Abstract
We determined the antimicrobial susceptibilities of 255 clinical isolates of anaerobic bacteria collected in 2007 and 2008 at a tertiary-care hospital in South Korea. Piperacillin-tazobactam, cefoxitin, imipenem, and meropenem were highly active β-lactam agents against most of the isolates tested. The rates of resistance of Bacteroides fragilis group organisms and anaerobic Gram-positive cocci to moxifloxacin were 11 to 18% and 0 to 27%, respectively.
Anaerobic bacterial resistance trends may vary greatly, depending on regions or institutions (1). The Clinical and Laboratory Standards Institute (CLSI) does not recommend routine susceptibility testing of all clinical isolates of anaerobic bacteria, except for the management of patients with serious infections (4). A recent survey indicated that only a few laboratories in the United States performed antimicrobial susceptibility testing of anaerobic bacteria due to the complex techniques and predictable susceptibilities involved (5). However, regional susceptibility patterns are pivotal in the empirical treatment of infected patients because these patterns are related to clinical outcomes (13). Therefore, periodic monitoring of the regional or institutional resistance trends of clinically important anaerobe isolates is recommended (4). Our investigation of resistance trends of Bacteroides fragilis group organisms from South Korea has been taking place since 1989 (9, 15). However, few studies have focused on the susceptibilities of other anaerobes. Therefore, the aim of this study was to determine the recent antimicrobial resistance patterns of frequently isolated anaerobes at a tertiary-care hospital in South Korea.
Anaerobes were isolated from blood, normally sterile body fluid, and abscess specimens, but Clostridium difficile was isolated from stool specimens of suspected C. difficile-associated disease patients at Severance Hospital in 2007 and 2008. The isolates were identified by either conventional methods (19) or the ATB 32A system (bioMérieux, Marcy l'Etoile, France). A total of 255 nonduplicated isolates were used in this study, including 63 of B. fragilis, 57 of other B. fragilis group species, 28 of Prevotella spp., 9 of other Gram-negative bacilli, 15 of Anaerococcus prevotii, 15 of Peptoniphilus asaccharolyticus, 15 of Finegoldia magna, 13 of Peptostreptococcus spp., 15 of C. perfringens, 12 of C. difficile, and 13 of other Gram-positive bacilli.
Antimicrobial susceptibility testing was performed using the CLSI agar dilution method (4). The medium used was Brucella agar (Becton Dickinson, Cockeysville, MD) supplemented with 5 μg hemin and 1 μg vitamin K1 per ml and 5% laked sheep blood. The antimicrobial powders used were piperacillin and tazobactam (Yuhan, Seoul, South Korea), cefoxitin (Merck Sharp & Dohme, West Point, PA), cefotetan (Daiichi Pharmaceutical, Tokyo, Japan), clindamycin (Korea Upjohn, Seoul, South Korea), imipenem, metronidazole (Choong Wae, Seoul, South Korea), chloramphenicol (Chong Kun Dang, Seoul, South Korea), meropenem (Sumitomo, Tokyo, Japan), moxifloxacin (Bayer Korea, Seoul, South Korea), and vancomycin (Eli Lilly & Co., Indianapolis, IN). For the combination of piperacillin and tazobactam, a constant tazobactam concentration of 4 μg/ml was added.
An inoculum of 105 CFU was applied with a Steers replicator (Craft Machine Inc., Woodline, PA), and the plates were incubated in an anaerobic chamber (Forma Scientific, Marietta, OH) for 48 h at 37°C. The MIC of each antimicrobial agent was defined as the concentration at which there was a marked reduction in growth, such as from confluent colonies to a haze, <10 tiny colonies, or 1 to 3 normal-sized colonies. B. fragilis ATCC 25285 and B. thetaiotaomicron ATCC 29741 were used as controls.
β-Lactamase production by anaerobic Gram-negative bacilli, with the exception of B. fragilis group organisms, was determined by applying test organisms to the Cefinase disks and recording the results after 30 min (Becton Dickinson, Cockeysville, MD).
