Fifty years devoted to anaerobes: historical, lessons, and highlights.

Luc J Dubreuil
Author Information
  1. Luc J Dubreuil: Clinical Microbiology Department, Faculty of Pharmacy, University of Lille, Lille, France. lucdubreuil4@gmail.com. ORCID

Abstract

Renew interest and enthusiasm for anaerobes stem from both technological improvements (culture media, production of an adequate anaerobic atmosphere, identification methods) and greater awareness on the part of clinicians. Anaerobic infections were historically treated empirically, targeting the species known to be involved in each type of infection. Prevotella, fusobacteria, and Gram-positive cocci (GPAC) were considered responsible for infections above the diaphragm whereas for intra-abdominal infections, Bacteroides of the fragilis group (BFG), GPAC and clostridia were predominantly implicated. The antibiotic susceptibility of anaerobes was only taken into consideration by the clinician in the event of treatment failure or when faced with infections by multidrug-resistant bacteria (MDR). The evolution of antibiotic resistance together with clinical failures due to the absence of detection of hetero-resistant clones has resulted in a greater need for accessible antibiotic susceptibility testing (AST) and disc diffusion method. Improved isolation and identification of anaerobes, along with the availability of accessible and robust methods for performing AST, will ensure that treatment, whether empirical or guided by an antibiogram, will lead to better outcomes for anaerobic infections.

Keywords

References

  1. Wilson SE, Judith A, Hopkins F (1995) Clinical correlates of anaerobic bacteriology in peritonitis. Clin Infect Dis 20(Suppl 2):S251–S256. https://doi.org/10.1093/clinids/20.supplement_2.s251 [DOI: 10.1093/clinids/20.supplement_2.s251]
  2. McNamara MJ, Pasquale MD, Evans SR (1993) Acute appendicitis and the use of intraperitoneal cultures. Surg Gynecol Obstet 177(393):7
  3. Mosdell DM, Morris DM, Voltura A, Pitcher DE, Twiest MW, Milne RL, Miscall BG, Fry DE (1991) Antibiotic treatment for surgical peritonitis. Ann Surg 214:543–549. https://doi.org/10.1097/00000658-199111000-00001 [DOI: 10.1097/00000658-199111000-00001]
  4. Dougherty SH, Saltzstein EC, Peacock JB, Mercer LC, Cano P (1989) Perforated or gangrenous appendicitis treated with aminoglycosides: how do bacterial cultures influence management? Arch Surg 124:1280–1283. https://doi.org/10.1001/archsurg.1989.01410110034006 [DOI: 10.1001/archsurg.1989.01410110034006]
  5. Chow AW, Guze LB (1974) Bacteroidaceae bacteremia: clinical experience with 112 patients. Medicine (Baltimore) 53:93–126 [DOI: 10.1097/00005792-197403000-00001]
  6. Hopkins JA, Lee JCH (1993) Susceptibility of intra-abdominal isolates at operation. A predictor of postoperative infection. Ann Surg 59:791–6
  7. Koperna T, Schulz F (1996) Prognosis and treatment of peritonitis. Do we need new scoring systems? Arch Surg 131:180–6. https://doi.org/10.1001/archsurg.1996.01430140070019 [DOI: 10.1001/archsurg.1996.01430140070019]
  8. Rosenblatt JE, Brook I (1993) Clinical relevance of susceptibility testing of anaerobic bacteria. Clin Infect Dis 16(suppl 4):S446–S448. https://doi.org/10.1093/clinids/16.supplement4.s446 [DOI: 10.1093/clinids/16.supplement4.s446]
  9. Snydman DR, Cuchural GJ Jr, McDermott L, Gill M (1992) Correlation of various in vitro testing methods with clinical outcomes in patients with Bacteroides fragilis group infections treated with cefoxitin: a retrospective analysis. Antimicrob Agents Chemother 36:540–544. https://doi.org/10.1128/AAC.36.3.540 [DOI: 10.1128/AAC.36.3.540]
  10. Salonen JH, Eerola E, Meurman O (1998) Clinical significance and outcome of anaerobic bacteremia. Clin Infect Dis 26:1413–1417. https://doi.org/10.1086/516355 [DOI: 10.1086/516355]
  11. Finegold SM, George WL. Milligan ME (1986) A disease-a-month classic. Anaerobic infections. Year book medical publishers, INC Chicago, London
  12. Brook I (1988) Recovery of anaerobic bacteria from clinical specimen in 12 years at two military hospitals. J Clin Microbiol 26:1181–1188. https://doi.org/10.1128/jcm.26.6.1181-1188.1988 [DOI: 10.1128/jcm.26.6.1181-1188.1988]
  13. Brook I (1988) Pediatric anaerobic infection. Diagnostics and management, 2nd edn. Mosby Company, St Louis Missouri
  14. Duerden BI, Drasar BS (1991) Anaerobes in human disease. Arnold, London
  15. Di Bella S, Antonello RM, Sanson G, Maraolo AE, Giacobbe DR et al (2022) Anaerobic bloodstream infections in Italy (ITANAEROBY): a 5-year retrospective nationwide survey. Anaerobe 75:102583. https://doi.org/10.1016/j.anaerobe.2022.102583 [DOI: 10.1016/j.anaerobe.2022.102583]
  16. Engelkirk PG, Duben-Engelkirk J, Dowell VR (1992) Principles and practice of clinical anaerobic bacteriology. Star publishing Co, Belmont
  17. Jousimies-Somer H, Summanen P, Citron DM, Baron JE, Wexler HM, Finegold SM (2002) Wadsworth-KTL anaerobic bacteriology manual, 6th edn. Star Publishing Company, Belmont
  18. Sedallian A, Dubreuil L, Riegel P (2019) Généralités sur les bactéries anaérobies. In: Freney J, Riegel P (eds) Bactériologie clinique 3 editions. ESKA, Paris, pp 1338–57
  19. Nagy E, Boyanova L, Justesen US, on behalf of ESCMID Study Group of Anaerobic Infections (2018) How to isolate, identify and determine antimicrobial susceptibility of anaerobic bacteria in routine laboratories. Clin Microbiol Infect 24:1139–1148. https://doi.org/10.1016/j.cmi.2018.02.008 [DOI: 10.1016/j.cmi.2018.02.008]
  20. Montravers P, Lepape A, Dubreuil L, Gauzit R, Pean Y, Benchimol D, Dupont H (2009) Clinical and microbiological profiles of community-acquired and nosocomial intra-abdominal infections: results of the French prospective, observational EBIIA study. J Antimicrob Chemother 63:785–794. https://doi.org/10.1093/jac/dkp005 [DOI: 10.1093/jac/dkp005]
