Abstract
This work assessed the polymicrobial flora of mandibular third molar pericoronitis. Obligate anaerobes were found in almost all cases (32 of 35). Amoxicillin and pristinamycin were the most effective against the flora, particularly aerobic organisms. Metronidazole alone or combined with spiramycin was the most effective drug against obligate anaerobes.
Pericoronitis is an inflammatory and infectious condition that may accompany the clinical emergence of teeth. The microbial flora that develops in the distally located pseudopocket is the major cause. This flora is predominantly anaerobic (3, 14, 17, 19, 20, 23, 26). Therapeutic management usually involves a local surgical procedure and the prescription of antibiotics, often of the β-lactam family (7). The frequency of antibiotic-resistant microorganisms is dependent on the populations and is related to the prescribing habits of practitioners in each country (9, 25). In a previous study with selective media, we demonstrated the presence of β-lactamase-producing bacteria in 9 out of 26 French patients suffering from pericoronitis (23). These results encouraged us to supplement the study in order to identify the flora in another 35 patients and to evaluate its susceptibility to different antibiotics.
Thirty-five adults (20 men, 15 women), aged 18 to 52 years (mean age, 26.8 ± 8.2 years), without systemic disease, suffering from pericoronitis associated with the eruption of a third mandibular molar, with acute pain and without antibiotic treatment in the previous 3 months, entered into this study with their informed consent (BIR 49 801). Clinical examination, sampling, microbiological processing with nonselective media, microbial identification, and β-lactamase production testing were performed as previously described (23).
Clinical examination showed a mean pseudopocket depth of 6.22 ± 2.79 mm. Edema, trismus, and suppuration were present in, respectively, 91, 50, and 23% of the patients. The samples comprised 1 to 17 detectable microorganisms (mean, 10.5 ± 3.58). Only one sample yielded a single microorganism, which was identified as Actinomyces viscosus.
The principal identification results are summarized in Table 1. Obligate anaerobes were detected in 32 out of 35 samples. The most frequently detected microorganisms were viridans group streptococci (32 of 35 samples) and those belonging to the genera Actinomyces (29 of 35 samples) and Prevotella (21 of 35 samples).
TABLE 1.
Microorganisms detected in this study
| Microorganism(s)a | Frequency |
|---|---|
| Obligate anaerobes | |
| Gram-positive cocci | |
| Anaerococcus (Peptostreptococcus) prevotii | 3 |
| Peptococcus niger | 1 |
| Micromonas (Peptostreptococcus) micros | 9 |
| Peptostreptococcus anaerobius | 1 |
| Peptostreptococcus spp. | 3 |
| Gram-positive bacilli | |
| Bifidobacterium spp. | 3 |
| Clostridium spp. | 4 |
| Eggertella (Eubacterium) lentum | 5 |
| Eubacterium sp. | 1 |
| Mobiluncus spp. | 3 |
| Gram-negative cocci, Veillonella spp. | 11 |
| Gram-negative bacilli | |
| Bacteroides stercoris | 1 |
| Fusobacterium mortiferum | 1 |
| Fusobacterium necrogenes | 1 |
| Fusobacterium nucleatum | 4 |
| Leptotrichia buccalis | 5 |
| Prevotella bivia/tannerae/oeneca | 2 |
| Prevotella buccae | 5 |
| Prevotella buccalis | 3 |
| Prevotella corporis | 1 |
| Prevotella bivia disiens | 3 |
| Prevotella intermedia/nigrescens/pallens | 14 |
| Prevotella loescheii | 2 |
| Prevotella melaninogenica | 2 |
| Prevotella oralis | 1 |
| Prevotella oris | 2 |
| Porphyromonas gingivalis | 1 |
| Microaerophils | |
| Bacteroides ureolyticus | 2 |
| Campylobacter rectus | 7 |
| Campylobacter gracilis | 4 |
| Aerobes | |
| Gram-positive cocci | |
| Gemella haemolysans | 5 |
| Gemella morbillorum | 7 |
| Gemella spp. | 2 |
| Lactococcus lactis cremoris | 1 |
| Lactococcus raffinolactis | 1 |
| Staphylococcus spp. | 7 |
| Streptococcus acidominimus | 1 |
| Streptococcus adjacens | 4 |
| Streptococcus anginosus | 21 |
| Streptococcus constellatus | 10 |
| Streptococcus intermedius | 2 |
| Streptococcus gordonii | 3 |
| Streptococcus mitis | 11 |
| Streptococcus mutans | 1 |
| Streptococcus oralis | 11 |
| Streptococcus pyogenes | 1 |
| Streptococcus sanguinis | 3 |
| Streptococcus salivarius | 2 |
| Streptococcus viridans | 2 |
| Streptococcus sp. | 3 |
| Gram-positive bacilli | |
| Actinomyces gerencseriae | 3 |
| Actinomyces israelii | 15 |
| Actinomyces meyeri | 4 |
| Actinomyces odontolyticus | 21 |
| Actinomyces naeslundii/viscosus | 10 |
| Actinomyces spp. | 2 |
| Bacillus spp. | 2 |
| Corynebacterium afermentans | 3 |
| Corynebacterium bovis | 1 |
| Corynebacterium striatum | 1 |
| Corynebacterium sp. | 3 |
| Lactobacillus acidophilus | 4 |
| Lactobacillus sp. | 1 |
| Propionibacterium acnes | 7 |
| Propionibacterium propionicus | 2 |
| Propionibacterium granulosum | 2 |
| Gram-negative bacilli | |
| Capnocytophaga sp. | 20 |
| Pseudomonas sp. | 1 |
Classification into anaerobes, microaerophils, and aerobes according to Bergey's Manual of Determinative Bacteriology (10).
