerobe"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"102691","DOI":"10.1016\/j.anaerobe.2022.102691","article-title":"High prevalence of cfiA positive Bacteroides fragilis isolates collected at a teaching hospital in Hohhot, China","volume":"79","author":"Wang","year":"2023","journal-title":"Anaerobe"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"e03603-21","DOI":"10.1128\/mbio.03603-21","article-title":"Comparative Genomics of Bacteroides fragilis Group Isolates Reveals Species-Dependent Resistance Mechanisms and Validates Clinical Tools for Resistance Prediction","volume":"13","author":"Wallace","year":"2022","journal-title":"mBio"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"709","DOI":"10.1080\/1040841X.2017.1303661","article-title":"The impact of insertion sequences on bacterial genome plasticity and adaptability","volume":"43","author":"Vandecraen","year":"2017","journal-title":"Crit. Rev. Microbiol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"437","DOI":"10.1093\/jac\/dkw436","article-title":"Phenotypic detection of the cfiA metallo-\u03b2-lactamase in Bacteroides fragilis with the meropenem\u2013EDTA double-ended Etest and the ROSCO KPC\/MBL Confirm Kit","volume":"72","author":"Schwensen","year":"2017","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"1553","DOI":"10.1093\/jac\/dkac088","article-title":"A novel Bacteroides metallo-\u03b2-lactamase (MBL) and its gene (crxA) in Bacteroides xylanisolvens revealed by genomic sequencing and functional analysis","volume":"77","author":"Lang","year":"2022","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"102688","DOI":"10.1016\/j.anaerobe.2022.102688","article-title":"Identification of cfxA gene variants and susceptibility patterns in \u03b2-lactamase-producing Prevotella strains","volume":"79","author":"Yokoyama","year":"2023","journal-title":"Anaerobe"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"142","DOI":"10.1590\/1678-775720150469","article-title":"Detection of cfxA2, cfxA3, and cfxA6 genes in beta-lactamase producing oral anaerobes","volume":"24","author":"Binta","year":"2016","journal-title":"J. Appl. Oral Sci."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"102240","DOI":"10.1016\/j.anaerobe.2020.102240","article-title":"Detection of beta-lactamase production in clinical Prevotella species by MALDI-TOF MS method","volume":"65","author":"Toprak","year":"2020","journal-title":"Anaerobe"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"1238","DOI":"10.1128\/AAC.45.4.1238-1243.2001","article-title":"Multicenter Survey of the Changing In Vitro Antimicrobial Susceptibilities of Clinical Isolates of Bacteroides fragilis Group, Prevotella, Fusobacterium, Porphyromonas, and Peptostreptococcus Species","volume":"45","author":"Aldridge","year":"2001","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"733","DOI":"10.1128\/JCM.38.2.733-736.2000","article-title":"Comparison of Effects of Medium Composition and Atmospheric Conditions on Detection of Bilophila wadsworthia \u03b2-Lactamase by Cefinase and Cefinase Plus Methods","volume":"38","author":"Summanen","year":"2000","journal-title":"J. Clin. Microbiol."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1093\/jac\/33.1.33","article-title":"Characterization of a \u03b2-lactamase from Clostridium clostridioforme","volume":"33","author":"Appelbaum","year":"1994","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"1270","DOI":"10.1128\/AAC.43.5.1270","article-title":"\u03b2-Lactamase Production and Antimicrobial Susceptibility of Oral Heterogeneous Fusobacterium nucleatum Populations in Young Children","volume":"43","author":"Kanervo","year":"1999","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1093\/jac\/26.1.7","article-title":"Alterations to the penicillin-binding proteins in the Bacteroides fragilis group: A mechanism for non-\u03b2-lactamase mediated cefoxitin resistance","volume":"26","author":"Wexler","year":"1990","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"S47","DOI":"10.1086\/341920","article-title":"Selection of Cefoxitin\u2014Resistant Bacteroides thetaiotaomicron Mutants and Mechanisms Involved in \u03b2\u2014Lactam Resistance","volume":"35","author":"Fang","year":"2002","journal-title":"Clin. Infect. Dis."