  21. Baron EJ, Strong CA, Mc Teague M, Vaisanen ML, Finegold SM (1995) Survival of anaerobic bacteria in original specimens transported by overnight services. Clin Infect Dis 20(Suppl 2):S174–S177. https://doi.org/10.1093/clinids/20.Supplement_2.S174 [DOI: 10.1093/clinids/20.Supplement_2.S174]
  22. Senneville E, Savage C, Nallet I, Yazdanpanah Y, Giraud F, Migaud H, Dubreuil L, Courcol R, Mouton Y (2006) Improved aero-anaerobe recovery from infected prosthetic joint samples taken from 72 patients and collected intraoperatively in Rosenow’s broth. Acta Orthop 77:120–124. https://doi.org/10.1080/17453670610045795 [DOI: 10.1080/17453670610045795]
  23. Rosenow EC (1914) The newer bacteriology of various infections as determined by special methods. J Am Med Ass 63:903–908 [DOI: 10.1001/jama.1914.02570110005002]
  24. Justesen US, Skov MN, Knudsen E, Holt HM, Sogaard P, Justesen T (2010) 16S rRNA gene sequencing in routine identification of anaerobic bacteria isolated from blood cultures. J Clin Microbiol 48:946–948. https://doi.org/10.1128/JCM.02075-09 [DOI: 10.1128/JCM.02075-09]
  25. Justesen US, Holm A, Knudsen E, Andersen LB, Jensen TG, Kemp M (2011) Species identification of clinical isolates of anaerobic bacteria: comparison of two matrix-assisted laser desorption ionization-time of flight mass spectrometry systems. J Clin Microbiol 49:4314–4318. https://doi.org/10.1128/JCM.05788-11 [DOI: 10.1128/JCM.05788-11]
  26. Nagy E, Becker S, Kostrewa M, Barta N, Urban E (2012) The value of MALDI-TOF MS for the identification of clinically relevant anaerobic bacteria in routine laboratories. J Med Microbiol 61:1393–1400. https://doi.org/10.1099/jmm.0.043927-0 [DOI: 10.1099/jmm.0.043927-0]
  27. Medceky M, Cejkova D, Polansky O, Karasova D, Kubosava T, Ciizek A, Rychlik I (2018) Whole genome sequencing and function prediction of 133 gut anaerobes isolated from chicken caecum in pure cultures. BMC Genomics 31:561. https://doi.org/10.1186/s12864-018-4959-4 [DOI: 10.1186/s12864-018-4959-4]
  28. Dubreuil L (2010) Methods for antimicrobial susceptibility testing of anaerobic bacteria. Méthodes d’étude des anaérobies. In: Courvalin P, Leclercq R, Rice LB (eds) Antibiogramme. Eska, Paris, pp 553–67
  29. Finegold SM (1992) Clinical relevance of antimicrobial susceptibility testing. Eur J Clin Microbiol Infect Dis 1002:1021–1024. https://doi.org/10.1007/BF01967793 [DOI: 10.1007/BF01967793]
  30. Brook I, Wexler HM, Goldstein EJC (2013) Antianaerobic antimicrobials: spectrum and susceptibility testing. Clin Microbiol Rev 26:526–546. https://doi.org/10.1128/CMR.00086-12 [DOI: 10.1128/CMR.00086-12]
  31. Bourgault AM, Harkness JL, Rosenblatt JE (1978) Clinical usefulness of susceptibility testing of anaerobes. Arch Intern Med 138(1825):7. https://doi.org/10.1001/archinte.1978.03630370039019 [DOI: 10.1001/archinte.1978.03630370039019]
  32. Clinical and Laboratory Standards Institute (2012) Methods for anti-microbial susceptibility testing of anaerobic bacteria. Approved standard, 8th ed. CLSI document M11-A8. Clinical and Laboratory Standards Institute, Wayne, PA.
  33. Hecht DW, Lederer L, Osmolski JR (1995) Susceptibility results for the Bacteroides fragilis group: comparison of the broth microdilution and agar dilution methods. Clin Infect Diseases 20(Suppl 2):S342. https://doi.org/10.1093/clinids/20.supplement_2.s342 [DOI: 10.1093/clinids/20.supplement_2.s342]
  34. Baron EJ, David AB (1984) Comparison of susceptibilities of anaerobic bacteria determined by agar dilution and by a microbroth. Method Rev infect Dis 6(suppl1):S249–S253. https://doi.org/10.1093/clinids/6.supplement1.s249 [DOI: 10.1093/clinids/6.supplement1.s249]
  35. Hughes C, Ashhurst-Smith C, Ferguson JK (2018) Gram negative anaerobe susceptibility testing in clinical isolates using Sensititre and Etest methods. Pathology 9:437–41. https://doi.org/10.1016/j.pathol.2017.10.020 [DOI: 10.1016/j.pathol.2017.10.020]
  36. Cherkaoui A, Fischer A, Azam N, Riat A, Schrenzel J (2018) A comparison of sensititre TM Anaerobe MIC plate with ATB ANA® test for the routine susceptibility testing of common anaerobe pathogens. Eur J Clin Microbiol Infect Dis 37:2279–2284. https://doi.org/10.1007/s10096-018-3369-5 [DOI: 10.1007/s10096-018-3369-5]
  37. Cordovana M, Ambretti S (2020) Antibiotic susceptibility testing of anaerobic bacteria by broth microdilution method using the MICRONAUT-S anaerobes MIC plates. Anaerobe 63:102217. https://doi.org/10.1016/j.anaerobe.2020.102217 [DOI: 10.1016/j.anaerobe.2020.102217]
  38. Koru O, Ozyurt M (2008) Determination of antimicrobial susceptibilities of clinically isolated anaerobic bacteria by E-test ATB-ANA and agar dilution. Anaerobe 14:161–165. https://doi.org/10.1016/j.anaerobe.2008.02.004 [DOI: 10.1016/j.anaerobe.2008.02.004]
  39. FDA-Antimicrobial Susceptibility Test (AST) Systems—Class ii Special Controls Guidance for Industry and FDA (2018) FDA. Available online: https://www.fda.gov/medical-devices/guidance-documents-medical-devices-and-radiation-emitting-products/antimicrobial-susceptibility-test-ast-systems-class-ii-special-controls-guidance-industry-and-fda
  40. Lee K, Yunseop J, Kwon O, Jang In I, Song W, Yoon G (1992) Evaluation of A commercial microdilution (ATB ANA) system for susceptibility testing of anaerobic bacteria. Korean J Clin Pathol 1992; 12: 341–6. Reported in English In: Ann Lab Med 12: 341–346
  41. Dubreuil L, Houcke I, Singer E (1999) Susceptibility Testing of anaerobic bacteria: evaluation of the redesigned (version 96) bioMerieux ATB ANA device. J Clin Microbiol 37:1824–1828. https://doi.org/10.1128/JCM.37.6.1824-1828.1999 [DOI: 10.1128/JCM.37.6.1824-1828.1999]
