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Antibiotic susceptibility of Atopobium vaginae
© De Backer et al; licensee BioMed Central Ltd. 2006
Received: 20 November 2005
Accepted: 16 March 2006
Published: 16 March 2006
Previous studies have indicated that a recently described anaerobic bacterium, Atopobium vaginae is associated with bacterial vaginosis (BV). Thus far the four isolates of this fastidious micro-organism were found to be highly resistant to metronidazole and susceptible for clindamycin, two antibiotics preferred for the treatment of BV.
Nine strains of Atopobium vaginae, four strains of Gardnerella vaginalis, two strains of Lactobacillus iners and one strain each of Bifidobacterium breve, B. longum, L. crispatus, L. gasseri and L. jensenii were tested against 15 antimicrobial agents using the Etest.
All nine strains of A. vaginae were highly resistant to nalidixic acid and colistin while being inhibited by low concentrations of clindamycin (range: < 0.016 μg/ml), rifampicin (< 0.002 μg/ml), azithromycin (< 0.016 – 0.32 μg/ml), penicillin (0.008 – 0.25 μg/ml), ampicillin (< 0.016 – 0.94 μg/ml), ciprofloxacin (0.023 – 0.25 μg/ml) and linezolid (0.016 – 0.125 μg/ml). We found a variable susceptibility for metronidazole, ranging from 2 to more than 256 μg/ml. The four G. vaginalis strains were also susceptible for clindamycin (< 0.016 – 0.047 μg/ml) and three strains were susceptible to less than 1 μg/ml of metronidazole. All lactobacilli were resistant to metronidazole (> 256 μg/ml) but susceptible to clindamycin (0.023 – 0.125 μg/ml).
Clindamycin has higher activity against G. vaginalis and A. vaginae than metronidazole, but not all A. vaginae isolates are metronidazole resistant, as seemed to be a straightforward conclusion from previous studies on a more limited number of strains.
Bacterial vaginosis is considered a common vaginal disorder in women of reproductive age. Whereas normal vaginal microflora consists of lactobacilli, especially L. crispatus [1–4], the disturbed vaginal microflora is characterized by the overgrowth of Gardnerella vaginalis and anaerobic bacteria such as Mobiluncus spp., Mycoplasma hominis and Prevotella spp. Recently several research groups showed – by means of cloning of the 16S rRNA-gene [3, 5], by Terminal Restriction Fragment Length Polymorphism analysis of the 16S rRNA gene (T-RFLP) [6, 7], by specific PCR [5, 8, 9], by Denaturing Gradient Gel Electrophoresis of the 16S rRNA gene (DGGE)  and by FISH [3, 11] – that a previously unrecognized organism, Atopobium vaginae, was strongly associated with bacterial vaginosis and with Gardnerella vaginalis.
During the last decade, the interest for bacterial vaginosis increased because of reports of adverse sequelae of this disorder, such as preterm birth [12–14], pelvic inflammatory disease [15, 16] and postpartum endometritis . In addition, several publications showed that an altered vaginal microflora is linked to an increased susceptibility to the acquisition of HIV [18, 19] and other sexually transmitted infectious agents such as Neisseria gonorrhoeae and Chlamydia trachomatis [18, 20].
The severity of the consequences of such sequelae asks for an adequate treatment of bacterial vaginosis. Currently the preferred antibiotic treatment regimen consists of clindamycin or metronidazole (oral or intravaginal). Recurrence rates of up to 30% within 3 months after treatment have been reported [21, 22]. This recurrence might be due to the survival of metronidazole or clindamycin resistant bacteria in the vagina, although Beigi et al.  showed recently that less than one percent of the cultivable vaginal anaerobic bacteria is resistant to metronidazole.
Another possible explanation might be the presence of some fastidious to unculturable, metronidazole resistant organism, a role for which A. vaginae is a likely candidate, since Geißdörfer et al.  and Ferris et al.  reported an MIC of > 32 μg/ml for metronidazole for the four isolates that were tested.
Here, we studied the susceptibility of nine other A. vaginae isolates for 15 antimicrobial agents by using the Etest and for comparison we included a limited number of other important vaginal bacteria such as lactobacilli, G. vaginalis and bifidobacteria and we compared our results with those of previously published articles.