Table 1 shows the MICs of antimicrobial agents and the resistance rates of the anaerobes tested. Among the 255 isolates, B. fragilis group organisms were the most prevalent (47%). These organisms are more virulent and more resistant to antimicrobial agents than most other anaerobes (3). In this study, piperacillin-tazobactam, cefoxitin, imipenem, and meropenem were highly active against B. fragilis group organisms, with resistance rates of less than 7%. The rates of resistance to imipenem and piperacillin-tazobactam were 4% and 7%, respectively, for other B. fragilis group organisms. However, much higher resistance rates were observed for piperacillin (27 to 51%), cefotetan (14 to 68%), and clindamycin (33 to 86%). These values were similar to those observed in 1997 to 2004 in the same hospital: piperacillin, 33 to 49%; cefotetan, 14 to 60%; clindamycin, 51 to 76% (15). A higher prevalence of resistance, in particular to clindamycin, was observed than in the United States, i.e.,19 to 35% (17). CLSI added a recommendation to test susceptibility to moxifloxacin in 2004 and 2007. In this study, the moxifloxacin resistance rates were 11% for B. fragilis and 18% for other B. fragilis group organisms. These rates were slightly higher than the 7 to 9% reported in Taiwan (11) but lower than those in Greece (14) and the United States (16 to 75% and 26 to 55%, respectively) (17).
TABLE 1.
Antimicrobial activities against 255 anaerobic bacteria isolated in 2007 to 2008
| Organism (no. of isolates) and antimicrobial agent | Breakpoint (μg/ml)a |
MIC (μg/ml) |
Susceptibility (%)a |
||||||
|---|---|---|---|---|---|---|---|---|---|
| S | I | R | Range | 50% | 90% | S | I | R | |
| Bacteroides fragilis (63) | |||||||||
| Piperacillin | ≤32 | 64 | ≥128 | 4->256 | 8 | >256 | 67 | 6 | 27 |
| Piperacillin-tazobactam | ≤32 | 64 | ≥128 | 0.25-128 | 1 | 4 | 97 | 2 | 2 |
| Cefoxitin | ≤16 | 32 | ≥64 | 8-128 | 16 | 32 | 79 | 16 | 5 |
| Cefotetan | ≤16 | 32 | ≥64 | 4->128 | 8 | 64 | 71 | 14 | 14 |
| Imipenem | ≤4 | 8 | ≥16 | 0.06-32 | 0.125 | 1 | 98 | 0 | 2 |
| Meropenem | ≤4 | 8 | ≥16 | 0.06-128 | 0.125 | 4 | 92 | 5 | 3 |
| Clindamycin | ≤2 | 4 | ≥8 | ≤0.06->128 | 0.5 | >128 | 67 | 0 | 33 |
| Moxifloxacin | ≤2 | 4 | ≥8 | 0.25->128 | 0.5 | 8 | 84 | 5 | 11 |
| Chloramphenicol | ≤8 | 16 | ≥32 | 2-16 | 4 | 4 | 98 | 2 | 0 |
| Metronidazole | ≤8 | 16 | ≥32 | 0.5-8 | 2 | 2 | 100 | 0 | 0 |
| B. fragilis group, other species (57)b | |||||||||
| Piperacillin | ≤32 | 64 | ≥128 | 8->256 | 128 | >256 | 42 | 7 | 51 |
| Piperacillin-tazobactam | ≤32 | 64 | ≥128 | 1->128 | 8 | 64 | 89 | 4 | 7 |
| Cefoxitin | ≤16 | 32 | ≥64 | 4->128 | 32 | 32 | 25 | 68 | 7 |