  42. Citron DM, Ostavari MI, Karlsson A, Goldstein EJ (1991) Evaluation of the E test for susceptibility testing of anaerobic bacteria. J Clin Microbiol 29:2197–2203. https://doi.org/10.1128/jcm.29.10.2197-2203.1991 [DOI: 10.1128/jcm.29.10.2197-2203.1991]
  43. Baquer F, Sawan AA, Auzou M, Grillon A, Jaulhac B, Join-Lambert O, Boyer PH (2021) Broth microdilution and gradient diffusion strips vs. reference agar dilution method: first evaluation for clostridiales species antimicrobial susceptibility testing antibiotics. Antibiotics (Basel) 10:975. https://doi.org/10.3390/antibiotics10080975 [DOI: 10.3390/antibiotics10080975]
  44. Rennie RP, Turnbulla L, Brosnikoffa C, Cloke J (2012) First comprehensive evaluation of the MIC evaluator device compared to e test and CLSI reference dilution methods for antimicrobial susceptibility testing of clinical strains of anaerobes and other fastidious bacterial species. J Clin Microbiol 50:1153–1157. https://doi.org/10.1128/JCM.05397-11 [DOI: 10.1128/JCM.05397-11]
  45. Rentenaar RJ, Bovo-Heijmans B, Diggle J, Fluit C, Wootton M (2021) False amoxicillin/clavulanic acid susceptibility in Bacteroides fragilis using gradient strip tests. Anaerobe 69:102358. https://doi.org/10.1016/j.anaerobe.2014.10.008 [DOI: 10.1016/j.anaerobe.2014.10.008]
  46. Palmer J, Chen S, Gottlieb T, Schiog F, Gilbert G (1994) False resistance to metronidazole of anaerobic bacteria using the E test. J Antimicrob Chemother 34:598–600. https://doi.org/10.1093/jac/34.4.598 [DOI: 10.1093/jac/34.4.598]
  47. Wilkins TD, Holdeman LV, Abramson IJ (1972) Standardized single disk method for antibiotic susceptibility testing of anaerobic bacteria. Antimicrob Agents Chemother 1:451–459. https://doi.org/10.1128/AAC.1.6.451 [DOI: 10.1128/AAC.1.6.451]
  48. Horn R, Bourgault AM, Lamothe F (1987) Disk diffusion susceptibility testing of the Bacteroides fragilis group. Antimicrob Agents Chemother 31:1596–1599. https://doi.org/10.1128/AAC.31.10.1596 [DOI: 10.1128/AAC.31.10.1596]
  49. Barry AL, Fuchs PC, Gerlach EH, Allen SD, Acar JF, Aldridge KE, Bourgault AM et al (1990) Multilaboratory evaluation of an agar diffusion disk susceptibility test for rapidly growing anaerobic bacteria. Rev Infect Dis 12(suppl2):S210-217. https://doi.org/10.1093/clinids/12.Supplement_2.S210.S210-217 [DOI: 10.1093/clinids/12.Supplement_2.S210.S210-217]
  50. Nagy E, Justesen US, Eitel Z, Urbán E, ESCMID study group on anaerobic infection (2015) Development of EUCAST disk diffusion method for susceptibility testing of the Bacteroides fragilis group isolates. Anaerobe 31:65–71. https://doi.org/10.1093/jac/dkw436 [DOI: 10.1093/jac/dkw436]
  51. Finegold SM (1990) Anaerobes: problems and controversies in bacteriology, infections, and susceptibility testing. Rev Infect Dis 12(suppl2):S223–S230. https://doi.org/10.1093/clinids/12.Supplement_2.S223 [DOI: 10.1093/clinids/12.Supplement_2.S223]
  52. Anaerobic bacteria Calibration of zone diameter breakpoints to MIC values Version 3.0 August 2023 http://www.eucast.org/
  53. CA-SFM (2011) Comité de l’antibiogramme. Recommandations, Société Française de microbiologie, https://www.sfm-microbiologie.org/
  54. Dubreuil L, on behalf the Members of the CA-SFM 2019 (2020) Improvement of a disk diffusion method for antibiotic susceptibility testing of anaerobic bacteria. French recommendations revisited for 2020. Anaerobe 64:102213. https://doi.org/10.1016/j.anaerobe.2020.102213 [DOI: 10.1016/j.anaerobe.2020.102213]
  55. Phillips I, King A, Nord CE, Hoffstedt B (1992) Antibiotic sensitivity of Bacteroides fragilis group in Europe. Eur J Clin Microbiol Infect Dis 11:292–304. https://doi.org/10.1007/BF01962068 [DOI: 10.1007/BF01962068]
  56. Hedberg M, Nord CE (2003) Antimicrobial susceptibilities of Bacteroides fragilis groupisolates in Europe. Clin Microbiol Infect 9:475–488. https://doi.org/10.1046/j.1469-0691.2003.00674.x [DOI: 10.1046/j.1469-0691.2003.00674.x]
  57. Nagy E, Urban E, Nord CE, on behalf of the ESCMID study group on antimicrobial resistance in anaerobic bacteria (2011) Antimicrobial susceptibility of Bacteroides fragilis group isolates in Europe: 20 years of experience. Clin Microbiol Infect 17:371–9. https://doi.org/10.1111/j.1469-0691.2010.03256.x [DOI: 10.1111/j.1469-0691.2010.03256.x]
  58. Betriu C, Rodríguez-Avial I, Gómez M, Culebras E, Picazo JJ (2005) Changing patterns of fluoroquinolone resistance among Bacteroides fragilis group organisms over a 6-year period (1997–2002). Diagn Microbiol Infect Dis 53:221–223. https://doi.org/10.1016/j.diagmicrobio.2005.06.012 [DOI: 10.1016/j.diagmicrobio.2005.06.012]
  59. Veloo ACM, Tokman HB, Jean-Pierre H, Dumont Y, Jeverica S, Lienhard R, Novak A, Rodloff A, Rotimi V, Wybo I, Nagy E (2020) Antimicrobial susceptibility profiles of anaerobic bacteria, isolated from human clinical specimens, within different European and surrounding countries. A joint ESGAI study. Anaerobe 61:102111. https://doi.org/10.1016/j.anaerobe.2019.102111 [DOI: 10.1016/j.anaerobe.2019.102111]
  60. Behra-Miellet J, Calvet L, Mory F, Muller C, Chomarat M, Bézian MC, Bland S et al (2003) Antibiotic resistance among anaerobic Gram-negative bacilli: lessons from a French multicentric survey. Anaerobe 9:105–111. https://doi.org/10.1016/S1075-9964(03)00066-0 [DOI: 10.1016/S1075-9964(03)00066-0]
  61. Koeth LM, Good CE, Appelbaum PC, Goldstein EJ, Rodloff AC, Claros M, Dubreuil L (2004) Surveillance of susceptibility patterns in 1297 European and US anaerobic and capnophilic isolates to co-amoxiclav and five other antimicrobial agents. J Antimicrob Chemother 53:1039–1044. https://doi.org/10.1093/jac/dkh248 [DOI: 10.1093/jac/dkh248]