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"1055","DOI":"10.1099\/jmm.0.45930-0","article-title":"Penicillin-binding proteins of Bacteroides fragilis and their role in the resistance to imipenem of clinical isolates","volume":"54","author":"Ayala","year":"2005","journal-title":"J. Med. Microbiol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"78","DOI":"10.1016\/j.anaerobe.2017.02.004","article-title":"Exposure to \u03b2-lactams results in the alteration of penicillin-binding proteins in Clostridium perfringens","volume":"45","author":"Park","year":"2017","journal-title":"Anaerobe"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"102179","DOI":"10.1016\/j.anaerobe.2020.102179","article-title":"\u03b2-Lactam resistance development affects binding of penicillin-binding proteins (PBPs) of Clostridium perfringens to the fluorescent penicillin, BOCILLIN FL","volume":"62","author":"Park","year":"2020","journal-title":"Anaerobe"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"120","DOI":"10.1093\/jac\/dkg297","article-title":"Penicillin-binding proteins involved in high-level piperacillin resistance in Veillonella spp.","volume":"52","author":"Theron","year":"2003","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1093\/jac\/dkl202","article-title":"Bacteroides fragilis BmeABC efflux systems additively confer intrinsic antimicrobial resistance","volume":"58","author":"Pumbwe","year":"2006","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"135","DOI":"10.1016\/j.ijantimicag.2004.01.008","article-title":"A Bacteroides thetaiotamicron porin that could take part in resistance to \u03b2-lactams","volume":"24","author":"Calvet","year":"2004","journal-title":"Int. J. Antimicrob. Agents"},{"key":"ref_64","doi-asserted-by":"crossref","unstructured":"Mayers, D.L. (2009). Antimicrobial Drug Resistance, Humana Press.","DOI":"10.1007\/978-1-59745-180-2"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1093\/jac\/dkx351","article-title":"Metronidazole: An update on metabolism, structure\u2013cytotoxicity and resistance mechanisms","volume":"73","author":"Dingsdag","year":"2018","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"214","DOI":"10.1016\/S0140-6736(78)90655-4","article-title":"Bacteroides fragilis resistant to metronidazole after long-term therapy","volume":"311","author":"Ingham","year":"1978","journal-title":"Lancet"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"40","DOI":"10.1016\/j.anaerobe.2018.10.004","article-title":"Metronidazole resistance and nim genes in anaerobes: A review","volume":"55","author":"Alauzet","year":"2019","journal-title":"Anaerobe"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"102715","DOI":"10.1016\/j.anaerobe.2023.102715","article-title":"Antimicrobial susceptibility of anaerobic clinical isolates: A two-year surveillance","volume":"80","author":"Casarotto","year":"2023","journal-title":"Anaerobe"},{"key":"ref_69","first-page":"e01125-19","article-title":"Draft Genome Sequence of a Metronidazole-Resistant Bacteroides fragilis Strain Isolated in Ecuador","volume":"8","author":"Zurita","year":"2019","journal-title":"Genome Announc."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"1253","DOI":"10.1128\/AAC.49.3.1253-1256.2005","article-title":"Inducible Metronidazole Resistance and nim Genes in Clinical Bacteroides fragilis Group Isolates","volume":"49","author":"Fang","year":"2005","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"dlab044","DOI":"10.1093\/jacamr\/dlab044","article-title":"Phenotypic and genotypic antimicrobial resistance in clinical anaerobic isolates from India","volume":"3","author":"Sood","year":"2021","journal-title":"JAC-Antimicrobial Resist."