Nine strains of Atopobium vaginae, four strains of Gardnerella vaginalis, two strains of Lactobacillus iners and one strain each of Bifidobacterium breve, B. longum, Lactobacillus crispatus, L. gasseri and L. jensenii were tested against 15 antibiotics (ampicillin, azithromycin, bacitracin, cefuroxime, ciprofloxacin, clindamycin, colistin, doxycycline, kanamycin, linezolid, metronidazole, nalidixic acid, penicillin, rifampicin and vancomycin) [see Additional file 1]. Six strains of A. vaginae (CCUG 42099, CCUG 44116, CCUG 44258, CCUG 38953T, CCUG 44125, CCUG 44061) were kindly provided by the Culture Collection of Göteborg (Sweden). The other strains were obtained from studies by cultivating vaginal samples (with informed consent) and identified by tDNA-PCR and 16S rRNA gene sequencing .
Strains were cultivated anaerobically using the GasPak anaerobic envelope system (Becton Dickinson, Erembodegem, Belgium) at 37°C on Trypticase Soy Agar (TSA) + 5 % sheep blood (Becton Dickinson). Epsilometer tests (Etest AB Biodisk, Solna, Sweden) were used to determine the minimal inhibitory concentrations (MIC). An inoculum taken from TSA + 5% sheep blood was suspended in 0.5 ml of physiological water and adjusted to the turbidity of a 1 McFarland standard. Before inoculating the plates and testing for metronidazole, plates were anaerobically incubated during 24 h. After application of the epsilometer, test plates were anaerobically incubated at 37°C. The inhibitory concentration was defined as the value on the test strip scale at which the inhibition zone intersected the strip edge, according to the manufacturers' instructions. MIC-values were read after 48 h for G. vaginalis, Lactobacillus spp. and Bifidobacterium spp. and after 72 h for A. vaginae.
Results and discussion
Value and reproducibility of Etest for MIC-determination of anaerobes
In this study we used the Etest for MIC-determination of vaginal bacteria towards 15 antibiotics. Croco et al.  concluded, from a study whereby the Etest was compared with the reference agar dilution method, that the Etest was a quantitatively accurate and reproducible method for routinely testing the antimicrobial susceptibilities of anaerobes, in particular of organisms associated with BV. Discordances were reported only for clindamycin susceptibility testing of lactobacilli and chloramphenicol susceptibility testing of the Bacteroides fragilis group. Schieven et al.  reported an agreement between the Etest and the reference agar dilution method within 1 log2 dilution of 87.4% for clindamycin and 85.1% for metronidazole for a total of 150 anaerobic isolates tested.
Antimicrobial susceptibility testing of Atopobium vaginae
The antibiotic susceptibility for ampicillin, azithromycin, bacitracin, cefuroxime, ciprofloxacin, clindamycin, colistin, doxycycline, kanamycin, linezolid, metronidazole, nalidixic acid, penicillin, rifampicin and vancomycin obtained for nine Atopobium vaginae isolates in this study is listed in additional file 1 [see Additional file 1].
Comparison of MIC-values as determined for Atopobium vaginae by Ferris et al.  and Geißdörfer et al.  and in this study.
Geißdörfer et al.  a
Ferris et al.  b
Number of strains
< 0.016 – 0.94
0.06 – 0.25
< 0.016 – 0.32
1 – 4
0.5 – 2
0.016 – 0.25
0.023 – 0.25
0.19 – 0.75
< 0.015 – 0.5
8 – 16
0.016 – 0.125
0.06 – 0.25
< 0.015 – 0.5
2 - > 256
0.06 – 1
0.008 – 0.25
< 0.015 – 2
1 – 4
We previously described the existence of a second genotype within A. vaginae. To this genotype belongs isolate PB2003/189-T1-4, of which the 16S rRNA gene sequence differs at 23 positions compared to the type strain, but is identical to that of an isolate no longer in our collection of which the sequence was submitted [Genbank: AJ585206] . This genotype 2 isolate showed a marked difference only for azithromycin (i.e. MIC of 0.32 μg/ml) with the other isolates (MIC of < 0.016 μg/ml).