  62. Brazier J, Chmelar D, Dubreuil L, Feierl G, Hedberg M, Kalenic S et al (2008) European surveillance study on antimicrobial susceptibility of Gram-positive anaerobic cocci. Int J Antimicrob Agents 31:316–320. https://doi.org/10.1016/j.ijantimicag.2007.11.006 [DOI: 10.1016/j.ijantimicag.2007.11.006]
  63. Boyanova L, Kolarov R, Mitov I (2015) Recent evolution of antibiotic resistance in the anaerobes as compared to previous decades. Anaerobe 31:4–10. https://doi.org/10.1016/j.anaerobe.2014.05.004 [DOI: 10.1016/j.anaerobe.2014.05.004]
  64. Dubreuil L, Odou MF (2010) Anaerobic bacteria and antibiotics: what kind of unexpected resistance could I find in my laboratory tomorrow? Anaerobe 16:555–559. https://doi.org/10.1016/j.anaerobe.2010.10.002 [DOI: 10.1016/j.anaerobe.2010.10.002]
  65. Theron MM, Van Rensburg J, Chalkley LJ (2004) Nitroimidazole resistance genes (nimB) in anaerobic Gram-positive cocci (previously Peptostreptococcus spp). J Antimicrob Chemother 54:240–2. https://doi.org/10.1093/jac/dkh270 [DOI: 10.1093/jac/dkh270]
  66. Faris B, Faris C, Clark J, Brown R, Poxton IR (1999) Metronidazole-resistant strain of Clostridium perfringens isolated from a clinical specimen. J Infect 39:164–165. https://doi.org/10.1016/s0163-4453(99)90013-0 [DOI: 10.1016/s0163-4453(99)90013-0]
  67. Wong SS, Woo PC, Luk WK, Yuen KY (1999) Susceptibility testing of Clostridium difficile against metronidazole and vancomycin by disk diffusion and E-test. Diagn Microbiol Infect Dis 34:1–6. https://doi.org/10.1016/s0732-8893(98)00139-4 [DOI: 10.1016/s0732-8893(98)00139-4]
  68. Peláez T, Alcalá L, Alonso R, Rodríguez-Créixems M, García-Lechuz JM, Bouza E (2002) Reassessment of Clostridium difficile susceptibility to metronidazole and vancomycin. Antimicrob Agents Chemother 46:1647–1650. https://doi.org/10.1128/AAC.46.6.1647-1650.2002 [DOI: 10.1128/AAC.46.6.1647-1650.2002]
  69. Mory F, Carlier JP, Alauzet C, Thouvenin M, Schuhmacher H, Lozniewski A (2005) Bacteremia caused by a metronidazole-resistant Prevotella. J Clin Microbiol 43:5380–5383. https://doi.org/10.1128/JCM.43.10.5380-5383.2005 [DOI: 10.1128/JCM.43.10.5380-5383.2005]
  70. Sandoe AT, Struthers JK, Brazier JS (2001) Subdural empyema caused by Prevotella loescheii with reduced susceptibility to metronidazole. J Antimicrob Chemother 47:366–367. https://doi.org/10.1093/jac/47.3.366 [DOI: 10.1093/jac/47.3.366]
  71. Chauldhry R, Mathur P, Dhawan B, Kumar L (2001) Emergence of metronidazole- resistant Bacteroides fragilis. India Emerg Infect Dis 7:485–486. https://doi.org/10.3201/eid0703.010332 [DOI: 10.3201/eid0703.010332]
  72. Rotimi VO, Khoursheed M, Brazier JS, Jamal WY, Khodakhast FB (1999) Bacteroides species highly resistant to metronidazole: an emerging clinical problem. Clin Microbiol Infect 5:166–169. https://doi.org/10.1111/j.1469-0691.1999.tb00531.x [DOI: 10.1111/j.1469-0691.1999.tb00531.x]
  73. Shapiro JM, Gupta R, Stefansson E, Fang FC, Limaye AP (2004) Isolation of metronidazole-resistant Bacteroides fragilis carrying the nimA nitroreductase gene from a patient in Washington state. J Clin Microbiol 42:4127–9. https://doi.org/10.1128/JCM.42.9.4127-4129.2004 [DOI: 10.1128/JCM.42.9.4127-4129.2004]
  74. Marchandin H, Jean-Pierre H, Campos J, Dubreuil L, Teyssier C, Jumas-Bilak E (2004) NimE gene in a metronidazole-susceptible Veillonella sp. strain. Antimicrob Agents Chemother 48:3207–8. https://doi.org/10.1128/AAC.48.8.3207-3208.2004 [DOI: 10.1128/AAC.48.8.3207-3208.2004]
  75. Alauzet C, Lozniewski A, Marchandin H (2019) Metronidazole resistance and nim genes in anaerobes: a review. Anaerobe 55:40–53. https://doi.org/10.1016/j.anaerobe.2018.10.004 [DOI: 10.1016/j.anaerobe.2018.10.004]
  76. Ghotaslou R, Bannazadeh Baghi H, Alizadeh N, Yekani M, Arbabi S, Memar MY (2018) Mechanisms of Bacteroides fragilis resistance to metronidazole. Infect Genet Evol 64:156–163. https://doi.org/10.1016/j.meegid.2018.06.020 [DOI: 10.1016/j.meegid.2018.06.020]
  77. O’Grady K, Knight DR, Riley TV (2021) Antimicrobial resistance in Clostridioides difficile. Eur J Clin Microbiol Infect Dis 40:2459–2478. https://doi.org/10.1007/s10096-021-04311-5 [DOI: 10.1007/s10096-021-04311-5]
  78. Wickramage I, Spigaglia P, Sun X (2021) Mechanisms of antibiotic resistance of Clostridioides difficile. J Antimicrob Chemother 76:3077–3090. https://doi.org/10.1093/jac/dkab231 [DOI: 10.1093/jac/dkab231]
  79. Sóki J, Eitel Z, Urbán E, Nagy E, on behalf of the ESCMID Study Group on Anaerobic Infections (2013) Molecular analysis of the carbapenem and metronidazole resistance mechanisms of Bacteroides strains reported in a Europe-wide antibiotic resistance survey. Int J Antimicrob Agents 41:122–5. https://doi.org/10.1016/j.ijantimicag.2012.10.001 [DOI: 10.1016/j.ijantimicag.2012.10.001]
  80. Pelaez T, Cercenado E, Alcala L, Marín M, Martín-Lopez A, Martínez- Alarcon J, Catalan P, Sanchez-Somolinos M, Bouza E (2008) Metronidazole resistance in Clostridium difficile is heterogeneous. J Clin Microbiol 46:3028–3032. https://doi.org/10.1128/JCM.00524-08 [DOI: 10.1128/JCM.00524-08]
  81. Hidri N, Barraud O, Garnier F, Martin C, Ploy MC, Denis F (2008) A propos d'une souche de Eggerthella lenta isolée dans une hémoculture résistante a l'Imipénème. Poster. 38th Réunion interdisciplinaire de chimiothérapie anti- infectieuse, RICAI. Paris, France
  82. Dubreuil L, Veloo AC, Sóki J, on behalf of the ESCMID Study Group for Anaerobic Infections (ESGAI) (2021) Correlation between antibiotic resistance and clinical outcome of anaerobic infections; mini-review. Anaerobe 72:102463. https://doi.org/10.1016/j.anaerobe.2021.102463 [DOI: 10.1016/j.anaerobe.2021.102463]
  83. Baaity Z, von Loewenich FD, Nagy E, Orosz L, Burián K, Somogyvári F, Sóki J (2022) Phenotypic and molecular characterization of carbapenem-heteroresistant Bacteroides fragilis strains. Antibiotics (Basel) 11:590. https://doi.org/10.3390/antibiotics11050590 [DOI: 10.3390/antibiotics11050590]
