Ann Lab Med 2019; 39(2): 190-199  https://doi.org/10.3343/alm.2019.39.2.190
Antimicrobial Susceptibility Patterns of Anaerobic Bacterial Clinical Isolates From 2014 to 2016, Including Recently Named or Renamed Species
Jung-Hyun Byun, M.D.1, Myungsook Kim, Ph.D.1, Yangsoon Lee, M.D.2*, Kyungwon Lee, M.D.1, and Yunsop Chong, Ph.D.1

1Department of Laboratory Medicine, Research Institute of Bacterial Resistance, Yonsei University College of Medicine, Seoul, Korea.

2Department of Laboratory Medicine, Hanyang University Seoul Hospital, Hanyang University College of Medicine, Seoul, Korea.

Corresponding author: Yangsoon Lee, M.D. Department of Laboratory Medicine, Hanyang University Seoul Hospital, Hanyang University College of Medicine, 222-1 Wangsimni-ro, Seongdong-gu, Seoul 04763, Korea. Tel: +82-2-2290-9655, Fax: +82-2-2290-9193, yangsoon@hanyang.ac.kr
Received: May 15, 2018; Revised: July 17, 2018; Accepted: October 25, 2018; Published online: November 13, 2018.
© Korean Society for Laboratory Medicine. All rights reserved.

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
Abstract

Background

Anaerobic bacterial resistance trends may vary across regions or institutions. Regional susceptibility patterns are pivotal in the empirical treatment of anaerobic infections. We determined the antimicrobial resistance patterns of clinically important anaerobic bacteria, including recently named or renamed anaerobes.

Methods

A total of 521 non-duplicated clinical isolates of anaerobic bacteria were collected from a tertiary-care hospital in Korea between 2014 and 2016. Anaerobes were isolated from blood, body fluids, and abscess specimens. Each isolate was identified by conventional methods and by Bruker biotyper mass spectrometry (Bruker Daltonics, Leipzig, Germany) or VITEK matrix-assisted laser desorption ionization time-of-flight mass spectrometry (bioMérieux, Marcy-l'Étoile, France). Antimicrobial susceptibility was tested using the agar dilution method according to the CLSI guidelines. The following antimicrobials were tested: piperacillin-tazobactam, cefoxitin, cefotetan, imipenem, meropenem, clindamycin, moxifloxacin, chloramphenicol, tetracycline, and metronidazole.

Results

Most Bacteroides fragilis isolates were susceptible to piperacillin-tazobactam, imipenem, and meropenem. The non-fragilis Bacteroides group (including B. intestinalis, B. nordii, B. pyogenes, B. stercoris, B. salyersiae, and B. cellulosilyticus) was resistant to meropenem (14%) and cefotetan (71%), and Parabacteroides distasonis was resistant to imipenem (11%) and cefotetan (95%). Overall, the Prevotella and Fusobacterium isolates were more susceptible to antimicrobial agents than the B. fragilis group isolates. Anaerobic gram-positive cocci exhibited various resistance rates to tetracycline (6–86%). Clostridioides difficile was highly resistant to penicillin, cefoxitin, imipenem, clindamycin, and moxifloxacin.

Conclusions

Piperacillin-tazobactam, cefoxitin, and carbapenems are highly active β-lactam agents against most anaerobes, including recently named or renamed species.

Keywords: Antimicrobial resistance pattern, Anaerobes, Bacteroides, Korea
INTRODUCTION

The prevalence of antibiotic resistance in anaerobes is increasing, which impacts both antibiotic treatment and patient mortality [1]. Regional susceptibility patterns are pivotal in the empirical treatment of anaerobic infections. As the resistance trends of anaerobic bacteria may vary greatly, across regions or institutions [2, 3, 4], antimicrobial susceptibility tests (ASTs) should be performed to assist with empirical antimicrobial treatment of anaerobic infections.

The CLSI has stated that routine ASTs for anaerobes are not necessary, because antibiotic resistance is often predictable [5]. Therefore, we do not always perform ASTs; however, since 1989, we have been performing periodic ASTs to investigate resistance trends among clinical bacterial isolates [6, 7, 8, 9].