| Cefotetan | ≤16 | 32 | ≥64 | 4->128 | >128 | >128 | 89 | 5 | 86 |
| Imipenem | ≤4 | 8 | ≥16 | 0.13-32 | 0.5 | 4 | 95 | 2 | 4 |
| Meropenem | ≤4 | 8 | ≥16 | 0.13-8 | 0.25 | 2 | 98 | 2 | 0 |
| Clindamycin | ≤2 | 4 | ≥8 | 0.06->128 | >128 | >128 | 16 | 16 | 68 |
| Moxifloxacin | ≤2 | 4 | ≥8 | 0.13->128 | 2 | 16 | 72 | 10 | 18 |
| Chloramphenicol | ≤8 | 16 | ≥32 | 4-16 | 4 | 8 | 98 | 2 | 0 |
| Metronidazole | ≤8 | 16 | ≥32 | 0.5-4 | 2 | 2 | 100 | 0 | 0 |
| Prevotella intermedia (10) | |||||||||
| Piperacillin | ≤32 | 64 | ≥128 | 2-16 | 8 | 16 | 100 | 0 | 0 |
| Piperacillin-tazobactam | ≤32 | 64 | ≥128 | ≤0.03 | ≤0.03 | ≤0.03 | 100 | 0 | 0 |
| Cefoxitin | ≤16 | 32 | ≥64 | 0.5-4 | 2 | 4 | 100 | 0 | 0 |
| Cefotetan | ≤16 | 32 | ≥64 | 0.13-16 | 2 | 16 | 100 | 0 | 0 |
| Imipenem | ≤4 | 8 | ≥16 | 0.02-0.06 | 0.03 | 0.06 | 100 | 0 | 0 |
| Meropenem | ≤4 | 8 | ≥16 | 0.03-0.06 | 0.06 | 0.06 | 100 | 0 | 0 |
| Clindamycin | ≤2 | 4 | ≥8 | ≤0.06-2 | ≤0.06 | ≤0.06 | 100 | 0 | 0 |
| Moxifloxacin | ≤2 | 4 | ≥8 | 0.5 | 0.5 | 0.5 | 100 | 0 | 0 |
| Chloramphenicol | ≤8 | 16 | ≥32 | 0.5-1 | 0.5 | 1 | 100 | 0 | 0 |
| Metronidazole | ≤8 | 16 | ≥32 | 0.5-2 | 0.5 | 2 | 100 | 0 | 0 |
| Prevotella spp. (18)c | |||||||||
| Piperacillin | ≤32 | 64 | ≥128 | 0.5-256 | 16 | 128 | 78 | 11 | 11 |
| Piperacillin-tazobactam | ≤32 | 64 | ≥128 | ≤0.03-16 | ≤0.03 | 4 | 100 | 0 | 0 |
| Cefoxitin | ≤16 | 32 | ≥64 | 0.5-32 | 1 | 32 | 89 | 11 | 0 |
| Cefotetan | ≤16 | 32 | ≥64 | 0.5-64 | 4 | 64 | 72 | 11 | 17 |
| Imipenem | ≤4 | 8 | ≥16 | 0.03-1 | 0.06 | 0.5 | 100 | 0 | 0 |
| Meropenem | ≤4 | 8 | ≥16 | 0.03-1 | 0.125 | 0.5 | 100 | 0 | 0 |
| Clindamycin | ≤2 | 4 | ≥8 | ≤0.06-128 | ≤0.06 | 128 | 50 | 0 | 50 |
| Moxifloxacin | ≤2 | 4 | ≥8 | 0.5-16 | 2 | 8 | 56 | 33 | 11 |
| Chloramphenicol | ≤8 | 16 | ≥32 | 0.5-8 | 4 | 8 | 100 | 0 | 0 |
| Metronidazole | ≤8 | 16 | ≥32 | 0.5-8 | 4 | 8 | 100 | 0 | 0 |
| Other Gram-negative bacilli (9)d | |||||||||
| Piperacillin | ≤32 | 64 | ≥128 | 0.06-32 | NAg | NA | NA | NA | NA |
| Piperacillin-tazobactam | ≤32 | 64 | ≥128 | ≤0.03-4 | NA | NA | NA | NA | NA |
| Cefoxitin | ≤16 | 32 | ≥64 | ≤0.06-8 | NA | NA | NA | NA | NA |
| Cefotetan | ≤16 | 32 | ≥64 | ≤0.06-8 | NA | NA | NA | NA | NA |
| Imipenem | ≤4 | 8 | ≥16 | 0.02-4 | NA | NA | NA | NA | NA |
| Meropenem | ≤4 | 8 | ≥16 | ≤0.008-4 | NA | NA | NA | NA | NA |
| Clindamycin | ≤2 | 4 | ≥8 | ≤0.06-128 | NA | NA | NA | NA | NA |
| Moxifloxacin | ≤2 | 4 | ≥8 | 0.25-128 | NA | NA | NA | NA | NA |
| Chloramphenicol | ≤8 | 16 | ≥32 | 0.13-4 | NA | NA | NA | NA | NA |
| Metronidazole | ≤8 | 16 | ≥32 | 0.13-1 | NA | NA | NA | NA | NA |
| Peptostreptococcus spp. (13)e | |||||||||
| Piperacillin | ≤32 | 64 | ≥128 | 0.06-16 | 0.25 | 16 | 100 | 0 | 0 |