  84. Mazuet C, Yoon EJ, Boyer S, Pignier S, Blanc T, Doehring I, Meziane-Cherif D, Dumant-Forest C, Sautereau J, Legeay C, Bouvet P, Bouchier C, Quijano-Roy S, Pestel-Caron M, Courvalin P, Popoff MR (2016) A penicillin- and metronidazole-resistant Clostridium botulinum strain responsible for an infant botulism case. Clin Microbiol Infect 22:644. https://doi.org/10.1016/j.cmi.2016.04.011 [DOI: 10.1016/j.cmi.2016.04.011]
  85. Song Y, Liu C, Molitoris DR, Tomzynski TJ, Lawson PA, Collins MD, Finegold SM (2003) Clostridium bolteae sp. nov., isolated from human sources. Syst Appl Microbiol 26:84–9. https://doi.org/10.1078/072320203322337353 [DOI: 10.1078/072320203322337353]
  86. Bouvet P, K’Ouas G, Le Coustumier A, Popoff MR (2012) Clostridium celerecrescens, often misidentified as “Clostridium clostridioforme group”, is involved in rare human infection cases. Diagn Microbiol Infect Dis 74:299–302. https://doi.org/10.1016/j.diagmicrobio.2012.06.024 [DOI: 10.1016/j.diagmicrobio.2012.06.024]
  87. Warren YA, Tyrrell KL, Citron DM, Goldstein EJC (2006) Clostridium aldenense sp. nov. and Clostridium citroniae sp. nov. isolated from human clinical infections. J Clin Microbiol 44:2416–22. https://doi.org/10.1128/JCM.00116-06 [DOI: 10.1128/JCM.00116-06]
  88. Rafii F, Park M, Wynne R (2005) Evidence for active drug efflux in fluoroquinolone resistance in Clostridium hathewayi. Chemotherapy 51:256–62. https://doi.org/10.1159/000087253 [DOI: 10.1159/000087253]
  89. Toth M, Stewart NK, Smith C, Vakulenko SB (2018) Intrinsic class D ß-lactamases of Clostridium difficile. mBio 9:1803–18. https://doi.org/10.1128/mBio.01803-18 [DOI: 10.1128/mBio.01803-18]
  90. Alexander CJ, Citron DM, Brazier JS, Goldstein EJC (1995) Identification and antimicrobial resistance patterns of clinical Isolates of Clostridium clostridioforme, Clostridium innocuum, and Clostridium ramosum compared with those of clinical isolates of Clostridium perfringens. J Clin Microbiol 33:3209–3215. https://doi.org/10.1128/jcm.33.12.3209-3215.1995 [DOI: 10.1128/jcm.33.12.3209-3215.1995]
  91. Citron DM, Merriam CV, Tyrrell KL, Warren YA, Fernandez H, Goldstein EJ (2003) In vitro activities of ramoplanin, teicoplanin, vancomycin, linezolid, bacitracin, and four other antimicrobials against intestinal anaerobic bacteria. Antimicrob Agents Chemother 47:2334–2338. https://doi.org/10.1128/AAC.47.7.2334-2338.2003 [DOI: 10.1128/AAC.47.7.2334-2338.2003]
  92. Goldstein EJC, Merriam CV, Citron DM (2020) 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. Antimicrob Agents Chemother 64:1088–1120. https://doi.org/10.1128/AAC.01088-20 [DOI: 10.1128/AAC.01088-20]
  93. Mory F, Lozniewski A, David V, Carlier JP, Dubreuil L, Leclercq R (1998) Low-level vancomycin resistance in Clostridium innocuum. J Clin Microbiol 36:1767–1768. https://doi.org/10.1128/JCM.36.6.1767-1768.1998 [DOI: 10.1128/JCM.36.6.1767-1768.1998]
  94. Goldstein EJ, Citron DM, Merriam CV, Warren YA, Tyrrell KL, Fernandez HT (2004) In vitro activities of the new semisynthetic glycopeptide telavancin (TD-6424), vancomycin, daptomycin, linezolid, and four comparator agents against anaerobic gram-positive species and Corynebacterium spp.. Antimicrob Agents Chemother 48:2149–2152. https://doi.org/10.1128/AAC.48.6.2149-2152.2004 [DOI: 10.1128/AAC.48.6.2149-2152.2004]
  95. Marvaud JC, Mory F, Lambert T (2011) Clostridium clostridioforme and Atopobium minutum clinical isolates with VanB-type resistance in France. J Clin Microbiol 49:3436–3438. https://doi.org/10.1128/JCM.00308-11 [DOI: 10.1128/JCM.00308-11]
  96. Zhou Y, Li J, Schwarz S, Zhang S, Tao J, Fan R, Walsh TR, Wu C, Wang Y (2020) Mobile oxazolidinone/phenicol resistance gene optrA in chicken Clostridium perfringens. J Antimicrob Chemother 75:3067–3069. https://doi.org/10.1093/jac/dkaa236 [DOI: 10.1093/jac/dkaa236]
  97. Zhang S, Liu P, Wang Y, Shen Z, Wang S (2021) Multiresistance gene cfr(C) in Clostridium perfringens of cattle origin from China. J Antimicrob Chemother 76:3310–3312. https://doi.org/10.1093/jac/dkab339 [DOI: 10.1093/jac/dkab339]
  98. Stojković V, Ulate MF, Hidalgo-Villeda F, Aguilar E, Monge-Cascante C, Pizarro-Guajardo M, Tsai K, Tzoc E, Camorlinga M, Paredes-Sabja D, Quesada-Gómez C, Fujimori DG, Rodríguez C (2019) Cfr(B), cfr(C), and a new cfr-like gene, cfr(E), in Clostridium difficile strains recovered across Latin America. Antimicrob Agents Chemother 20(64):01074–01119. https://doi.org/10.1128/AAC.01074-19 [DOI: 10.1128/AAC.01074-19]
  99. Eubank TA, Gonzales-Luna AJ, Hurdle JG, Garey KW (2022) Genetic mechanisms of vancomycin resistance in Clostridioides difficile: a systematic review. Antibiotics (Basel) 11:258. https://doi.org/10.3390/antibiotics11020258 [DOI: 10.3390/antibiotics11020258]
  100. Peng Z, Jin D, Kim HB, Stratton CW, Wu B, Tang Y-W, Sun X (2017) Update on antimicrobial resistance in Clostridium difficile: resistance mechanisms and antimicrobial susceptibility testing. J Clin Microbiol 55:1998–2008. https://doi.org/10.1128/JCM.02250-16 [DOI: 10.1128/JCM.02250-16]
  101. Darkoh C, Keita K, Odo C, Oyaro M, Brown EL, Arias CA et al (2022) Emergence of clinical Clostridioides difficile isolates with decreased susceptibility to vancomycin. Clin Infect Dis 74:120–126. https://doi.org/10.1093/cid/ciaa912 [DOI: 10.1093/cid/ciaa912]
  102. Goldstein EJC, Citron DM, Sears P et al (2011) Comparative susceptibilities to fidaxomicin (OPT-80) of isolates collected at baseline, recurrence, and failure from patients in two phase III trials of fidaxomicin against Clostridium difficile infection. Antimicrob Agents Chemother 55:5194–5199. https://doi.org/10.1128/AAC.00625 [DOI: 10.1128/AAC.00625]