Anaerobic gram-negative bacilli (GNB) are clinically important because they have high resistance rates relative to other anaerobic bacteria [10]. Recently, a related cluster of multidrug-resistant Bacteroides fragilis isolates were recovered from several patients, which resulted in treatment failure in some cases [11, 12]. Furthermore, a number of anaerobic species have recently been named or renamed. Parabacteroides distasonis and P. goldsteinii were reclassified from the genus Bacteroides; Alloscardovia omnicolens, Bulleidia extructa, Leptotrichia trevisanii, Alistipes finegoldii, and Alistipes onderdonkii were named in the 2000s [13, 14, 15, 16, 17, 18]. Moreover, AST data for infrequently isolated species are quite limited. Therefore, we collected rarely isolated anaerobic bacteria from clinical specimens and evaluated them using ASTs. In addition, we determined the antimicrobial resistance patterns of clinically important anaerobic bacteria, including recently named or renamed anaerobes.

METHODS

Bacterial isolates

A total of 521 non-duplicated clinical anaerobic bacteria isolates were collected from a tertiary-care hospital (Severance Hospital, Seoul, Korea) between 2014 and 2016. Anaerobes were isolated from blood, body fluids, and abscess specimens. Each isolate was identified by conventional methods, Bruker biotyper mass spectrometry (Bruker Daltonics, Leipzig, Germany), or VITEK matrix-assisted laser desorption ionization time-of-flight mass spectrometry (bioMérieux, Marcy-l'Étoile, France).

We tested a total of 230 gram-negative isolates, including 60 Bacteroides fragilis, 68 non-fragilis Bacteroides spp., 29 Parabacteroides spp., 33 Prevotella spp., 19 Fusobacterium spp., 10 other anaerobic GNB, and 11 Veillonella spp. Non-fragilis Bacteroides isolates were divided into two groups as follows: Group I included B. thetaiotaomicron, B. caccae, B. uniformis, B. vulgatus, and B. ovatus; Group II were recently classified, renamed, or infrequently isolated including B. intestinalis, B. nordii, B. pyogenes, B. stercoris, B. salyersiae, and B. cellulosilyticus. A total of 291 gram-positive isolates were tested, including 31 Finegoldia magna, 29 Parvimonas micra, 14 other gram-positive cocci (GPC), 15 Clostridioides difficile, 27 Clostridium spp., 34 Actinomyces odontolyticus, 23 Actinomyces spp., 18 Bifidobacterium spp., 38 Eggerthella lenta, 36 Lactobacillus spp., and 26 other gram-positive bacilli.

ASTs

ASTs were conducted using the agar dilution method, and minimum inhibitory concentrations (MICs) were interpreted according to the CLSI guidelines [5, 19]. The medium used was Brucella agar (Becton Dickinson, Cockeysville, MD, USA) supplemented with 5 µg/mL hemin, 1 µg/mL vitamin K1, and 5% laked sheep blood. The following antimicrobials were tested: penicillin (Sigma Aldrich, Yongin, Korea), piperacillin-tazobactam (Yuhan, Seoul, Korea), cefoxitin (Merck Sharp & Dohme, West Point, PA, USA), cefotetan (Daiichi Pharmaceutical, Tokyo, Japan), imipenem and metronidazole (Choongwae, Seoul, Korea), clindamycin (Korea Upjohn, Seoul, Korea), meropenem (Sumitomo, Tokyo, Japan), moxifloxacin (Bayer Korea, Seoul, Korea), chloramphenicol (Chong Kun Dang, Seoul, Korea), and tetracycline (Sigma Aldrich). For the piperacillin and tazobactam combination, a constant concentration of tazobactam (4 µg/mL) was added. An inoculum of 105 colony forming units (CFUs) was applied with a Steers replicator (Craft Machine Inc., Woodline, PA, USA), and the plates were incubated in an anaerobic chamber (Forma Scientific, Marietta, OH, USA) for 48 hours at 37℃. Quality control was tested with the following two organisms: B. fragilis ATCC 25285 and B. thetaiotaomicron ATCC 29741. Double-disk potentiation tests (DPTs) with dipicolinic acid were carried out on Brucella agar to screen for carbapenemase-producing B. fragilis group isolates [20].