| Piperacillin-tazobactam | ≤32 | 64 | ≥128 | ≤0.03-16 | 0.25 | 16 | 100 | 0 | 0 |
| Cefoxitin | ≤16 | 32 | ≥64 | 0.25-16 | 1 | 16 | 100 | 0 | 0 |
| Cefotetan | ≤16 | 32 | ≥64 | ≤0.06-128 | 4 | 64 | 62 | 8 | 31 |
| Imipenem | ≤4 | 8 | ≥16 | ≤0.008-4 | 0.125 | 2 | 100 | 0 | 0 |
| Meropenem | ≤4 | 8 | ≥16 | 0.01-4 | 0.25 | 4 | 100 | 0 | 0 |
| Clindamycin | ≤2 | 4 | ≥8 | ≤0.06-128 | 0.125 | 64 | 77 | 0 | 23 |
| Moxifloxacin | ≤2 | 4 | ≥8 | ≤0.06-8 | 0.125 | 0.25 | 92 | 0 | 8 |
| Chloramphenicol | ≤8 | 16 | ≥32 | 1-2 | 2 | 2 | 100 | 0 | 0 |
| Metronidazole | ≤8 | 16 | ≥32 | 0.25-1 | 0.5 | 1 | 100 | 0 | 0 |
| Anaerococcus prevotii (15) | |||||||||
| Piperacillin | ≤32 | 64 | ≥128 | ≤0.06-0.5 | 0.125 | 0.25 | 100 | 0 | 0 |
| Piperacillin-tazobactam | ≤32 | 64 | ≥128 | ≤0.03-1 | 0.125 | 0.125 | 100 | 0 | 0 |
| Cefoxitin | ≤16 | 32 | ≥64 | ≤0.06-4 | 0.5 | 1 | 100 | 0 | 0 |
| Cefotetan | ≤16 | 32 | ≥64 | ≤0.06-4 | 1 | 2 | 100 | 0 | 0 |
| Imipenem | ≤4 | 8 | ≥16 | ≤0.008-0.25 | 0.06 | 0.25 | 100 | 0 | 0 |
| Meropenem | ≤4 | 8 | ≥16 | ≤0.008-0.25 | 0.06 | 0.125 | 100 | 0 | 0 |
| Clindamycin | ≤2 | 4 | ≥8 | ≤0.06-128 | 2 | 128 | 60 | 0 | 40 |
| Moxifloxacin | ≤2 | 4 | ≥8 | ≤0.06-8 | 0.25 | 8 | 87 | 0 | 13 |
| Chloramphenicol | ≤8 | 16 | ≥32 | 1-16 | 4 | 8 | 93 | 7 | 0 |
| Metronidazole | ≤8 | 16 | ≥32 | 0.25-1 | 1 | 1 | 100 | 0 | 0 |
| Peptoniphilus asaccharolyticus (15) | |||||||||
| Piperacillin | ≤32 | 64 | ≥128 | ≤0.06-0.25 | ≤0.06 | ≤0.06 | 100 | 0 | 0 |
| Piperacillin-tazobactam | ≤32 | 64 | ≥128 | ≤0.03-0.25 | ≤0.03 | 0.06 | 100 | 0 | 0 |
| Cefoxitin | ≤16 | 32 | ≥64 | ≤0.06-1 | ≤0.06 | 0.5 | 100 | 0 | 0 |
| Cefotetan | ≤16 | 32 | ≥64 | 0.13-2 | 0.25 | 1 | 100 | 0 | 0 |
| Imipenem | ≤4 | 8 | ≥16 | ≤0.008-0.13 | ≤0.008 | 0.03 | 100 | 0 | 0 |
| Meropenem | ≤4 | 8 | ≥16 | ≤0.008-0.06 | ≤0.008 | 0.03 | 100 | 0 | 0 |
| Clindamycin | ≤2 | 4 | ≥8 | ≤0.06-32 | 0.125 | 32 | 67 | 0 | 33 |
| Moxifloxacin | ≤2 | 4 | ≥8 | 0.13-2 | 0.25 | 2 | 100 | 0 | 0 |
| Chloramphenicol | ≤8 | 16 | ≥32 | 1-4 | 2 | 4 | 100 | 0 | 0 |
| Metronidazole | ≤8 | 16 | ≥32 | 0.5-2 | 1 | 1 | 100 | 0 | 0 |
| Finegoldia magna (15) | |||||||||
| Piperacillin | ≤32 | 64 | ≥128 | ≤0.06-0.25 | ≤0.06 | 0.125 | 100 | 0 | 0 |
| Piperacillin-tazobactam | ≤32 | 64 | ≥128 | ≤0.03-0.25 | 0.06 | 0.125 | 100 | 0 | 0 |
| Cefoxitin | ≤16 | 32 | ≥64 | ≤0.06-1 | 0.5 | 1 | 100 | 0 | 0 |
| Cefotetan | ≤16 | 32 | ≥64 | 0.12-4 | 1 | 2 | 100 | 0 | 0 |
| Imipenem | ≤4 | 8 | ≥16 | ≤0.008-0.13 | 0.06 | 0.125 | 100 | 0 | 0 |
| Meropenem | ≤4 | 8 | ≥16 | 0.03-0.13 | 0.06 | 0.125 | 100 | 0 | 0 |
| Clindamycin | ≤2 | 4 | ≥8 | ≤0.06-128 | 0.25 | 64 | 73 | 13 | 13 |
| Moxifloxacin | ≤2 | 4 | ≥8 | 0.13-32 | 0.5 | 8 | 60 | 13 | 27 |