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"60","DOI":"10.1128\/AAC.01003-09","article-title":"Metronidazole Resistance in Prevotella spp. and Description of a New nim Gene in Prevotella baroniae","volume":"54","author":"Alauzet","year":"2010","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"705","DOI":"10.1093\/jac\/dkl285","article-title":"Dissemination of nim-class genes, encoding nitroimidazole resistance, among different species of Gram-negative anaerobic bacteria isolated in Athens, Greece","volume":"58","author":"Katsandri","year":"2006","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"3207","DOI":"10.1128\/AAC.48.8.3207-3208.2004","article-title":"nimE Gene in a Metronidazole-Susceptible Veillonella sp. Strain","volume":"48","author":"Marchandin","year":"2004","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"240","DOI":"10.1093\/jac\/dkh270","article-title":"Nitroimidazole resistance genes (nimB) in anaerobic Gram-positive cocci (previously Peptostreptococcus spp.)","volume":"54","author":"Theron","year":"2004","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1093\/jac\/dkh296","article-title":"Metronidazole resistance in Bacteroides spp. carrying nim genes and the selection of slow-growing metronidazole-resistant mutants","volume":"54","author":"Gal","year":"2004","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"3767","DOI":"10.1128\/AAC.00386-13","article-title":"Two Multidrug-Resistant Clinical Isolates of Bacteroides fragilis Carry a Novel Metronidazole Resistance nim Gene (nimJ)","volume":"57","author":"Husain","year":"2013","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1016\/j.jgar.2016.01.009","article-title":"Lactate dehydrogenase activity in Bacteroides fragilis group strains with induced resistance to metronidazole","volume":"5","author":"Stanko","year":"2016","journal-title":"J. Glob. Antimicrob. Resist."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"267","DOI":"10.1093\/jac\/dkp203","article-title":"Overexpression of the rhamnose catabolism regulatory protein, RhaR: A novel mechanism for metronidazole resistance in Bacteroides thetaiotaomicron","volume":"64","author":"Patel","year":"2009","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"2634","DOI":"10.1093\/jac\/dku219","article-title":"Deficiency of the ferrous iron transporter FeoAB is linked with metronidazole resistance in Bacteroides fragilis","volume":"69","author":"Veeranagouda","year":"2014","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"898453","DOI":"10.3389\/fmicb.2022.898453","article-title":"Modulation of Iron Import and Metronidazole Resistance in Bacteroides fragilis Harboring a nimA Gene","volume":"13","author":"Paunkov","year":"2022","journal-title":"Front. Microbiol."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"346","DOI":"10.1016\/j.resmic.2010.04.003","article-title":"Bacteroides fragilis RecA protein overexpression causes resistance to metronidazole","volume":"161","author":"Steffens","year":"2010","journal-title":"Res. Microbiol."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"S26","DOI":"10.1086\/647940","article-title":"Lessons Learned from the Anaerobe Survey: Historical Perspective and Review of the Most Recent Data (2005\u20132007)","volume":"50","author":"Snydman","year":"2010","journal-title":"Clin. Infect. Dis."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"228","DOI":"10.1080\/17843286.1989.11718022","article-title":"In Vitro Activity of Amoxycillin Plus Clavulanic Acid And Ticarcillin Plus Clavulanic Acid Compared With That Of Other Antibiotics Against Anaerobic Bacteria","volume":"44","author":"Rosseel","year":"1989","journal-title":"Acta Clin. Belg."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"102207","DOI":"10.1016\/j.anaerobe.2020.102207","article-title":"Epidemiology and microbiological features of anaerobic bacteremia in two French University hospitals","volume":"64","author":"Dumont","year":"2020","journal-title":"Anaerobe"},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"102583","DOI":"10.1016\/j.anaerobe.2022.102583","article-title":"Anaerobic bloodstream infections in Italy (ITANAEROBY): A 5-year retrospective nationwide survey","volume":"75","author":"Antonello","year":"2022","journal-title":"Anaerobe"},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"102111","DOI":"10.1016\/j.anaerobe.2019.102111","article-title":"Antimicrobial susceptibility profiles of anaerobic bacteria, isolated from human clinical specimens, within different European and surrounding countries. A joint ESGAI study","volume":"61","author":"Veloo","year":"2020","journal-title":"Anaerobe"},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"226","DOI":"10.1016\/j.anaerobe.2017.06.004","article-title":"erm gene distribution