RESULTS

Anaerobic gram-negative isolates

Most of the gram-negative isolates tested were susceptible to piperacillin-tazobactam, imipenem, and meropenem, as their resistance rates to these three antimicrobials were <7% (Table 1). Low frequencies of resistance to chloramphenicol and metronidazole were observed for most of the anaerobic gram-negative bacterial isolates tested.

High rates of resistance to penicillin (98–100%), cefotetan (12–71%), and clindamycin (38–69%) were noted for the B. fragilis group isolates. The resistance of B. fragilis isolates to cefotetan was 12%; however, the non-fragilis Bacteroides Group II isolates showed high resistance to cefotetan (71%). Furthermore, Parabacteroides spp. (including P. distasonis), reclassified from the genus Bacteroides, showed very high resistance to cefotetan (95–100%). The resistance of B. fragilis and non-fragilis Bacteroides group I and II isolates to moxifloxacin was 20% and 16%, respectively. Overall, Parabacteroides spp. exhibited higher resistance rates relative to B. fragilis spp., especially for clindamycin (79%) and moxifloxacin (24%). Bacteroides fragilis exhibited imipenem and meropenem-resistance rates of 5%. Non-fragilis Bacteroides Group I showed resistance to only imipenem (2%), while non-fragilis Bacteroides Group II showed resistance to only meropenem (14%). The meropenem MIC required to decrease growth by 90% (MIC90=16 µg/mL) for non-fragilis Bacteroides Group II was higher than that for B. fragilis and non-fragilis Bacteroides Group I (MIC90=2 µg/mL). Four carbapenem-non-susceptible B. fragilis isolates showed positive results on DPTs, whereas eight carbapenem-non-susceptible non-fragilis Bacteroides isolates (including B. thetaiotaomicron, B. intestinalis, B. nordii, P. distasonis, and P. merdae) showed negative results.

Overall, Prevotella and Fusobacterium isolates were more susceptible to antimicrobial agents than B. fragilis group isolates. Interestingly, one Prevotella spp. isolate was resistant to metronidazole (3%). The other anaerobic GNB were susceptible to most of the antibiotics tested. However, all Leptotrichia isolates were resistant to moxifloxacin (MIC=8–16 µg/mL). Megamonas spp. and Sutterella wadsworthensis were resistant to piperacillin-tazobactam (MIC ≥128 µg/mL), and three Veillonella isolates (27%) were resistant to metronidazole.

Anaerobic gram-positive isolates

A total of 74 anaerobic GPC, including 31 Finegoldia magna and 29 Parvimonas micra, exhibited various resistance rates to moxifloxacin (6–48%), clindamycin (3–43%), and tetracycline (6–86%). Overall, F. magna isolates were more susceptible than other GPC isolates, with a resistance rate <6% to all antimicrobials tested (Table 1). The resistance rate of the other GPC isolates to penicillin was 36%, with all species identified as Peptoniphilus.

C. difficile showed high resistance to penicillin (100%), cefoxitin (100%), imipenem (93%), and moxifloxacin (53%). All non-odontolyticus Actinomyces and Lactobacillus isolates and 65% of Actinomyces odontolyticus isolates were resistant to metronidazole. All non-odontolyticus Actinomyces isolates were susceptible to the other antimicrobial agents tested, except for clindamycin (22% resistance) and tetracycline (22% resistance). E. lenta demonstrated high resistance rates to penicillin (47%), cefotetan (95%), tetracycline (61%), and moxifloxacin (32%). Other GPB, such as Actinotignum, Alloscardovia, Bulleidia, Collinsella, Flavonifractor, and Slackia, were generally susceptible to all agents tested, except for metronidazole.

DISCUSSION

The Bacteroides fragilis group of anaerobic gram-negative isolates (including Parabacteroides spp.) are the most clinically significant anaerobes because they are commonly isolated from clinical specimens and show greater virulence and resistance than most other anaerobes [10]. The resistance of B. fragilis isolates to cefotetan remained low for several years: 14% in 1997–2004 [8], 14% in 2007–2008 [7], 13% in 2009–2012 [9], and 12% in 2014–2016.