| Chloramphenicol | ≤8 | 16 | ≥32 | 2-4 | 4 | 4 | 100 | 0 | 0 |
| Metronidazole | ≤8 | 16 | ≥32 | 0.5-1 | 0.5 | 1 | 100 | 0 | 0 |
| Clostridium perfringens (15) | |||||||||
| Piperacillin | ≤32 | 64 | ≥128 | ≤0.06-0.5 | 0.25 | 0.5 | 100 | 0 | 0 |
| Piperacillin-tazobactam | ≤32 | 64 | ≥128 | ≤0.03-1 | 0.25 | 0.5 | 100 | 0 | 0 |
| Cefoxitin | ≤16 | 32 | ≥64 | 0.5-2 | 1 | 2 | 100 | 0 | 0 |
| Cefotetan | ≤16 | 32 | ≥64 | ≤0.06-1 | 0.25 | 1 | 100 | 0 | 0 |
| Imipenem | ≤4 | 8 | ≥16 | 0.03-0.25 | 0.125 | 0.125 | 100 | 0 | 0 |
| Meropenem | ≤4 | 8 | ≥16 | ≤0.008-0.03 | 0.015 | 0.015 | 100 | 0 | 0 |
| Clindamycin | ≤2 | 4 | ≥8 | ≤0.06-128 | 2 | 4 | 80 | 13 | 7 |
| Moxifloxacin | ≤2 | 4 | ≥8 | 0.25-16 | 0.5 | 0.5 | 93 | 0 | 7 |
| Chloramphenicol | ≤8 | 16 | ≥32 | 2-8 | 4 | 4 | 100 | 0 | 0 |
| Metronidazole | ≤8 | 16 | ≥32 | 0.02-0.06 | 0.03 | 0.06 | 100 | 0 | 0 |
| Vancomycin | NA | NA | NA | 0.25-1 | 0.5 | 0.5 | NA | NA | NA |
| Clostridium difficile (12) | |||||||||
| Piperacillin | ≤32 | 64 | ≥128 | 2-8 | 4 | 8 | 100 | 0 | 0 |
| Piperacillin-tazobactam | ≤32 | 64 | ≥128 | 1-16 | 4 | 8 | 100 | 0 | 0 |
| Cefoxitin | ≤16 | 32 | ≥64 | 64->128 | 64 | >128 | 0 | 0 | 100 |
| Cefotetan | ≤16 | 32 | ≥64 | 8-128 | 8 | 128 | 83 | 0 | 17 |
| Imipenem | ≤4 | 8 | ≥16 | 0.25-16 | 4 | 8 | 58 | 33 | 8 |
| Meropenem | ≤4 | 8 | ≥16 | 0.25-2 | 2 | 2 | 100 | 0 | 0 |
| Clindamycin | ≤2 | 4 | ≥8 | 2-128 | 64 | 128 | 8 | 8 | 83 |
| Moxifloxacin | ≤2 | 4 | ≥8 | 1->128 | 16 | 32 | 25 | 0 | 75 |
| Chloramphenicol | ≤8 | 16 | ≥32 | 1-16 | 4 | 16 | 83 | 17 | 0 |
| Metronidazole | ≤8 | 16 | ≥32 | 0.5-2 | 1 | 1 | 100 | 0 | 0 |
| Vancomycin | NA | NA | NA | 0.25-2 | 0.5 | 2 | NA | NA | NA |
| Other Gram-positive bacilli (13)f | |||||||||
| Piperacillin | ≤32 | 64 | ≥128 | ≤0.06-64 | 1 | 8 | 92 | 8 | 0 |
| Piperacillin-tazobactam | ≤32 | 64 | ≥128 | ≤0.03-64 | 0.5 | 8 | 92 | 8 | 0 |
| Cefoxitin | ≤16 | 32 | ≥64 | 0.13-32 | 2 | 16 | 92 | 8 | 0 |
| Cefotetan | ≤16 | 32 | ≥64 | 0.13->128 | 4 | 64 | 85 | 0 | 15 |
| Imipenem | ≤4 | 8 | ≥16 | ≤0.008-2 | 0.06 | 0.5 | 100 | 0 | 0 |
| Meropenem | ≤4 | 8 | ≥16 | ≤0.008-16 | 0.125 | 2 | 92 | 0 | 8 |
| Clindamycin | ≤2 | 4 | ≥8 | ≤0.06->128 | 0.06 | >128 | 85 | 0 | 15 |
| Moxifloxacin | ≤2 | 4 | ≥8 | ≤0.06-4 | 1 | 2 | 92 | 8 | 0 |
| Chloramphenicol | ≤8 | 16 | ≥32 | 1-16 | 1 | 2 | 92 | 8 | 0 |
| Metronidazole | ≤8 | 16 | ≥32 | 0.5->128 | 16 | >128 | 46 | 8 | 46 |
S, susceptible; I, intermediate; R, resistant.
Bacteroides thetaiotaomicron (n = 25), B. caccae (n = 3), B. distasonis (n = 9), B. ovatus (n = 8), and B. vulgatus (n = 12).
Prevotella bivia (n = 10), P. buccae (n = 5), and P. oralis (n = 3).