Antimicrobial susceptibility testing of Gardnerella vaginalis
We tested 4 strains of Gardnerella vaginalis. By using the Etest method in an anaerobic environment we found in general slightly lower values for ampicillin (range: < 0.016 – 0.047 μg/ml), penicillin (0.004 – 0.047 μg/ml), cefuroxim (< 0.016 – 0.125 μg/ml) and rifampicin (0.5 – 0.75 μg/ml) (Table 1), compared to other publications [25, 27, 28] [see Additional file 2]. The range of the MIC-values of Gardnerella vaginalis for clindamycin (range: < 0.016 – 0.047 μg/ml), colistin (> 1024 μg/ml), doxycycline (0.25 – 32 μg/ml), kanamycin (16 – 32 μg/ml), metronidazole (0.75 – 16 μg/ml), nalidixic acid (> 256 μg/ml) and vancomycin (0.125 – 0.38 μg/ml) is comparable with other studies [25, 27–31] [see Additional file 2]. G. vaginalis is, according to NCCLS standards for anaerobic bacteria, susceptible to ampicillin (range: < 0.016 – 0.047 μg/ml), penicillin (0.004 – 0.047 μg/ml) and azithromycin (< 0.016 – 0.047 μg/ml). In 1993, Goldstein et al.  reported that 20% of G. vaginalis strains were resistant to metronidazole (MIC ≥ 16 μg/ml). In 2002, the same group reported a resistance of 29% to metronidazole for G. vaginalis . All four strains in our study were susceptible.
Antimicrobial susceptibility testing of Lactobacillusspp
Most of the Lactobacillus spp. we tested show a low MIC-value for ampicillin (range for all lactobacilli: 0.064 – 0.5 μg/ml), azithromycin (0.023 – 0.125 μg/ml), cefuroxim (< 0.016 – 1 μg/ml), linezolid (0.19 – 1.5 μg/ml), penicillin (0.047 – 0.19 μg/ml), rifampicin (0.016 – 2 μg/ml) and vancomycin (0.38 – 1 μg/ml) [see Additional file 1]. All strains were resistant to metronidazole (range for all lactobacilli: > 256 μg/ml). The strains of the species L. crispatus, L. jensenii and L. gasseri were all highly resistant to ciprofloxacin (range: > 32 μg/ml) in contrast to both L. iners strains (range: 0.25 – 0.38 μg/ml).
The single strain of L. crispatus tested yielded a very low MIC-value for clindamycin (< 0.016 μg/ml) and a high MIC-value for rifampicin compared to the other lactobacilli. The strain of L. gasseri tested showed comparable results to those of previous publications [32, 33] for clindamycin, metronidazole, penicillin and vancomycin [see Additional file 2], indicating that this species is much more resistant to clindamycin than L. crispatus.
All lactobacilli were resistant to metronidazole (> 256 μg/ml) but susceptible for clindamycin (0.023 – 0.125 μg/ml). There were no literature data to compare the susceptibility of L. iners and L. jensenii for the antimicrobial agents tested in this study.
Antimicrobial susceptibility testing of Bifidobacteriumspp
Both of the tested Bifidobacterium strains are sensitive to a low amount of ampicillin (B. longum: 0.25 μg/ml, B. breve: 0.38 μg/ml), azithromycin (B. longum: 0.064 μg/ml, B. breve: 0.25 μg/ml), clindamycin (B. breve and B. longum: < 0.016 μg/ml), linezolid (B. longum: 0.25 μg/ml, B. breve: 0.38 μg/ml), penicillin (B. longum: 0.19 μg/ml, B. breve: 0.5 μg/ml), rifampicin (B. longum: 0.25 μg/ml, B. breve: 0.19 μg/ml) and vancomycin (B. longum: 0.38 μg/ml, B. breve: 1 μg/ml) [see Additional file 1]. The strains tested showed comparable results with previous publications except for linezolid and kanamycin [see Additional file 2], where we obtained a lower value than described [33–35].
Bacterial vaginosis is a polymicrobial disease and the organisms involved are likely to be in symbiotic relationship to each other for various metabolic requirements. Antimicrobial treatment may affect susceptible members of the consortia which may negatively alter the microenvironment for resistant organisms, such as A. vaginae and G. vaginalis.
By knowing the antibiotic susceptibility of the vaginal species it might be possible to develop new regimens for the treatment of recurrent bacterial vaginosis.
For example, this study showed that metronidazole resistance of A. vaginae is not an intrinsic feature. Further research needs to make clear whether this metronidazole resistance might be acquired by the presence and activation of nim-genes . Metronidazole resistance up to 29%  has been described for G. vaginalis but mechanisms are not yet clarified. Possibly this could be due to the lack of nitroreductases necessary to produce the hydroxymetabolite of metronidazole, which has stronger antibiotic activity than the parent compound.
Lactobacilli are resistant to metronidazole and it has been demonstrated that recolonistation of the vagina by H2O2-producing lactobacilli after metronidazole treatment occurs more frequently compared to clindamycin treatment .
Overview of the MIC-value ranges for Atopobium vaginae and Gardnerella vaginalis for 15 antimicrobial agents.