  103. Schwanbeck J, Riedel T, Laukien F et al (2019) Characterization of a clinical Clostridioides difficile isolate with markedly reduced fidaxomicin susceptibility and a V1143D mutation in rpoB. J Antimicrob Chemother 74:6–10. https://doi.org/10.1093/jac/dky375 [DOI: 10.1093/jac/dky375]
  104. Marchandin H, Anjou C, Poulen G, Freeman J, Wilcox M, Jean-Pierre H, Barbut F (2023) In vivo emergence of a still uncommon resistance to fidaxomicin in the urgent antimicrobial resistance threat Clostridioides difficile. J Antimicrob Chemother 78:1992–1999. https://doi.org/10.1093/jac/dkad194 [DOI: 10.1093/jac/dkad194]
  105. Veloo AC, Welling GW, Degener JE (2011) Antimicrobial susceptibility of clinically relevant Gram-positive anaerobic cocci collected over a three-year period in the Netherlands. Antimicrob Agents Chemother 55:1199–203. https://doi.org/10.1128/AAC.01771-09 [DOI: 10.1128/AAC.01771-09]
  106. Shilnikova II, Dmitrieva NV (2015) Evaluation of antibiotic susceptibility of Gram- positive anaerobic cocci isolated from cancer patients of the N. N. Blokhin Russian Cancer Research Center. J Pathog 2015:648134. https://doi.org/10.1155/2015/648134 [DOI: 10.1155/2015/648134]
  107. Guérin F, Dejoies L, Degand N, Guet-Revillet H, Janvier F, Corvec S, et al. On Behalf of the Gmc Study Group (2021) In vitro antimicrobial susceptibility profiles of Gram-positive anaerobic cocci responsible for human invasive infections. Microorganisms. 9:1665. https://doi.org/10.3390/microorganisms9081665
  108. Maraki S, Mavromanolaki VE, Stafylaki D, Kasimati A (2020) Antimicrobial susceptibility patterns of clinically significant Gram-positive anaerobic bacteria in a Greek tertiary-care hospital, 2017–2019. Anaerobe 64:102245. https://doi.org/10.1016/j.anaerobe.2020.102245 [DOI: 10.1016/j.anaerobe.2020.102245]
  109. Akgül Ö, Söyletir G, Toprak NÜ (2020) Antimicrobial susceptibility of pathogenic Gram-positive anaerobic cocci: data of a university hospital in Turkey. Mikrobiyol Bul 54(404):417. https://doi.org/10.5578/mb.69556 [DOI: 10.5578/mb.69556]
  110. Shetty S, Anegundi R, Shenoy PA, Vishwanath S (2023) Understanding antimicrobial susceptibility profile of Finegoldia magna: an insight to an untrodden path. Ann Clin Microbiol Antimicrobials 22:30. https://doi.org/10.1186/s12941-023-00583-1 [DOI: 10.1186/s12941-023-00583-1]
  111. Tan TY, Ng LSY, Kwang LL, Rao S, Eng LC (2017) Clinical characteristics and antimicrobial susceptibilities of anaerobic bacteremia in an acute care hospital. Anaerobe 43:69–74. https://doi.org/10.1016/j.anaerobe.2016.11.009 [DOI: 10.1016/j.anaerobe.2016.11.009]
  112. Cobo F, Granger JR, Sampedro A, Navarro-Mari JM (2017) Infected breast cyst due to Prevotella buccae resistant to metronidazole. Anaerobe 48:177–178. https://doi.org/10.1016/j.anaerobe.2017.08.015 [DOI: 10.1016/j.anaerobe.2017.08.015]
  113. Veloo ACM, Chlebowicz M, Winter HLJ, Bathoorn D, Rossen JWA (2018) Three metronidazole-resistant Prevotella bivia strains harbour a mobile element, encoding a novel nim gene, nimK, and an efflux small MDR transporter. J Antimicrob Chemother 73:2687–2690. https://doi.org/10.1093/jac/dky236 [DOI: 10.1093/jac/dky236]
  114. Alauzet C, Mory F, Teyssier C, Hallage H, Carlier JP, Grollier G, Lozniewski A (2010) Metronidazole resistance in Prevotella spp. and description of a new Nim gene in Prevotella baroniae. Antimicrob Agents Chemother 54:60–4. https://doi.org/10.1128/AAC.01003-09 [DOI: 10.1128/AAC.01003-09]
  115. Mory F, Carlier JP, Alauzet C, Thouvenin M, Schuhmacher H, Lozniewski A (2005) Bacteremia caused by a metronidazole-resistant Prevotella. J Clin Microbiol 43:5380–3. https://doi.org/10.1128/JCM.43.10.5380-5383.2005 [DOI: 10.1128/JCM.43.10.5380-5383.2005]
  116. Piriz S, Vadillo S, Quesada A, Criado J, Cerrato R, Ayala J (2004) Relationship between penicillin-binding protein patterns and ß lactamases in clinical isolates of Bacteroides fragilis with different susceptibility to ß-lactams antibiotic. J Med Microbiol 53:213–21. https://doi.org/10.1099/jmm.0.05409-0 [DOI: 10.1099/jmm.0.05409-0]
  117. Rogers MB, Parker AC, Smith CJ (1993) Cloning and characterization of the endogenous cephalosporinase gene, cepA, from Bacteroides fragilis reveals a new subgroup of Ambler class A beta-lactamases. Antimicrob Agents Chemother 37:2391–2400. https://doi.org/10.1128/AAC.37.11.2391 [DOI: 10.1128/AAC.37.11.2391]
  118. Rogers MB, Bennett TK, Payne CM, Smith CJ (1994) Insertional activation of cepA leads to high-level beta-lactamase expression in Bacteroides fragilis clinical isolates. J Bacteriol 176:4376–84. https://doi.org/10.1128/jb.176.14.4376-4384.1994 [DOI: 10.1128/jb.176.14.4376-4384.1994]
  119. Sóki J, Keszőcze A, Nagy I, Burián K, Nagy E (2021) An update on ampicillin resistance and β-lactamase genes of Bacteroides spp. J Med Microbiol 70:001393. https://doi.org/10.1099/jmm.0.001393 [DOI: 10.1099/jmm.0.001393]
  120. Odou MF, Singer E, Romond MB, Dubreuil L (1988) Isolation and characterization of a porin-like protein of 45 kilodaltons from Bacteroides fragilis. FEMS (Microbiol Soc) Microbiol Lett 166(347):54
  121. Odou MF, Singer E, Dubreuil L (2001) Description of complex forms of a porin in Bacteroides fragilis and possible implication of this protein in antibiotic resistance. Anaerobe 7(219):25. https://doi.org/10.1006/anae.2001.0385 [DOI: 10.1006/anae.2001.0385]
  122. Behra-Miellet J, Calvet L, Dubreuil L (2004) A Bacteroides thetaiotamicron porin that could take part in resistance to beta-lactams. Int J Antimicrob Agents 24(135):43. https://doi.org/10.1016/j.ijantimicag.2004.01.008 [DOI: 10.1016/j.ijantimicag.2004.01.008]
  123. Yekani M, Rezaee MA, Beheshtirouy S, Baghi HB, Bazmani A, Farzinazar A, Memar MY, Sóki J (2022) Carbapenem resistance in Bacteroides fragilis: a review of molecular mechanisms. Anaerobe 76:102606. https://doi.org/10.1016/j.anaerobe.2022.102606 [DOI: 10.1016/j.anaerobe.2022.102606]