Porphyromonas asaccharolytica (n = 2), Fusobacterium varium (n = 3), F. necrogenes (n = 2), F. nucleatum (n = 1), and F. mortiferum (n = 1).
Peptostreptococcus anaerobius (n = 9) and P. micros (n = 4).
Acitnomyces odontolyticus (n = 3), A. israelii (n = 2), A. meyeri (n = 1), A. naeslundii (n = 1), Bifidobacterium adolescentis (n = 3), Bifidobacterium sp. (n = 1), Eubacterium lentum (n = 1), and Eubacterium sp. (n = 1).
NA, not available/not applicable.
Overall, Prevotella, Porphyromonas, and Fusobacterium isolates are more susceptible than B. fragilis group organisms (7). Among these organisms, β-lactamase producers were resistant to penicillin and ampicillin (3, 7). A recent study showed that 94% of the Prevotella isolates tested were β-lactamase producers, which correlated well with susceptibility to penicillin (11). In the present study, β-lactamase production was detected in 26 Prevotella isolates (94%) and 1 Fusobacterium isolate (14%). While 50% of the non-P. intermedia Prevotella isolates were resistant to clindamycin, all of the P. intermedia isolates were susceptible to clindamycin. Other studies indicated that 17% and 36% of the P. intermedia isolates were resistant to clindamycin (8, 16).
Anaerobic Gram-positive cocci account for approximately one-quarter of all isolates from anaerobic infections. They may cause various infections, including skin infections, necrotizing pneumonia, and bacteremia (18). Several species previously placed in the genus Peptostreptococcus have been reclassified into new genera, including Anaerococcus, Finegoldia, Micrococcus, and Peptoniphilus (7). These organisms exhibited various rates of resistance to penicillin, clindamycin, and metronidazole (7). A European surveillance study showed that the majority of the isolates found to be resistant to clindamycin and penicillin were identified as F. magna (2). In our study, the rates of resistance of Gram-positive cocci to clindamycin and moxifloxacin varied according to species. The highest clindamycin resistance observed was 40% of A. prevotii isolates, followed by 33% of P. asaccharolyticus isolates. These rates were much higher than those reported in Europe (4%) and the United States (8%) (1, 2) but similar to the 25.9% observed in 1994 in South Korea (10). The rates of resistance to moxifloxacin varied from 27% among F. magna isolates to 0% among P. asaccharolyticus isolates. The difference in resistance rates among anaerobic Gram-positive cocci may be of importance. The resistance patterns of these organisms could help in the selection of appropriate antimicrobial treatment options, although susceptibility testing of individual patient isolates is not performed.