The resistance of B. fragilis isolates to moxifloxacin has steadily increased over the past 11 years, from 11% in 2007–2008 to 20% in 2014–2016. The current values are similar to those observed in 2010–2012 in the USA (19.1%) [21]. The resistance to moxifloxacin among non-fragilis Bacteroides group species has not increased; the rates have ranged from 18% in 2007–2008 to 16% in 2014–2016 [7]. This may reflect the fact that the B. fragilis group includes former members of the group previously reclassified as Parabacteroides spp. [7]. Parabacteroides spp. had a higher resistance rate to clindamycin and a lower resistance rate to moxifloxacin compared with isolates in the USA (50% and 44%, respectively) [21].

We observed that non-fragilis Bacteroides Group II had higher resistance rates to meropenem than imipenem, while non-fragilis Bacteroides Group I demonstrated the opposite pattern. Such patterns have been previously reported by Sóki et al. [22]; however, they did not include the carbapenem resistance patterns of non-fragilis Bacteroides Group II.

Prevotella spp. were highly susceptible to most antimicrobials except penicillin and clindamycin. The resistance rates to clin-damycin remained high, at 45%, for Prevotella spp., compared with 50% in 2007–2008 [7]. Only one Prevotella spp. isolate was resistant to metronidazole. This represents an even lower rate of resistance than that reported in Greece (8%) [23]. The Veillonella resistance rate to metronidazole was 27%, higher than that reported in the USA (11%) [4].

The anaerobic GPC isolates exhibited various rates of resistance to penicillin, clindamycin, and metronidazole [2]. However, the resistance rate of GPC to clindamycin, moxifloxacin, and tetracycline varied across species. The resistance of C. difficile to imipenem has rapidly increased over the past years, from 8% in 2007–2008 to 93% in 2014–2016 [7]. There is a general assumption that resistance varies with ribotype; Lee et al. [24] showed that ribotypes 017 and 018 have high MICs for moxifloxacin and imipenem, compared with ribotype 001. Metronidazole-resistant isolates were common among Actinomyces and Lactobacillus spp. A study in Argentina showed that all Actinomyces spp. were susceptible to penicillin, and 21.2% were resistant to clindamycin [25]. E. lenta has been commonly associated with gastrointestinal infections; its overall mortality is significant, ranging from 36% to 48% [26, 27]. The E. lenta resistance rates we observed were much higher than those in Australia (0% for penicillin and 12% for moxifloxacin) [26].

The limitations of this study were the small number of renamed and reclassified bacteria and bacterial isolates collected. Further, it was a single-center, retrospective study.

In conclusion, piperacillin-tazobactam, cefoxitin, and carbapenems were β-lactam agents highly active against most of the anaerobic bacteria we tested. However, recently renamed non-fragilis Bacteroides group isolates showed resistance to meropenem (14%). These data suggest the importance of ongoing surveillance to provide clinically relevant information to clinicians for the empirical management of infections caused by anaerobic organisms. Continuous monitoring is necessary to detect changes in antimicrobial resistance patterns.

Authors' Disclosures of Potential Conflicts of Interest:

No potential conflicts of interest relevant to this article were reported.

Acknowledgements

We wish to thank Seungeun Ji and Young Hee Seo for their technical assistance. This study was supported by a faculty research grant from Yonsei University (6-2016-0071).

Tables

Antimicrobial susceptibility of 521 anaerobic bacterial isolates from 2014 to 2016