  124. Wallace MJ, Jean S, Wallace MA, Burnham CD, Dantas G (2022) Comparative genomics of Bacteroides fragilis group isolates reveals species-dependent resistance mechanisms and validates clinical tools for resistance prediction. mBio 13:03603–21. https://doi.org/10.1128/mbio.03603-21 [DOI: 10.1128/mbio.03603-21]
  125. Sydenham TV, Overballe-Petersen S, Hasman H, Wexler H, Kemp M, Justesen US (2019) Complete hybrid genome assembly of clinical multidrug-resistant Bacteroides fragilis isolates enables comprehensive identification of antimicrobial-resistance genes and plasmids. Microb Genom 5:000312. https://doi.org/10.1099/mgen.0.000312 [DOI: 10.1099/mgen.0.000312]
  126. Gutacker M, Valsangiacomo C, Piffaretti JC (2000) Identification of two genetic groups in Bacteroides fragilis by multilocus enzyme electrophoresis: distribution of antibiotic resistance (cfiA, cepA) and enterotoxin (bft) encoding genes. Microbiol 146:1241–1254. https://doi.org/10.1099/00221287-146-5-1241 [DOI: 10.1099/00221287-146-5-1241]
  127. Sóki J, Edwards R, Hedberg M, Fang H, Nagy E, Nord CE, on behalf of the ESCMID Study Group on Antimicrobial Resistance in Anaerobic Bacteria (2006) Examination of cfiA-mediated carbapenem resistance in Bacteroides fragilis strains from a European antibiotic susceptibility survey. Int J Antimicrob Agents 28:497–502. https://doi.org/10.1016/j.ijantimicag.2006.07.021 [DOI: 10.1016/j.ijantimicag.2006.07.021]
  128. Jeverica S, Sóki J, Premru MM, Nagy E, Papst L (2019) High prevalence of division II (cfiA positive) isolates among blood stream Bacteroides fragilis in Slovenia as determined by MALDI-TOF MS. Anaerobe 58:30–34. https://doi.org/10.1016/j.anaerobe.2019.01.011 [DOI: 10.1016/j.anaerobe.2019.01.011]
  129. Podglajen I, Breuil J, Bordon F, Gutmann L, Collatz E (1992) A silent carbapenemase gene in strains of Bacteroides fragilis can be expressed after a one-step mutation. FEMS Microbiol Lett 91:21–30. https://doi.org/10.1016/0378-1097(92)90557-5 [DOI: 10.1016/0378-1097(92)90557-5]
  130. Schwensen SA, Acar Z, Sydenham TV, Johansson ÅC, Justesen US (2017) Phenotypic detection of the cfiA metallo-β-lactamase in Bacteroides fragilis with the meropenem-EDTA double-ended E-test and the ROSCO KPC/MBL confirm kit. J Antimicrob Chemother 72:437–440. https://doi.org/10.1093/jac/dkw436 [DOI: 10.1093/jac/dkw436]
  131. Nagy E, Becker S, Sóki J, Urbán E, Kostrzewa M (2011) 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. J Med Microbiol 60:1584–1590. https://doi.org/10.1099/jmm.0.031336-0 [DOI: 10.1099/jmm.0.031336-0]
  132. Cordovana M, Kostrzewa M, Sóki J, Witt E, Ambretti S, Pranada AB (2018) Bacteroides fragilis: a whole MALDI-based workflow from identification to confirmation of carbapenemase production for routine laboratories. Anaerobe 54:246–253. https://doi.org/10.1016/j.anaerobe.2018.04.004 [DOI: 10.1016/j.anaerobe.2018.04.004]
  133. Wang Y, Guo B, Gao X, Wen J, Wang Z, Wang J (2023) High prevalence of cfiA positive Bacteroides fragilis isolates collected at a teaching hospital in Hohhot, China. Anerobe 79:102691. https://doi.org/10.1016/j.anaerobe.2022.102691 [DOI: 10.1016/j.anaerobe.2022.102691]
  134. Kaeuffer C, Tiffany RT, Driancourt L, Romain B, Ruch Y, Jaulhac B, Boyer HM (2021) First case of bacteraemia due to carbapenem-resistant Bacteroides faecis. Antibiotics (Basel) 10:319. https://doi.org/10.3390/antibiotics10030319 [DOI: 10.3390/antibiotics10030319]
  135. Hurlbut S, Cuchural GJ, Tally FP (1990) Imipenem resistance in Bacteroides distasonis mediated by a novel ß-lactamase. Antimicrob Agents Chemother 34:117–120. https://doi.org/10.1128/AAC.34.1.117 [DOI: 10.1128/AAC.34.1.117]
  136. Sadarangani SP, Cunningham SA, Jeraldo PR, Wilson JW, Khare R, Patel R (2015) Metronidazole- and carbapenem-resistant Bacteroides thetaiotaomicron isolated in Rochester, Minnesota, in 2014. Antimicrob Agents Chemother 59:4157–4161. https://doi.org/10.1128/AAC.00677-15 [DOI: 10.1128/AAC.00677-15]
  137. Citron DM, Tyrrell KL, Merriam V, Goldstein EJ (2011) In vitro activity of ceftazidime-NXL104 against 396 strains of beta-lactamase-producing anaerobes. Antimicrob Agents Chemother 55:3616–3620. https://doi.org/10.1128/AAC.01682-10 [DOI: 10.1128/AAC.01682-10]
  138. Dubreuil LJ, Mahieux S, Neut C, Miossec C, Pace J (2012) Anti-anaerobic activity of a new ß-lactamase inhibitor NXL104 in combination with ß-lactams and metronidazole. Int J Antimicrob Agents 39(500):4. https://doi.org/10.1016/j.ijantimicag.2012.02.013 [DOI: 10.1016/j.ijantimicag.2012.02.013]
  139. Syndman DR, Jacobus NV, McDermott LA (2016) In vitro evaluation of the activity of imipenem-relebactam against 451 recent clinical isolates of Bacteroides group and related species. Antimicrob Agents Chemother 60:6393–6397. https://doi.org/10.1128/AAC.01125-16 [DOI: 10.1128/AAC.01125-16]
  140. Goldstein EJC, Citron DM, Tyrrell KL, Leoncio E, Merriama CV (2018) Comparative in vitro activities of relebactam, imipenem, the combination of the two, and six comparator antimicrobial agents against 432 strains of anaerobic organisms, including imipenem-resistant strains. Antimicrob Agents Chemother 62:01992–02017. https://doi.org/10.1128/AAC.01992-17 [DOI: 10.1128/AAC.01992-17]
  141. Lomovskaya O, Tsivkovski R, Nelson K, Rubio-Aparicio D, Sun D, Totrov M, Dudleya MN (2020) Spectrum of beta-lactamase inhibition by the cyclic boronate QPX7728, an ultrabroad-spectrum beta-lactamase inhibitor of serine and metallo-beta-lactamases: enhancement of activity of multiple antibiotics against isogenic strains expressing single beta-lactamases. Antimicrob Agents Chemother 64:212–220. https://doi.org/10.1128/AAC.00212-20 [DOI: 10.1128/AAC.00212-20]