among Norwegian Bacteroides isolates and evaluation of phenotypic tests to detect inducible clindamycin resistance in Bacteroides species","volume":"47","author":"Johnsen","year":"2017","journal-title":"Anaerobe"},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"78","DOI":"10.1016\/j.anaerobe.2018.04.009","article-title":"In vitro activity of tigecycline and comparators against a European collection of anaerobes collected as part of the Tigecycline Evaluation and Surveillance Trial (T.E.S.T.) 2010\u20132016","volume":"51","author":"Rodloff","year":"2018","journal-title":"Anaerobe"},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"198","DOI":"10.1016\/j.jiac.2022.10.018","article-title":"Prevalence of antimicrobial-resistant Cutibacterium isolates and development of multiplex PCR method for Cutibacterium species identification","volume":"29","author":"Koizumi","year":"2023","journal-title":"J. Infect. Chemother."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"1357","DOI":"10.1007\/s10096-020-03852-5","article-title":"Propionibacterium\/Cutibacterium species\u2013related positive samples, identification, clinical and resistance features: A 10-year survey in a French hospital","volume":"39","author":"Broly","year":"2020","journal-title":"Eur. J. Clin. Microbiol. Infect. Dis."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"422","DOI":"10.1093\/jac\/dkv347","article-title":"Resistance patterns in clinical isolates of pathogenic Actinomyces species","volume":"71","author":"Steininger","year":"2016","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"3559","DOI":"10.1128\/JB.182.12.3559-3571.2000","article-title":"Characterization of a Bacteroides Mobilizable Transposon, NBU2, Which Carries a Functional Lincomycin Resistance Gene","volume":"182","author":"Wang","year":"2000","journal-title":"J. Bacteriol."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1016\/j.anaerobe.2005.01.005","article-title":"Genetic basis of resistance in Propionibacterium acnes strains isolated from diverse types of infection in different European countries","volume":"11","author":"Oprica","year":"2005","journal-title":"Anaerobe"},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"102220","DOI":"10.1016\/j.anaerobe.2020.102220","article-title":"Molecular basis of macrolide-lincosamide-streptogramin (MLS) resistance in Finegoldia magna clinical isolates","volume":"64","author":"Lachaal","year":"2020","journal-title":"Anaerobe"},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"630","DOI":"10.1128\/AAC.45.2.630-632.2001","article-title":"Macrolide Resistance in Peptostreptococcus spp. Mediated by ermTR: Possible Source of Macrolide-Lincosamide-Streptogramin B Resistance in Streptococcus pyogenes","volume":"45","author":"Reig","year":"2001","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"70","DOI":"10.1080\/17843286.1996.11718489","article-title":"In Vitro Activity of Amoxycillin\/Clavulanate and Ticarcillin\/Clavulanate Compared with That of Other Antibiotics Against Anaerobic Bacteria: Comparison with the Results of the 1987 Survey","volume":"51","author":"Rosseel","year":"1996","journal-title":"Acta Clin. Belg."},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"102471","DOI":"10.1016\/j.anaerobe.2021.102471","article-title":"Different breakpoints interpretation yielded distinct resistance rates to moxifloxacin of clinically significant anaerobic bacteria","volume":"72","author":"Cobo","year":"2021","journal-title":"Anaerobe"},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1080\/1120009X.2022.2106637","article-title":"Time to reconsider moxifloxacin anti-anaerobic activity?","volume":"34","author":"Principe","year":"2022","journal-title":"J. Chemother."},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"1598","DOI":"10.1086\/503907","article-title":"Fluoroquinolones and Anaerobes","volume":"42","author":"Stein","year":"2006","journal-title":"Clin. Infect. Dis."