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Susceptibility

β-Lactamase Production and Antimicrobial Susceptibility of Oral Heterogeneous Fusobacterium nucleatum Populations in Young Children

E. Könönen, A. Kanervo, K. Salminen, H. Jousimies-Somer
E. Könönen
Anaerobe Reference Laboratory, National Public Health Institute, Helsinki, and
Department of Medical Microbiology and Immunology, University of Aarhus, Aarhus, Denmark
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A. Kanervo
Anaerobe Reference Laboratory, National Public Health Institute, Helsinki, and
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K. Salminen
Pfizer Finland, Espoo, Finland, and
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H. Jousimies-Somer
Anaerobe Reference Laboratory, National Public Health Institute, Helsinki, and
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DOI: 10.1128/AAC.43.5.1270
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ABSTRACT

Oral Fusobacterium nucleatum populations from 20 young, healthy children were examined for β-lactamase production. Ten children (50%) harbored, altogether, 25 β-lactamase-positiveF. nucleatum isolates that were identified as F. nucleatum subsp. polymorphum, F. nucleatum subsp. nucleatum, and F. nucleatum subsp. vincentii (J. L. Dzink, M. T. Sheenan, and S. S. Socransky, Int. J. Syst. Bacteriol. 40:74–78, 1990). In vitro susceptibility of these β-lactamase-producing and 26 non-β-lactamase-producing F. nucleatum isolates was tested with penicillin G, amoxicillin-clavulanic acid, tetracycline hydrochloride, metronidazole, trovafloxacin, and azithromycin. Except for penicillin G, the antimicrobials exhibited good activity against all F. nucleatum isolates.

Fusobacterium nucleatumis one of the most frequently found anaerobic species in the oral cavity in early childhood (11). It is also commonly found in various infections in oral and nonoral sites. Pediatric infections in which F. nucleatum is involved are located mainly in the upper respiratory tract and the head and neck (5), suggesting an oral source. F. nucleatum is a heterogeneous bacterial group; its division into several subspecies has been made on the basis of electrophoretic patterns of enzyme mobilities or whole-cell proteins and on the basis of DNA-DNA homology (6, 7). However, F. nucleatum subspecies cannot be separated from each other by conventional biochemical testing alone. Differences in pathogenic potential among F. nucleatumsubspecies have been reported (8, 27), indicating that the various subspecies may exhibit differences in such characteristics as β-lactamase production. Except for one report of a β-lactamase-producing Fusobacterium nucleatum subsp.polymorphum strain from the blood of a seriously ill patient (9), no data on β-lactamase production by different F. nucleatum subspecies exist. The first reports of penicillin resistance due to β-lactamase production byF. nucleatum were published in the mid-1980s (1, 3, 24). The frequency of β-lactamase production by fusobacteria seems to be increasing (2). We have observed surprisingly high frequencies of β-lactamase production by several anaerobic, gram-negative species in oral sites, especially by pigmentedPrevotella spp., in infants and young children (13, 14, 19). In the present study, our aim was to examine β-lactamase production among heterogeneous oral F. nucleatum populations isolated from young, healthy children. Secondly, by using cellular fatty acid (CFA) analysis for subspecies identification, we tried to determine if β-lactamase production is characteristic only of a certain subspecies. Finally, the activity of potential alternative antimicrobials for F. nucleatum was determined.

Altogether, 123 F. nucleatum isolates originated from young, healthy children (11) from whom at least three simultaneous oral isolates were available. The children (10 boys and 10 girls ranging in age from 2 to 3.4 years) had not received systemic antimicrobial treatment within at least 1 month preceding the specimen collection (Table 1). The clinicalF. nucleatum isolates, with various colony morphologies, were indole positive and lipase negative, produced butyric acid as a major metabolic end product, and did not convert lactate to propionate.F. nucleatum subsp. polymorphum ATCC 10953T, Fusobacterium nucleatum subsp.nucleatum ATCC 25586T, Fusobacterium nucleatum subsp. vincentii ATCC 49256T,Fusobacterium nucleatum subsp. fusiforme NCTC 11326T, Fusobacterium nucleatum subsp.animalis NCTC 12276T, Fusobacterium periodonticum ATCC 33693T (a closely related strain) were used as reference strains. The bacterial isolates were maintained in vials containing 20% sterilized skim milk at −70°C until further testing. An automatic CFA analysis, based on capillary column gas-liquid chromatography designed by the Microbial Identification System (MIS) (MIDI, Newark, N.J.) and with the Moore Broth Library database (versions 3.8 and 3.9) as a reference, was used as previously described (15) to presumptively identify the clinicalF. nucleatum isolates to the subspecies level. A dendrogram (cluster analysis) was constructed for β-lactamase-positive F. nucleatum isolates and all reference strains.

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Table 1.