N of isolates and antimicrobial agentsBreakpoint (μg/mL)MIC (μg/mL)Susceptibility (%)*
SIRRange50%90%SIR
Bacteroides fragilis (60)
 Penicillin≤ 0.51≥24– > 12816> 12800100
 Piperacillin-tazobactam≤ 3264≥ 1280.12– > 128149505
 Cefoxitin≤ 1632≥ 644–6483282127
 Cefotetan≤ 1632≥ 642– > 128864751312
 Imipenem≤48≥ 16≤0.06–320.1219505
 Meropenem≤48≥ 16≤ 0.06– > 1280.1229235
 Clindamycin≤24≥8≤ 0.06– > 1281> 12860238
 Moxifloxacin≤24≥8≤0.06–320.5877320
 Chloramphenicol≤816≥ 324–84810000
 Metronidazole≤816≥ 320.25–84410000
Non-fragilis Bacteroides group I (54)
 Penicillin≤ 0.51≥2≤ 0.06– > 128128> 1282098
 Piperacillin-tazobactam≤ 3264≥ 128≤ 0.06– > 1288329326
 Cefoxitin≤ 1632≥ 641– > 128163257357
 Cefotetan≤ 1632≥ 640.5– > 12864> 128172459
 Imipenem≤48≥ 16≤0.06–320.529442
 Meropenem≤48≥ 16≤ 0.06–40.5210000
 Clindamycin≤24≥8≤ 0.06– > 128> 128> 128201169
 Moxifloxacin≤24≥8≤0.06–322878715
 Chloramphenicol≤816≥ 322–88810000
 Metronidazole≤816≥ 320.5–82410000
Non-fragilis Bacteroides group II (14)
 Penicillin≤ 0.51≥216– > 12816> 12800100
 Piperacillin-tazobactam≤ 3264≥ 1280.5–3283210000
 Cefoxitin≤ 1632≥ 641–64323243507
 Cefotetan≤ 1632≥ 644– > 1286412821771
 Imipenem≤48≥ 160.12–20.25210000
 Meropenem≤48≥ 160.12–320.251686014
 Clindamycin≤24≥80.5– > 128> 128> 12836064
 Moxifloxacin≤24≥80.5–6411679021
 Chloramphenicol≤816≥ 324–88810000
 Metronidazole≤816≥ 322–42410000
Parabacteroides distasonis (19)
 Penicillin≤ 0.51≥2≤ 0.06– > 128> 128> 1285095
 Piperacillin-tazobactam≤ 3264≥ 128≤ 0.06– > 12832> 12889011
 Cefoxitin≤ 1632≥ 641–1283264214237
 Cefotetan≤ 1632≥ 641– > 128128> 1285095
 Imipenem≤48≥ 16≤0.06–6411689011
 Clindamycin≤24≥8≤ 0.06– > 128> 128> 12851679
 Moxifloxacin≤24≥80.12–320.51679021
 Chloramphenicol≤816≥ 322–88810000
 Metronidazole≤816≥ 320.5–42410000
Parabacteroides spp. (10)§
 Penicillin≤ 0.51≥28– > 128> 128> 12800100
 Piperacillin-tazobactam≤ 3264≥ 1282–32163210000
 Cefoxitin≤ 1632≥ 6416–643264205030
 Cefotetan≤ 1632≥ 6464– > 128128> 12800100
 Imipenem≤48≥ 161–41410000
 Clindamycin≤24≥80.5– > 128> 128> 12820080
 Moxifloxacin≤24≥80.25–160.516601030
 Chloramphenicol≤816≥ 324–88810000
 Metronidazole≤816≥ 321–42410000
Prevotella spp. (33)ǁ
 Penicillin≤ 0.51≥2≤ 0.06– > 12816326391
 Piperacillin-tazobactam≤ 3264≥ 128≤ 0.06–8≤ 0.06≤ 0.0610000
 Cefoxitin≤ 1632≥ 640.5–32149730
 Cefotetan≤ 1632≥ 640.5–642328893
 Imipenem≤48≥ 16≤ 0.06–1≤ 0.06≤ 0.0610000
 Clindamycin≤24≥8≤ 0.06– > 128≤ 0.06> 12855045
 Moxifloxacin≤24≥80.12–640.5470219
 Chloramphenicol≤816≥ 321–16289190
 Metronidazole≤816≥ 320.12–32189163
Fusobacterium spp.(19)
 Penicillin≤ 0.51≥2≤ 0.06– > 1280.25479516
 Piperacillin-tazobactam≤ 3264≥ 128≤ 0.06–82410000