Atopobium vaginae (n = 9)
Gardnerella vaginalis (n = 4)
< 0.016 – 0.94
< 0.016 – 0.047
< 0.016 – 0.32
< 0.016 – 0.047
1 – 4
0.75 – 2
0.016 – 0.25
< 0.016 – 0.125
0.023 – 0.25
0.75 – 2
< 0.016 – 0.047
0.19 – 0.75
0.25 – 32
8 – 16
16 – 32
0.016 – 0.125
0.125 – 0.19
2 – 256
0.75 – 16
0.008 – 0.25
0.004 – 0.047
0.5 – 0.75
1 – 4
0.125 – 0.38
This work was supported through a research grant of the Bijzonder Onderzoeksfonds of the University of Gent (UGent) and the Fund for Scientific Research Flanders (Belgium). We thank the Culture Collection of the University of Göteborg, Sweden for kindly providing Atopobium vaginae isolates.
- Antonio MA, Hawes SE, Hillier SL: The identification of vaginal Lactobacillus species and the demographic and microbiologic characteristics of women colonized by these species. J Infect Dis. 1999, 180: 1950-1956. 10.1086/315109.View ArticlePubMedGoogle Scholar
- Vallor AC, Antonio MA, Hawes SE, Hillier SL: Factors associated with acquisition of, or persistent colonization by, vaginal lactobacilli: role of hydrogen peroxide production. J Infect Dis. 2001, 184: 1431-1436. 10.1086/324445.View ArticlePubMedGoogle Scholar
- Fredricks DN, Fiedler TL, Marrazzo JM: Molecular identification of bacteria associated with bacterial vaginosis. N Engl J Med. 2005, 353: 1899-1911. 10.1056/NEJMoa043802.View ArticlePubMedGoogle Scholar
- Verhelst R, Verstraelen H, Claeys G, Verschraegen G, Van Simaey L, De Ganck C, De Backer E, Temmerman M, Vaneechoutte M: Comparison between Gram stain and culture for the characterization of vaginal microflora: Definition of a distinct grade that resembles grade I microflora and revised categorization of grade I microflora. BMC Microbiol. 2004, 5: 61-10.1186/1471-2180-5-61.View ArticleGoogle Scholar
- Verhelst R, Verstraelen H, Claeys G, Verschraegen G, Delanghe J, Van Simaey L, De Ganck C, Temmerman M, Vaneechoutte M: Cloning of 16S rRNA genes amplified from normal and disturbed vaginal microflora suggests a strong association between Atopobium vaginae, Gardnerella vaginalis and bacterial vaginosis. BMC Microbiol. 2004, 4: 16-10.1186/1471-2180-4-16.View ArticlePubMedPubMed CentralGoogle Scholar
- Verhelst R, Verstraelen H, De Backer E, Claeys G, Verschraegen G, Van Simaey L, De Ganck C, Temmerman M, Vaneechoutte M: Characterization of vaginal microflora at three time points in pregnancy by Gram stain, culture and T-RFLP identifies L. gasseri as the Lactobacillus species most present in bacterial vaginosis. Submitted to BMC infectious diseases.Google Scholar
- Verstraelen H, Verhelst R, Claeys G, Temmerman M, Vaneechoutte M: Culture-independent analysis of vaginal microflora: the unrecognized association of Atopobium vaginae with bacterial vaginosis. Am J Obstet Gynecol. 2004, 191: 1130-1132. 10.1016/j.ajog.2004.04.013.View ArticlePubMedGoogle Scholar
- Ferris MJ, Masztal A, Aldridge KE, Fortenberry JD, Fidel PL Jr, Martin DH: Association of Atopobium vaginae, a recently described metronidazole resistant anaerobe, with bacterial vaginosis. BMC Infect Dis. 2004, 4: 5-10.1186/1471-2334-4-5.View ArticlePubMedPubMed CentralGoogle Scholar
- Burton JP, Chilcott CN, Al-Qumber M, Brooks HJ, Wilson D, Tagg JR, Devenish C: A preliminary survey of Atopobium vaginae in women attending the Dunedin gynaecology out-patients clinic: Is the contribution of the hard-to-culture microbiota overlooked in gynaecological disorders?. Aust N Z J Obstet Gynaecol. 2005, 45: 450-452. 10.1111/j.1479-828X.2005.00456.x.View ArticlePubMedGoogle Scholar