C. perfringens is generally very susceptible to most antibiotics (7). The present study showed that all of the antimicrobial agents tested had high activity against this organism. C. difficile has highly variable resistance to β-lactams, including penicillin, cephalosporins, imipenem, clindamycin, and moxifloxacin (6, 7). In our study, the rates of resistance to cefoxitin, clindamycin, and moxifloxacin were 100%, 85%, and 77%, respectively. The C. difficile NAP1/027 epidemic isolates were known to be resistant to moxifloxacin (12). A high rate of resistance to moxifloxacin was observed in this study, although none of the isolates were NAP1/027 strains. Other Gram-positive bacilli, such as Actinomyces, Bifidobacterium, and Eubacterium species, are generally susceptible to β-lactams, including penicillin. Metronidazole-resistant isolates were common among these organisms (3). In our study, 46% of these organisms were resistant to metronidazole.
In conclusion, piperacillin-tazobactam, cefoxitin, imipenem, meropenem, metronidazole, and chloramphenicol remain active against most anaerobic isolates. The rates of resistance of Gram-positive cocci to clindamycin and moxifloxacin are variable according to species. The rates of resistance to moxifloxacin are as follows: C. difficile, 75%; anaerobic Gram-positive cocci, 0 to 27%; B. fragilis group organisms, 11 to 18%. Continuous monitoring is necessary to detect pattern changes at regional centers.
Acknowledgments
This study was supported by a grant from the Korea Healthcare Technology R&D Project, Ministry for Health, Welfare & Family Affairs, Republic of Korea (A080504).
Footnotes
Published ahead of print on 28 June 2010.
REFERENCES
- 1.Aldridge, K. E., D. Ashcraft, K. Cambre, C. L. Pierson, S. G. Jenkins, and J. E. Rosenblatt. 2001. Multicenter survey of the changing in vitro antimicrobial susceptibilities of clinical isolates of Bacteroides fragilis group, Prevotella, Fusobacterium, Porphyromonas, and Peptostreptococcus species. Antimicrob. Agents Chemother. 45:1238-1243. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.Brazier, J., D. Chmelar, L. Dubreuil, G. Feierl, M. Hedberg, S. Kalenic, E. Kononen, B. Lundgren, H. Malamou-Ladas, E. Nagy, A. Sullivan, and C. E. Nord. 2008. European surveillance study on antimicrobial susceptibility of Gram-positive anaerobic cocci. Int. J. Antimicrob. Agents 31:316-320. [DOI] [PubMed] [Google Scholar]
- 3.Citron, D. M., I. R. Poxton, and E. J. Baron. 2007. Bacteroides, Porphyromonas, Prevotella, Fusobacterium, and other anaerobic gram-negative rods, p. 911-932. In P. R. Murray, E. J. Baron, J. H. Jorgensen, M. L. Landry, and M. A. Pfaller (ed.), Manual of clinical microbiology, 9th ed. ASM Press, Washington, DC.
- 4.Clinical and Laboratory Standards Institute. 2007. Methods for antimicrobial susceptibility testing of anaerobic bacteria. Approved standard M11-A7, 7th ed. Clinical and Laboratory Standards Institute, Wayne, PA.