 Cefoxitin≤ 1632≥ 640.12–164810000
 Cefotetan≤ 1632≥ 64≤0.06–32249550
 Imipenem≤48≥ 16≤ 0.06–41210000
 Meropenem≤48≥ 16≤ 0.06–2≤ 0.06110000
 Clindamycin≤24≥8≤ 0.06–128216582121
 Moxifloxacin≤24≥8≤ 0.06–12848424711
 Chloramphenicol≤816≥ 32≤ 0.06–22210000
 Metronidazole≤816≥ 320.12–1≤ 0.06110000
Other gram-negative bacilli (10)**
 Penicillin≤ 0.51≥2≤ 0.06– > 128116303040
 Piperacillin-tazobactam≤ 3264≥ 128≤ 0.06– > 128112880020
 Cefoxitin≤ 1632≥ 640.25–3223280200
 Cefotetan≤ 1632≥ 640.5–322490100
 Imipenem≤48≥ 16≤ 0.06–0.50.250.2510000
 Clindamycin≤24≥8≤0.06–32≤ 0.06490010
 Moxifloxacin≤24≥8≤0.06–160.516501040
 Chloramphenicol≤816≥ 320.25–84810000
 Metronidazole≤816≥ 32≤0.06–64NANANANANA
Veillonella spp. (11)††
 Penicillin≤ 0.51≥22–1641600100
 Piperacillin-tazobactam≤ 3264≥ 1284–12816329109
 Cefoxitin≤ 1632≥ 642–84810000
 Cefotetan≤ 1632≥ 640.5–32129190
 Imipenem≤48≥ 160.25–80.5029190
 Clindamycin≤24≥8≤ 0.06– > 128≤ 0.0629109
 Moxifloxacin≤24≥8≤0.06–640.2548299
 Chloramphenicol≤816≥ 320.5–22210000
 Metronidazole≤816≥ 322–3283273027
Finegoldia magna (31)
 Penicillin≤ 0.51≥2≤ 0.06–0.12≤ 0.06≤ 0.0610000
 Piperacillin-tazobactam≤ 3264≥ 128≤ 0.06–0.12≤ 0.06≤ 0.0610000
 Cefoxitin≤ 1632≥ 640.25–40.5210000
 Cefotetan≤ 1632≥ 640.12–40.25210000
 Imipenem≤48≥ 16≤ 0.06– ≤ 0.06≤ 0.06≤ 0.0610000
 Clindamycin≤24≥8≤0.06–64≤ 0.060.59433
 Moxifloxacin≤24≥80.12–80.250.59406
 Metronidazole≤816≥ 320.12–81110000
 Tetracycline≤48≥ 16≤0.06–160.2549406
Parvimonas micra (29)
 Penicillin≤ 0.51≥2≤ 0.06–0.250.120.2510000
 Piperacillin-tazobactam≤ 3264≥ 128≤ 0.06–20.120.2510000
 Cefoxitin≤ 1632≥ 640.25–40.5110000
 Cefotetan≤ 1632≥ 640.5–21210000
 Imipenem≤48≥ 16≤ 0.06–0.25≤ 0.060.1210000
 Clindamycin≤24≥8≤ 0.06–128112876024
 Moxifloxacin≤24≥8≤0.06–3223252048
 Metronidazole≤816≥ 320.5–41210000
 Tetracycline≤48≥ 161–64163245055
Other gram-positive cocci (14)i
 Penicillin≤ 0.51≥2≤ 0.06–80.12864036
 Piperacillin-tazobactam≤ 3264≥ 128≤0.06–160.251610000
 Cefoxitin≤ 1632≥ 64≤0.06–160.51610000
 Cefotetan≤ 1632≥ 640.25–128412850743
 Imipenem≤48≥ 16≤ 0.06–40.25410000
 Clindamycin≤24≥8≤ 0.06–1280.2512850743
 Moxifloxacin≤24≥80.12–162864729
 Metronidazole≤816≥ 320.5–82210000
 Tetracycline≤48≥ 160.25–64326414086
Clostridioides difficile (15)
 Penicillin≤ 0.51≥22–42400100
 Piperacillin-tazobactam≤ 3264≥ 1284–16161610000
 Cefoxitin≤ 1632≥ 64128– > 128128> 12800100
 Cefotetan≤ 1632≥ 6416–643264204040
 Imipenem≤48≥ 164–6416327093
 Clindamycin≤24≥81– > 12816> 12872767
 Moxifloxacin≤24≥81–32163247053
 Metronidazole≤816≥ 320.5–42210000
 Tetracycline≤48≥ 160.25–320.532601327
Clostridium spp. (27)j
 Penicillin≤ 0.51≥2≤ 0.06–20.52741511