- Ferris MJ, Masztal A, Martin DH: Use of species-directed 16S rRNA gene PCR primers for detection of Atopobium vaginae in patients with bacterial vaginosis. J Clin Microbiol. 2004, 42: 5892-5894. 10.1128/JCM.42.12.5892-5894.2004.View ArticlePubMedPubMed CentralGoogle Scholar
- Swidsinski A, Mendling W, Loening-Baucke V, Ladhoff A, Swidsinski S, Hale LP, Lochs H: Adherent biofilms in bacterial vaginosis. Obstet Gynecol. 2005, 106: 1013-1023.View ArticlePubMedGoogle Scholar
- Hay PE, Lamont RF, Taylor-Robinson D, Morgan DJ, Ison C, Pearson J: Abnormal bacterial colonisation of the genital tract and subsequent preterm delivery and late miscarriage. Brit Med J. 1994, 308: 295-298.View ArticlePubMedPubMed CentralGoogle Scholar
- Hillier SL, Nugent RP, Eschenbach DA, Krohn MA, Gibbs RS, Martin DH, Klebanoff MA: Association between bacterial vaginosis and preterm delivery of a low-birth-weight infant. N Engl J Med. 1995, 333: 1737-1742. 10.1056/NEJM199512283332604.View ArticlePubMedGoogle Scholar
- Leitich H, Bodner-Adler B, Brunbauer M, Kaider A, Egarter C, Husslein P: Bacterial vaginosis as a risk factor for preterm delivery: A meta-analysis. Am J Obstet Gynecol. 2003, 189: 139-147. 10.1067/mob.2003.339.View ArticlePubMedGoogle Scholar
- Haggerty CL, Hillier SL, Bass DC, Ness RB: PID evaluation and clinical health study investigators. Bacterial vaginosis and anaerobic bacteria are associated with endometritis. Clin Infect Dis. 2004, 39: 990-995. 10.1086/423963.View ArticlePubMedGoogle Scholar
- Ness RB, Kip KE, Hillier SL, Soper DE, Stamm CA, Sweet RL, Rice P, Richter HE: A cluster analysis of bacterial vaginosis-associated microflora and pelvic inflammatory disease. Am J Epidemiol. 2005, 162: 585-590. 10.1093/aje/kwi243.View ArticlePubMedGoogle Scholar
- Watts DH, Krohn MA, Hillier SL, Eschenbach DA: Bacterial vaginosis as a risk factor for post-cesarean endometritis. Obstet Gynecol. 1990, 75: 52-58.PubMedGoogle Scholar
- Martin HL, Richardson BA, Nyange PM, Lavreys L, Hillier SL, Chohan B, Mandaliya K, Ndinya-Achola JO, Bwayo J, Kreiss J: Vaginal lactobacilli, microbial flora, and risk of human immunodeficiency virus type 1 and sexually transmitted disease acquisition. J Infect Dis. 1999, 180: 1863-1868. 10.1086/315127.View ArticlePubMedGoogle Scholar
- Sewankambo N, Gray RH, Wawer MJ, Paxton L, McNaim D, Wabwire-Mangen F, Serwadda D, Li C, Kiwanuka N, Hillier SL, Rabe L, Gaydos CA, Quinn TC, Konde-Lule J: HIV-1 infection associated with abnormal vaginal flora morphology and bacterial vaginosis. Lancet. 1997, 350: 546-550. 10.1016/S0140-6736(97)01063-5.View ArticlePubMedGoogle Scholar
- Hawes SE, Hillier SL, Benedetti J, Stevens CE, Koutsky LA, Wolner-Hanssen P, Holmes KK: Hydrogen peroxide-producing lactobacilli and acquisition of vaginal infections. J Infect Dis. 1996, 174: 1058-1063.View ArticlePubMedGoogle Scholar
- Hay P: Recurrent bacterial vaginosis. Curr Infect Dis Rep. 2000, 2: 506-512.View ArticlePubMedGoogle Scholar
- Larsson PG, Forsum U: Bacterial vaginosis, a disturbed bacterial flora and treatment enigma. APMIS. 2005, 113: 305-316. 10.1111/j.1600-0463.2005.apm_113501.x.View ArticlePubMedGoogle Scholar
- Beigi RH, Austin MN, Meyn LA, Krohn MA, Hillier SL: Antimicrobial resistance associated with the treatment of bacterial vaginosis. Am J Obstet Gynecol. 2004, 191: 1124-1129. 10.1016/j.ajog.2004.05.033.View ArticlePubMedGoogle Scholar