Most of the obligate anaerobes identified in this study may be found in the healthy oral cavity (12) but also are associated with oral diseases (13, 16, 22, 24), numerous localized infections, particularly of the ear-nose-throat region and the respiratory system (4, 11), usually in conjunction with infections associated with polymicrobial flora and systemic infections. The frequent presence of microaerophilic bacteria and facultative anaerobes that grow predominantly anaerobically (members of the genera Actinomyces, Propionibacterium, and Capnocytophaga) confirms the anaerobic shift of this flora. These data can tentatively be compared with those described in a previous study with DNA probes, in which the microbial index for some anaerobic bacteria was shown to be elevated compared with that of control patients with asymptomatic erupting third molars (3).
Interestingly, members of the genus Actinomyces were detected in 29 of the samples. The members of genus Actinomyces belong to the normal flora of the oral cavity and may be associated with dental caries and gingivitis (2, 24) or may also be responsible for more destructive diseases, such as actinomycosis (5, 8, 21), especially Actinomyces israelii. The presence of A. israelii in 15 samples, associated with that of other microorganisms found in cervicofacial actinomycosis lesions (21), suggests that in certain cases the pathogenic processes might be similar to those of actinomycosis. In order to confirm this hypothesis, further studies are needed with a demographically similar disease-free group for comparative and control purposes.
These data reinforce the concept of infection due to polymicrobial flora in the case of pericoronitis and highlight the need for efficacy against anaerobic flora when antibiotic treatment is administered. However, we must pay attention to the fact that some other bacterial agents that are not cultivable are still unknown and may have a role in pericoronitis.
Susceptibility to amoxicillin (A1, 0.5 mg/liter; A2, 4 mg/liter), spiramycin (S1, 1 mg/liter; S2, 4 mg/liter), metronidazole (M, 4 mg/liter), pristinamycin (P1, 1 mg/liter; P2, 2 mg/liter), and the combination of spiramycin and metronidazole (MS1, 1 and 4 mg/liter; MS2, 4 and 4 mg/liter) was evaluated at the critical concentrations defined by the Antibiotic Sensitivity Test Committee of the French Microbiology Society in accordance with the recommendations of the NCCLS (18) and the Antibiotic Sensitivity Test Committee of the French Microbiology Society (6). Four reference strains were used on each dish tested: Bacteroides fragilis (ATCC 25285), Bacteroides thetaiotaomicron (ATCC 29741), Escherichia coli (CIP 7624), and Actinomyces odontolyticus (laboratory strain BC 21).
The results of the antibiotic susceptibility tests are summarized in Table 2. Susceptibility to the antibiotics tested was found in, respectively, 193 (A1), 209 (A2), 94 (S1), 158 (S2), 69 (M), 136 (MS1), 173 (MS2), 201 (P1), and 206 (P2) of the 211 strains tested. β-Lactamase production was detected in six strains (two Staphylococcus and four Prevotella strains) obtained from five samples. Amoxicillin and the combination of spiramycin and metronidazole are the antibiotics most regularly prescribed by French clinicians (15; Anonymous, Letter, Lett. Chir. Dent. 6:15, 2002). Pristinamycin is one of the two antibiotics recommended in France for patients at high risk of infection who are allergic to amoxicillin (1). The results of the antibiotic sensitivity tests show that amoxicillin and pristinamycin are the most effective drugs against the strains tested and against the strains classified as aerobic in particular. Metronidazole alone or combined with spiramycin, amoxicillin at 4 mg/liter, and pristinamycin are the most effective drugs against obligate anaerobic bacteria. The efficacy of the latter drug confirms its value in acute cases and after the failure of other antibiotics.