- 5.Goldstein, E. J., D. M. Citron, P. J. Goldman, and R. J. Goldman. 2008. National hospital survey of anaerobic culture and susceptibility methods: III. Anaerobe 14:68-72. [DOI] [PubMed] [Google Scholar]
- 6.Goldstein, E. J., D. M. Citron, C. V. Merriam, Y. A. Warren, K. L. Tyrrell, and H. T. Fernandez. 2008. In vitro activities of doripenem and six comparator drugs against 423 aerobic and anaerobic bacterial isolates from infected diabetic foot wounds. Antimicrob. Agents Chemother. 52:761-766. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Hecht, D. W. 2006. Anaerobes: antibiotic resistance, clinical significance, and the role of susceptibility testing. Anaerobe 12:115-121. [DOI] [PubMed] [Google Scholar]
- 8.Lakhssassi, N., N. Elhajoui, J. P. Lodter, J. L. Pineill, and M. Sixou. 2005. Antimicrobial susceptibility variation of 50 anaerobic periopathogens in aggressive periodontitis: an interindividual variability study. Oral Microbiol. Immunol. 20:244-252. [DOI] [PubMed] [Google Scholar]
- 9.Lee, K., H. B. Shin, and Y. Chong. 1998. Antimicrobial resistance patterns of Bacteroides fragilis group organisms in Korea. Yonsei Med. J. 39:578-586. [DOI] [PubMed] [Google Scholar]
- 10.Lee, K., Y. Chong, S. H. Jeong, X. S. Xu, and O. H. Kwon. 1996. Emerging resistance of anaerobic bacteria to antimicrobial agents in South Korea. Clin. Infect. Dis. 23(Suppl. 1):S73-S77. [DOI] [PubMed] [Google Scholar]
- 11.Liu, C. Y., Y. T. Huang, C. H. Liao, L. C. Yen, H. Y. Lin, and P. R. Hsueh. 2008. Increasing trends in antimicrobial resistance among clinically important anaerobes and Bacteroides fragilis isolates causing nosocomial infections: emerging resistance to carbapenems. Antimicrob. Agents Chemother. 52:3161-3168. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.McDonald, L. C., G. E. Killgore, A. Thompson, R. C. Owens, Jr., S. V. Kazakova, S. P. Sambol, S. Johnson, and D. N. Gerding. 2005. An epidemic, toxin gene-variant strain of Clostridium difficile. N. Engl. J. Med. 353:2433-2441. [DOI] [PubMed] [Google Scholar]
- 13.Nguyen, M. H., V. L. Yu, A. J. Morris, L. McDermott, M. W. Wagener, L. Harrell, and D. R. Snydman. 2000. Antimicrobial resistance and clinical outcome of Bacteroides bacteremia: findings of a multicenter prospective observational trial. Clin. Infect. Dis. 30:870-876. [DOI] [PubMed] [Google Scholar]
- 14.Papaparaskevas, J., A. Pantazatou, A. Katsandri, D. P. Houhoula, N. J. Legakis, A. Tsakris, and A. Avlamis. 2008. Moxifloxacin resistance is prevalent among Bacteroides and Prevotella species in Greece. J. Antimicrob. Chemother. 62:137-141. [DOI] [PubMed] [Google Scholar]
- 15.Roh, K. H., S. Kim, C. K. Kim, J. H. Yum, M. S. Kim, D. Yong, K. Lee, J. M. Kim, and Y. Chong. 2009. Resistance trends of Bacteroides fragilis group over an 8-year period, 1997-2004, in Korea. Korean J. Lab. Med. 29:293-298. [DOI] [PubMed] [Google Scholar]
- 16.Santos, F. A., E. M. Bastos, P. H. Rodrigues, M. de Uzeda, M. A. de Carvalho, M. Farias Lde, and E. S. Moreira. 2002. Susceptibility of Prevotella intermedia/Prevotella nigrescens (and Porphyromonas gingivalis) to propolis (bee glue) and other antimicrobial agents. Anaerobe 8:9-15. [DOI] [PubMed] [Google Scholar]
- 17.Snydman, D. R., N. V. Jacobus, L. A. McDermott, R. Ruthazer, Y. Golan, E. J. Goldstein, S. M. Finegold, L. J. Harrell, D. W. Hecht, S. G. Jenkins, C. Pierson, R. Venezia, V. Yu, J. Rihs, and S. L. Gorbach. 2007. National survey on the susceptibility of Bacteroides fragilis group: report and analysis of trends in the United States from 1997 to 2004. Antimicrob. Agents Chemother. 51:1649-1655. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Song, Y., and S. M. Finegold. 2007. Peptostreptococcus, Finegoldia, Anaerococcus, Peptoniphilus, Veillonella, and other anaerobic cocci, p. 862-871. In P. R. Murray, E. J. Baron, J. H. Jorgensen, M. L. Landry, and M. A. Pfaller (ed.), Manual of clinical microbiology, 9th ed. ASM Press, Washington, DC.
- 19.Summanen, P., E. J. Baron, D. M. Citron, C. Strong, H. M. Wexler, and S. M. Finegold. 1993. Wadsworth anaerobic bacteriology manual, 5th ed. Star Publishing, Belmont, CA.