  142. Ghotasou R, Baghi HB, Alizadeh N, Yekani M, Arbabi S, Memar MY (2018) Mechanisms of Bacteroides fragilis resistance to metronidazole. Infect Genet Evol 64:156–163. https://doi.org/10.1016/j.meegid.2018.06.020 [DOI: 10.1016/j.meegid.2018.06.020]
  143. Baaity Z, Jamal W, Rotimi VO, Burian K, Leitsch D, Somogyvari F, Nagy E, Sóki J (2021) Molecular characterization of metronidazole resistant Bacteroides strains from Kuwait. Anaerobe 69:102357. https://doi.org/10.1016/j.anaerobe.2021.102357 [DOI: 10.1016/j.anaerobe.2021.102357]
  144. Otte E, Nielsen HL, Hasman H, Fuglsang-Damgaard D (2017) First report of metronidazole resistant, nimD-positive, Bacteroides stercoris isolated from an abdominal abscess in a 70-year-old woman. Anaerobe 43:91–93. https://doi.org/10.1016/j.anaerobe.2016.12.01 [DOI: 10.1016/j.anaerobe.2016.12.01]
  145. Copsey-Mawe S, Hughes H, Scotford S, Anderson B, Davis C, Perry MD, Morris TE (2021) UK Bacteroides species surveillance survey: change in antimicrobial resistance over 16 year (2000–2916). Anaerobe 72:102447. https://doi.org/10.1016/j.anaerobe.2021.102447 [DOI: 10.1016/j.anaerobe.2021.102447]
  146. Imwattana K, Kiratisin P, Riley TV (2022) Antimicrobial-resistant Bacteroides fragilis in Thailand and their inhibitory effect in vitro on the growth of Clostridioides difficile. Anaerobe 73:102505. https://doi.org/10.1016/j.anaerobe.2021.102505 [DOI: 10.1016/j.anaerobe.2021.102505]
  147. Hartmeyer GN, Sóki J, Nagy E, Justesen US (2012) Multidrug-resistant Bacteroides fragilis group on the rise in Europe? J Med Microbiol 61:1784–1788. https://doi.org/10.1099/jmm.0.049825-0 [DOI: 10.1099/jmm.0.049825-0]
  148. Sóki J, Hedberg M, Patrick S, Bálint B, Herczeg R, Nagy I, Hecht DW, Nagy E, Urbán E (2016) Emergence and evolution of an international cluster of MDR Bacteroides fragilis isolates. J Antimicrob Chemother 71:2441–2448. https://doi.org/10.1093/jac/dkw175 [DOI: 10.1093/jac/dkw175]
  149. Boyanova L, Markovska R, Ivan MI (2019) Multidrug resistance in anaerobes. Future Microbiol 14:1055–1064. https://doi.org/10.2217/fmb-2019-0132 [DOI: 10.2217/fmb-2019-0132]
  150. Rong SMM, Rodloff AC, Stingu CZ (2021) Diversity of antimicrobial resistance genes in Bacteroides and Parabacteroides strains isolated in Germany. J Global Antimicrob resistance 24:328–334. https://doi.org/10.1016/j.jgar.2021.01.007 [DOI: 10.1016/j.jgar.2021.01.007]
  151. Behra-Miellet J, Calvet L, Dubreuil L (2003) Activity of linezolid against anaerobic bacteria. Int J Antimicrob Agents 22:28–34. https://doi.org/10.1016/s0924-8579(03)00087-6 [DOI: 10.1016/s0924-8579(03)00087-6]
  152. Wareham DW, Wilks M, Ahmed D, Brazier JS, Millar M (2005) Anaerobic sepsis due to multidrug-resistant Bacteroides fragilis: microbiological cure and clinical response with linezolid therapy. Clin Infect Dis 40:67–68. https://doi.org/10.1086/428623 [DOI: 10.1086/428623]
  153. Goldstein EJ, Citron DM, Tyrrell KL, Leoncio ES, Merriam CV (2017) The underappreciated in vitro activity of tedizolid against Bacteroides fragilis species, including strains resistant to metronidazole and carbapenems. Anaerobe 43:1–3. https://doi.org/10.1016/j.anaerobe.2016.09.008 [DOI: 10.1016/j.anaerobe.2016.09.008]
  154. Ghotaslou R, Yekani M, Memar MY (2018) The role of efflux pumps in Bacteroides fragilis resistance to antibiotics. Microbiol Res 210:1–5. https://doi.org/10.1016/j.micres.2018.02.007 [DOI: 10.1016/j.micres.2018.02.007]
  155. Wexler HM (2012) Pump it up: occurrence and regulation of multi-drug efflux pumps5in Bacteroides fragilis. Anaerobe 18:200–208. https://doi.org/10.1016/j.anaerobe.2011.12.017 [DOI: 10.1016/j.anaerobe.2011.12.017]
  156. Pumbwe L, Glass D, Wexler HM (2006) Efflux pump overexpression in multiple-antibiotic-resistant mutants of Bacteroides fragilis. Antimicrob Agents Chemother 2006(50):3150–3153. https://doi.org/10.1128/AAC.00141-06 [DOI: 10.1128/AAC.00141-06]
  157. Miyamae S, Ueda O, Yoshimura F, Hwang J, Tanaka Y, Nikaido H (2001) A MATE family multidrug efflux transporter pumps out fluoroquinolones in Bacteroides thetaiotaomicron. Antimicrob Agents Chemother 45:3341–3346. https://doi.org/10.1128/AAC.00141-06 [DOI: 10.1128/AAC.00141-06]
  158. Boiten KE, Kuijper EJ, Schuele L, van Prehn J, Bode LGM, Maat I, van Asten SAV, Notermans DW, Rossen JWA, Veloo ACM (2023) Characterization of mobile genetic elements in multidrug-resistant Bacteroides fragilis isolates from different hospitals in the Netherlands. Anaerobe 81:102722. https://doi.org/10.1016/j.anaerobe.2023.102722 [DOI: 10.1016/j.anaerobe.2023.102722]

MeSH Term

Humans
Drug Resistance, Bacterial
Bacteria, Anaerobic
Clostridium
Microbial Sensitivity Tests
Gram-Positive Cocci
Anti-Bacterial Agents
Bacterial Infections

Chemicals

Anti-Bacterial Agents

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Created with Highcharts 10.0.0infectionsanaerobesAnaerobicantibioticsusceptibilityanaerobicidentificationmethodsgreaterGPACtreatmentbacteriaaccessibletestingASTwillRenewinterestenthusiasmstemtechnologicalimprovementsculturemediaproductionadequateatmosphereawarenesspartclinicianshistoricallytreatedempiricallytargetingspeciesknowninvolvedtypeinfectionPrevotellafusobacteriaGram-positivecocciconsideredresponsiblediaphragmwhereasintra-abdominalBacteroidesfragilisgroupBFGclostridiapredominantlyimplicatedtakenconsiderationclinicianeventfailurefacedmultidrug-resistantMDRevolutionresistancetogetherclinicalfailuresdueabsencedetectionhetero-resistantclonesresultedneeddiscdiffusionmethodImprovedisolationalongavailabilityrobustperformingensurewhetherempiricalguidedantibiogramleadbetteroutcomesFiftyyearsdevotedanaerobes:historicallessonshighlightsAntibioticClinicaloutcomeResistancemechanism

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