 Piperacillin-tazobactam≤ 3264≥ 128≤0.06–320.51610000
 Cefoxitin≤ 1632≥ 640.25–12826485411
 Cefotetan≤ 1632≥ 640.25– > 1284> 12878419
 Imipenem≤48≥ 160.25–8149640
 Clindamycin≤24≥8≤ 0.06– > 1281> 12863433
 Moxifloxacin≤24≥80.12–12813274719
 Metronidazole≤816≥ 320.25–64289307
 Tetracycline≤48≥ 160.12–641664261163
Actinomyces odontolyticus (34)
 Penicillin≤ 0.51≥2≤ 0.06–80.58531829
 Piperacillin-tazobactam≤ 3264≥ 1280.5–644329190
 Cefoxitin≤ 1632≥ 64≤0.06–321169730
 Cefotetan≤ 1632≥ 640.5–1288128651224
 Imipenem≤48≥ 16≤ 0.06–80.529730
 Clindamycin≤24≥8≤ 0.06– > 1280.5> 12862038
 Moxifloxacin≤24≥82–32229703
 Metronidazole≤816≥ 328– > 12832> 12862965
 Tetracycline≤48≥ 162–3221679021
Actinomyces spp. (23)ǁǁ
 Penicillin≤ 0.51≥2≤ 0.06–0.50.120.1210000
 Piperacillin-tazobactam≤ 3264≥ 128≤ 0.06–10.5110000
 Cefoxitin≤ 1632≥ 640.12–10.25110000
 Cefotetan≤ 1632≥ 64≤ 0.06–40.5410000
 Imipenem≤48≥ 16≤ 0.06–0.25≤ 0.060.2510000
 Clindamycin≤24≥8≤ 0.06– > 1280.25> 12878022
 Moxifloxacin≤24≥80.5–21210000
 Metronidazole≤816≥ 3232– > 128> 128> 12800100
 Tetracycline≤48≥ 160.5–6413278022
Bifidobacterium spp. (18)¶¶
 Penicillin≤ 0.51≥2≤ 0.06–40.124721117
 Piperacillin-tazobactam≤ 3264≥ 128≤0.06–320.121610000
 Cefoxitin≤ 1632≥ 64≤0.06–6416483017
 Cefotetan≤ 1632≥ 640.25– > 1282> 12872028
 Imipenem≤48≥ 16≤ 0.06–10.120.510000
 Clindamycin≤24≥8≤ 0.06– > 1280.5> 12872028
 Moxifloxacin≤24≥8≤0.06–16148966
 Metronidazole≤816≥ 320.5– > 1288> 128671122
 Tetracycline≤48≥ 162–12821683611
Eggerthella lenta (38)
 Penicillin≤ 0.51≥20.5–21284547
 Piperacillin-tazobactam≤ 3264≥ 12816–32163210000
 Cefoxitin≤ 1632≥ 642–328169550
 Cefotetan≤ 1632≥ 6432– > 128128> 1280595
 Imipenem≤48≥ 160.5–0.50.5110000
 Clindamycin≤24≥80.12–0.50.5> 12863037
 Moxifloxacin≤24≥80.12–4464472132
 Metronidazole≤816≥ 320.5–11110000
 Tetracycline≤48≥ 160.5–32326437361
Lactobacillus spp. (36)***
 Penicillin≤ 0.51≥2≤ 0.06– > 1280.52562222
 Piperacillin-tazobactam≤ 3264≥ 1280.5– > 128489406
 Cefoxitin≤ 1632≥ 644– > 128> 128> 12817381
 Cefotetan≤ 1632≥ 648– > 128> 128> 1283097
 Imipenem≤48≥ 16≤0.06–160.25886113
 Clindamycin≤24≥8≤ 0.06–10.120.510000
 Moxifloxacin≤24≥80.25–4129460
 Metronidazole≤816≥ 3232– > 128> 128> 12800100
 Tetracycline≤48≥ 160.5– > 128832443322
Other gram-positive bacilli (26)†††
 Penicillin≤ 0.51≥2≤ 0.06–40.120.259604
 Piperacillin-tazobactam≤ 3264≥ 128≤ 0.06–20.12210000
 Cefoxitin≤ 1632≥ 64≤0.06–161410000
 Cefotetan≤ 1632≥ 64≤0.06–32289640
 Imipenem≤48≥ 16≤ 0.06–0.5≤ 0.060.1210000
 Clindamycin≤24≥8≤0.06–64≤ 0.0648588
 Moxifloxacin≤24≥8≤ 0.06–40.2519640
 Metronidazole≤816≥ 320.25– > 1288> 12860040
 Tetracycline≤48≥ 160.25–82872280