},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"593","DOI":"10.1128\/CMR.00008-07","article-title":"Bacteroides: The Good, the Bad, and the Nitty-Gritty","volume":"20","author":"Wexler","year":"2007","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"526","DOI":"10.1128\/CMR.00086-12","article-title":"Antianaerobic Antimicrobials: Spectrum and Susceptibility Testing","volume":"26","author":"Brook","year":"2013","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_103","doi-asserted-by":"crossref","first-page":"284","DOI":"10.1542\/pir.25-8-284","article-title":"Chloramphenicol: A Review","volume":"25","author":"Balbi","year":"2004","journal-title":"Pediatr. Rev."},{"key":"ref_104","doi-asserted-by":"crossref","first-page":"334","DOI":"10.1097\/00006254-197805000-00009","article-title":"Apparent failure of chloramphenicol in the treatment of anaerobic infections","volume":"33","author":"Thadepalli","year":"1978","journal-title":"Obstet Gynecol. Surv."},{"key":"ref_105","doi-asserted-by":"crossref","first-page":"736","DOI":"10.1128\/AAC.10.4.736","article-title":"Susceptibility of Anaerobic Bacteria to 23 Antimicrobial Agents","volume":"10","author":"Sutter","year":"1976","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_106","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1179\/1973947815Y.0000000068","article-title":"Antimicrobials therapy of anaerobic infections","volume":"28","author":"Brook","year":"2016","journal-title":"J. Chemother."},{"key":"ref_107","doi-asserted-by":"crossref","first-page":"327","DOI":"10.1902\/jop.2013.130081","article-title":"Antimicrobial Resistance and Prevalence of Resistance Genes of Obligate Anaerobes Isolated from Periodontal Abscesses","volume":"85","author":"Xie","year":"2014","journal-title":"J. Periodontol."},{"key":"ref_108","doi-asserted-by":"crossref","first-page":"1662","DOI":"10.1111\/j.1742-1241.2006.01188.x","article-title":"Tigecycline: A new glycylcycline antimicrobial","volume":"60","author":"Townsend","year":"2006","journal-title":"Int. J. Clin. Pract."},{"key":"ref_109","doi-asserted-by":"crossref","first-page":"S354","DOI":"10.1086\/431676","article-title":"The Efficacy and Safety of Tigecycline for the Treatment of Complicated Intra-Abdominal Infections: Analysis of Pooled Clinical Trial Data","volume":"41","author":"Babinchak","year":"2005","journal-title":"Clin. Infect. Dis."},{"key":"ref_110","doi-asserted-by":"crossref","first-page":"S341","DOI":"10.1086\/431675","article-title":"The Efficacy and Safety of Tigecycline in the Treatment of Skin and Skin\u2014Structure Infections: Results of 2 Double\u2014Blind Phase 3 Comparison Studies with Vancomycin\u2014Aztreonam","volume":"41","author":"Grosse","year":"2005","journal-title":"Clin. Infect. Dis."},{"key":"ref_111","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1128\/AAC.40.1.1","article-title":"Tetracycline resistance mediated by ribosomal protection","volume":"40","author":"Taylor","year":"1996","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_112","doi-asserted-by":"crossref","first-page":"1218","DOI":"10.1093\/nar\/16.3.1218","article-title":"Homology of the TetM with translational elongation factors: Implications for potential modes of tetM conferred tetracycline resistance","volume":"16","author":"Brown","year":"1988","journal-title":"Nucleic Acids Res."},{"key":"ref_113","doi-asserted-by":"crossref","first-page":"102717","DOI":"10.1016\/j.anaerobe.2023.102717","article-title":"First large-scale study of antimicrobial susceptibility data, and genetic resistance determinants, in Fusobacterium necrophorum highlighting the importance of continuing focused susceptibility trend surveillance","volume":"80","author":"Perry","year":"2023","journal-title":"Anaerobe"},{"key":"ref_114","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1016\/S1075-9964(03)00058-1","article-title":"Acquired tetracycline and\/or macrolide\u2013lincosamides\u2013streptogramin resistance in anaerobes","volume":"9","author":"Roberts","year":"2003","journal-title":"Anaerobe"},{"key":"ref_115","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1016\/j.anaerobe.2005.10.004","article-title":"Anaerobes: Antibiotic resistance, clinical significance, and the role of susceptibility testing","volume":"12","author":"Hecht","year":"2006","journal-title":"Anaerobe"},{"key":"ref_116","doi-asserted-by":"crossref","first-page":"522","DOI":"10.1016\/j.ijantimicag.2011.07.010","article-title":"Investigation of the prevalence of tetQ, tetX and tetX1 genes in Bacteroides strains with