TABLE 2.
Evaluation of antibiotic susceptibility of strains isolated from patients with pericoronitis on selective media containing antibioticsa
| Microorganisms | nb | No.
of strains resistant to concn
testedc
|
||||||||
|---|---|---|---|---|---|---|---|---|---|---|
| A1 | A2 | S1 | S2 | M | MS1 | MS2 | P1 | P2 | ||
| Aerobesf | 157 | 11 | 0 | 89 | 43 | 142 | 75 | 38 | 2 | 0 |
| Actinomyces spp. | 51 | 1 | 0 | 11 | 8 | 51 | 11 | 8 | 0 | 0 |
| A. odontolyticus | 19 | 1 | 0 | 1 | 1 | 19 | 1 | 1 | 0 | 0 |
| A. israelii | 16 | 0 | 0 | 3 | 2 | 16 | 3 | 2 | 0 | 0 |
| A. naeslundii | 8 | 0 | 0 | 4 | 3 | 8 | 4 | 3 | 0 | 0 |
| Capnocytophaga spp. | 21 | 1 | 0 | 16 | 5 | 7 | 5 | 2 | 0 | 0 |
| Corynebacterium spp. | 5 | 0 | 0 | 3 | 1 | 5 | 3 | 1 | 0 | 0 |
| Gemella spp. | 10 | 2 | 0 | 7 | 5 | 10 | 7 | 5 | 0 | 0 |
| Propionibacterium spp. | 11 | 1 | 0 | 2 | 1 | 10 | 2 | 1 | 1 | 0 |
| Staphylococcus spp. | 7 | 4 | 0 | 6 | 5 | 7 | 6 | 5 | 0 | 0 |
| Streptococcus spp. | 37 | 1 | 0 | 33 | 12 | 37 | 30 | 10 | 0 | 0 |
| S. anginosusd | 19 | 0 | 0 | 18 | 6 | 18 | 17 | 5 | 0 | 0 |
| S. oralise | 12 | 1 | 0 | 11 | 5 | 12 | 9 | 4 | 0 | 0 |
| Anaerobesf | 54 | 7 | 2 | 28 | 10 | 0 | 0 | 0 | 8 | 5 |
| Prevotella spp. | 25 | 4 | 1 | 9 | 2 | 0 | 0 | 0 | 3 | 0 |
| Veillonella spp. | 5 | 2 | 1 | 5 | 5 | 0 | 0 | 0 | 5 | 5 |
| Fusobacterium spp. | 4 | 1 | 0 | 4 | 2 | 0 | 0 | 0 | 0 | 0 |
| Micromonas micros | 4 | 0 | 0 | 3 | 0 | 0 | 0 | 0 | 0 | 0 |
Several strains of the same species from the same sample may have been tested. All of the strains tested are not listed.
n, number of strains isolated.
A1, amoxicillin at 0.5 mg/liter; A2, amoxicillin at 4 mg/liter; S1, spiramycin at 1 mg/liter; S2, spiramycin at 4 mg/liter; M, metronidazole at 4 mg/liter; MS1, metronidazole-spiramycin at 4 and 1 mg/liter; MS2, metronidazole-spiramycin at 4 and 4 mg/liter; P1, pristinamycin at 1 mg/liter; P2, pristinamycin at 2 mg/liter.
Streptococcus anginosus group.
Streptococcus oralis group.
Classification into aerobes and anaerobes according to Bergey's Manual of Determinative Bacteriology (10).
The broad spectrum of amoxicillin fully encompasses the microorganisms found in pericoronitis. However, the presence of β-lactamase-producing microorganisms, as has already been demonstrated in a previous study (23), may cause failure of antibiotic treatment of pericoronitis. Metronidazole is particularly interesting in infections due to polymicrobial flora, in which anaerobic microorganisms predominate. Its combination with a macrolide (spiramycin) extends the spectrum to certain non-obligately anaerobic bacteria, allowing its use in pericoronitis with a well-documented mixed aerobic-anaerobic flora.
Acknowledgments
We thank Hélène Pinsard-Solhi, Carine Desoindre, Sylvie Piel, Xavier Moisan, Noël Grosset, and Céline Allaire for technical and editorial assistance.
The work described here was performed in the Equipe de Biologie Buccale and the Laboratoire de Microbiologie Pharmaceutique and funded by the Fondation Langlois, Conseil Régional de Bretagne, and Laboratoire Aventis.
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