*Susceptibility was determined by breakpoint according to the CLSI M100 27th edition [19]; Bacteroides thetaiotaomicron (N=26), B. caccae (N=9), B. uniformis (N=7), B. vulgatus (N=7), B. ovatus (N=5); B. intestinalis (N=4), B. nordii (N =3), B. pyogenes (N=2), B. stercoris (N=2), B. salyersiae (N=2), B. cellulosilyticus (N=1); §Parabacteroides goldsteinii (N=5), P. johnsonii (N=2), P. merdae (N=2), P. faecis (N=1); Prevotella buccae (N=15), P. bivia (N=10), P. nigrescens (N=3), P. buccalis (N=1), P. disiens (N=1), P. intermedia (N=1), P. melaninogenica (N=1), P. oralis (N=1); Fusobacterium varium (N=14), F. mortiferum (N=2), F. ulcerans (N=2), F. nucleatum (N=1); **Dialister pneumosintes (N=2), Leptotrichia trevisanii (N=2), L. buccalis (N=1), Alistipes finegoldii (N=1), A. onderdonkii (N=1), Bilophila sp. (N=1), Megamonas sp. (N=1), Sutterella wadsworthensis (N=1); ††Veillonella parvula (N=9), V. atypica (N=1), V. dispar (N=1); ‡‡Peptoniphilus anaerobius (N=3), P. asaccharolyticus (N=2), P. gorbachii (N=2), P. harei (N=1), Anaerococcus vaginalis (N=2), A. murdochii (N=1), A. prevotii (N=1), Ruminococcus gnavus (N=2); §§Clostridium bifermentans (N=3), C. hathewayi (N=3), C. innocuum (N=3), C. paraputrificum (N=3), C. perfringens (N=3), C. butyricum (N=2), C. ramosum (N=2), C. sordellii (N=2), C. tertium (N=2), C. cadaveris (N=1), C. scindens (N=1), C. sporogenes (N=1), C. bolteae (N=1); ∥∥Actinomyces oris (N=7), A. turicensis (N=7), A. neuii (N=4), A. viscosus (N =2), A. europaeus (N=1), A. meyeri (N=1), A. naeslundii (N=1); ¶¶Bifidobacterium dentium (N=5), B. longum (N=5), B. breve (N=4), B. bifidum (N=2), B. pseudocatenulatum (N=1), B. thermophilum (N=1); ***Lactobacillus paracasei (N=5), L. rhamnosus (N=5), L. sakei (N=5), L. salivarius (N=4), L. fermentum (N=3), L. mucosae (N=3), L. crispatus (N=2), L. gasseri (N=2), L. plantarum (N=2), L. reuteri (N=2), L. curvatus (N=1), L. harbinensis (N=1), L. sporogenes (N=1); †††Atopobium parvulum (N=7), A. rimae (N=2), Propionibacterium acnes (N=5), P. avidum (N=1), P. lymphophilum (N=1), Actinotignum schaalii (N=2), Alloscardovia omnicolens (N=2), Bulleidia extructa (N=2), Collinsella aerofaciens (N=2), Flavonifractor plautii (N=1), Slackia exigua (N=1).

Abbreviations: S, susceptible; I, intermediate; R, resistant; MIC, minimum inhibitory concentration.

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