elevated tigecycline minimum inhibitory concentrations","volume":"38","author":"Bartha","year":"2011","journal-title":"Int. J. Antimicrob. Agents"},{"key":"ref_117","doi-asserted-by":"crossref","first-page":"839","DOI":"10.1128\/AAC.40.4.839","article-title":"In vitro activities of U-100592 and U-100766, novel oxazolidinone antibacterial agents","volume":"40","author":"Zurenko","year":"1996","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_118","doi-asserted-by":"crossref","first-page":"815","DOI":"10.2165\/00003495-200059040-00007","article-title":"Linezolid","volume":"59","author":"Clemett","year":"2000","journal-title":"Drugs"},{"key":"ref_119","doi-asserted-by":"crossref","first-page":"e01088-20","DOI":"10.1128\/AAC.01088-20","article-title":"In Vitro Activity of Tedizolid Compared to Linezolid and Five Other Antimicrobial Agents against 332 Anaerobic Isolates, Including Bacteroides fragilis Group, Prevotella, Porphyromonas, and Veillonella Species","volume":"64","author":"Goldstein","year":"2020","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_120","doi-asserted-by":"crossref","first-page":"e67","DOI":"10.1086\/428623","article-title":"Anaerobic Sepsis Due to Multidrug\u2014Resistant Bacteroides fragilis: Microbiological Cure and Clinical Response with Linezolid Therapy","volume":"40","author":"Wareham","year":"2005","journal-title":"Clin. Infect. Dis."},{"key":"ref_121","doi-asserted-by":"crossref","first-page":"496","DOI":"10.1016\/j.ijantimicag.2017.03.013","article-title":"A cfr- like gene cfr (C) conferring linezolid resistance is common in Clostridium difficile","volume":"50","author":"Candela","year":"2017","journal-title":"Int. J. Antimicrob. Agents"},{"key":"ref_122","doi-asserted-by":"crossref","first-page":"151559","DOI":"10.1016\/j.ijmm.2022.151559","article-title":"Comprehensive investigation of antibiotic resistance gene content in cfiA-harboring Bacteroides fragilis isolates of human and animal origins by whole genome sequencing","volume":"312","author":"Cao","year":"2022","journal-title":"Int. J. Med. Microbiol."},{"key":"ref_123","doi-asserted-by":"crossref","first-page":"3310","DOI":"10.1093\/jac\/dkab339","article-title":"Multiresistance gene cfr(C) in Clostridium perfringens of cattle origin from China","volume":"76","author":"Zhang","year":"2021","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_124","doi-asserted-by":"crossref","first-page":"102666","DOI":"10.1016\/j.anaerobe.2022.102666","article-title":"Epidemiology and antibiotic susceptibility profiles of obligate anaerobes in a hospital of central Italy during a one-year (2019) survey","volume":"78","author":"Parisio","year":"2022","journal-title":"Anaerobe"},{"key":"ref_125","doi-asserted-by":"crossref","first-page":"65","DOI":"10.1016\/j.jgar.2017.10.020","article-title":"Molecular characterisation of multidrug-resistant Bacteroides isolates from Hungarian clinical samples","volume":"13","author":"Soki","year":"2018","journal-title":"J. Glob. Antimicrob. Resist."},{"key":"ref_126","doi-asserted-by":"crossref","first-page":"36","DOI":"10.1016\/j.anaerobe.2017.01.010","article-title":"Fatal sepsis caused by multidrug-resistant Bacteroides fragilis, harboring a cfiA gene and an upstream insertion sequence element, in Japan","volume":"44","author":"Nakamura","year":"2017","journal-title":"Anaerobe"},{"key":"ref_127","doi-asserted-by":"crossref","first-page":"379","DOI":"10.3390\/antibiotics4030379","article-title":"Multidrug Efflux Systems in Microaerobic and Anaerobic Bacteria","volume":"4","author":"Xu","year":"2015","journal-title":"Antibiotics"}],"container-title":["Microorganisms"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2607\/11\/6\/1474\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T19:46:46Z","timestamp":1760125606000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2607\/11\/6\/1474"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,6,1]]},"references-count":127,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2023,6]]}},"alternative-id":["microorganisms11061474"],"URL":"https:\/\/doi.org\/10.3390\/microorganisms11061474","relation":{},"ISSN":["2076-2607"],"issn-type":[{"value":"2076-2607","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,6,1]]}}}