- Geissdorfer W, Bohmer C, Pelz K, Schoerner C, Frobenius W, Bogdan C: Tuboovarian abscess caused by Atopobium vaginae following transvaginal oocyte recovery. J Clin Microbiol. 2003, 41: 2788-2790. 10.1128/JCM.41.6.2788-2790.2003.View ArticlePubMedPubMed CentralGoogle Scholar
- Croco JL, Erwin ME, Jennings JM, Putnam LR, Jones RN: Evaluation of the Etest for antimicrobial spectrum and potency determinations of anaerobes associated with bacterial vaginosis and peritonitis. Diagn Microbiol Infect Dis. 1994, 20: 213-219. 10.1016/0732-8893(94)90006-X.View ArticlePubMedGoogle Scholar
- Schieven BC, Massey VE, Lannigan R, Hussain Z: Evaluation of susceptibility of anaerobic organisms by the Etest and the reference agar dilution method. Clin Infect Dis. 1995, 20: S337-S338.View ArticlePubMedGoogle Scholar
- Kharsany AB, Hoosen AA, Van den Ende J: Antimicrobial susceptibilities of Gardnerella vaginalis. Antimicrob Agents Chemother. 1993, 37: 2733-2735.View ArticlePubMedPubMed CentralGoogle Scholar
- McCarthy LR, Mickelsen PA, Smith EG: Antibiotic susceptibility of Haemophilus vaginalis (Corynebacterium vaginale) to 21 antibiotics. Antimicrob Agents Chemother. 1979, 16: 186-189.View ArticlePubMedPubMed CentralGoogle Scholar
- Goldstein EJ, Citron DM, Cherubin CE, Hillier SH: Comparative susceptibility of the Bacteroides fragilis group species and other anaerobic bacteria to meropenem, imipenem, piperacillin, cefoxitin, ampicillin/sulbactam, clindamycin and metronidazole. J Antimicrob Chemother. 1993, 31: 363-372.View ArticlePubMedGoogle Scholar
- Goldstein EJ, Citron DM, Merriam CV, Warren YA, Tyrrell KL, Fernandez HT: In vitro activities of Garenoxacin(BMS 284756) against 108 clinical isolates of Gardnerella vaginalis. Antimicrob Agents Chemother. 2002, 46: 3995-3996. 10.1128/AAC.46.12.3995-3996.2002.View ArticlePubMedPubMed CentralGoogle Scholar
- Jones BM, Geary I, Lee ME, Duerden BI: Comparison of the in vitro activities of fenticonazole, other imidazoles, metronidazole, and tetracycline against organisms associated with bacterial vaginosis and skin infections. Antimicrob Agents Chemother. 1989, 33: 970-972.View ArticlePubMedPubMed CentralGoogle Scholar
- Danielsen M, Wind A: Susceptibility of Lactobacillus spp. to antimicrobial agents. Int J Food Microbiol. 2003, 82: 1-11. 10.1016/S0168-1605(02)00254-4.View ArticlePubMedGoogle Scholar
- Delgado S, Florez AB, Mayo B: Antibiotic susceptibility of Lactobacillus and Bifidobacterium species from the human gastrointestinal tract. Curr Microbiol. 2005, 50: 202-207. 10.1007/s00284-004-4431-3.View ArticlePubMedGoogle Scholar
- Lim KS, Huh CS, Baek YI: Antimicrobial susceptibility of bifidobacteria. J Dairy Sci. 1993, 76: 2168-2174.View ArticlePubMedGoogle Scholar
- Moubareck C, Gavini F, Vaugien L, Butel MJ, Doucet-Populaire F: Antimicrobial susceptibility of bifidobacteria. J Antimicrob Chemother. 2005, 55: 38-44. 10.1093/jac/dkh495.View ArticlePubMedGoogle Scholar
- Theron MM, Janse Van Rensburg MN, Chalkley LJ: Nitroimidazole resistance genes (nimB) in anaerobic Gram-positive cocci (previously Peptostreptococcus spp.). J Antimicrob Chemother. 2004, 54: 240-242. 10.1093/jac/dkh270.View ArticlePubMedGoogle Scholar
- Austin MN, Beigi RH, Meyn LA, Hillier SL: Microbiologic response to treatment of bacterial vaginosis with topical clindamycin or metronidazole. J Clin Microbiol. 2005, 43: 4492-4497. 10.1128/JCM.43.9.4492-4497.2005.View ArticlePubMedPubMed CentralGoogle Scholar
- The pre-publication history for this paper can be accessed here:http://www.biomedcentral.com/1471-2334/6/51/prepub
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