Characteristics of 20 children and the distribution of β-lactamase-producing F. nucleatum subspecies among their oral F. nucleatum populationsa

β-Lactamase production of all 123 clinical F. nucleatum isolates was examined by the qualitative chromogenic cephalosporin disk (AB Biodisk, Solna, Sweden) test (20). In vitro antimicrobial susceptibility to penicillin G, amoxicillin-clavulanic acid, tetracycline hydrochloride, metronidazole, trovafloxacin, and azithromycin was examined for all β-lactamase-positive isolates and the corresponding number of β-lactamase-negative isolates by using the National Committee for Clinical Laboratory Standards (NCCLS)-approved agar dilution method (18). MICs were determined in parallel on brucella blood agar and on fastidious anaerobe agar (FAA; Lab M Ltd., Bury, England), both supplemented with sheep blood, hemin, and vitamin K1(21). To aid the endpoint reading, a viability indicator dye, triphenyltetrazolium chloride (TTC) (21), was used forF. nucleatum isolates with hazy growth.

All F. nucleatum isolates produced major amounts of C14:0, C16:0, and C16:1-cis-9. The identification provided by MIS was used for the presumptive identification of the clinicalF. nucleatum isolates to the subspecies level. A dendrogram was constructed for the β-lactamase-positiveF. nucleatum isolates and all reference strains (Fig.1). Most of the isolates clustered together with the indicated F. nucleatum type strains, but some clinical isolates formed a subcluster that did not concisely conform to the pattern of any type strain. For the latter isolates, similarity indices were less than 0.3 (the highest possible match is 1.0) and/or the differences between the primary and secondary identification choices by MIS were less than 0.1.

Fig. 1.
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Fig. 1.

Dendrogram of β-lactamase-producing F. nucleatum isolates and the type strains F. nucleatum subsp. polymorphum ATCC 10953T,F. nucleatum subsp. nucleatum ATCC 25586T, F. nucleatum subsp.vincentii ATCC 49256T, F. nucleatum subsp. fusiforme NCTC 11326T,F. nucleatum subsp. animalis NCTC 12276T, and F. periodonticum ATCC 33693T, generated by cluster analysis of CFA profiles.

Ten children (50%) harbored a total of 25 β-lactamase-positiveF. nucleatum isolates. Both β-lactamase-positive and β-lactamase-negative F. nucleatum strains were simultaneously isolated from 9 of 10 children. According to MIS, 16 of the β-lactamase-positive isolates were identified as F. nucleatum subsp. polymorphum, 7 isolates were identified as F. nucleatum subsp. nucleatum, and 2 isolates were identified as F. nucleatum supsp.vincentii. The distribution of the β-lactamase-producing subspecies within the group of children studied is seen in Table 1. Activities of several antimicrobials against β-lactamase-positiveF. nucleatum isolates showed similar patterns on both agar media; the MICs determined on brucella agar and FAA agreed with each other within 1 log2 dilution. However, β-lactamase-negative isolates frequently exhibited poor growth on brucella plates. Table 2 presents the in vitro activities of penicillin G, amoxicillin-clavulanic acid, tetracycline hydrochloride, metronidazole, trovafloxacin, and azithromycin against 25 β-lactamase-producing and 26 non-β-lactamase-producing F. nucleatum isolates. MICs for the β-lactamase-positive isolates ranged from intermediate susceptibility (one isolate; MICs of 1 and 2 μg/ml on FAA and brucella agar, respectively) to high resistance to penicillin G (MIC of 256 μg/ml). Except for two isolates from the same child for which the MIC was 1 μg/ml, β-lactamase-negative isolates exhibited high susceptibility to penicillin G (MIC ≤ 0.03 μg/ml). Amoxicillin-clavulanic acid, tetracycline hydrochloride, metronidazole, and trovafloxacin had good activity against allF. nucleatum isolates. Azithromycin also proved to be effective against F. nucleatum, as only one strain for which MICs were 2 and 4 μg/ml on brucella agar and on FAA, respectively, was found.

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Table 2.

In vitro activities of antimicrobial agents against β-lactamase-producing and non-β-lactamase-producing F. nucleatum isolates

A surprisingly high frequency of β-lactamase production by oralF. nucleatum was found in these young, healthy children, as half of them harbored β-lactamase-producing isolates. No differences between children with and without β-lactamase-positive F. nucleatum isolates with respect to gender, age, or preceding antimicrobial treatment were observed. β-Lactamase production coincided well with penicillin resistance; the MICs of penicillin G on brucella agar varied from 2 to 256 μg/ml for β-lactamase-positive isolates compared with the low MICs of penicillin G for β-lactamase-negative isolates. Notably, as both β-lactamase-producing and non-β-lactamase-producing variants can be simultaneously present in the mouth, several isolates per sample should be tested to determine the true rate of β-lactamase production within a bacterial species. As with our previous experience with pigmented Prevotella species (13, 14), the multiple isolate testing may partly explain the high frequency of β-lactamase production by F. nucleatum in young children observed in the present study.

CFA analysis under standardized conditions has proved to be a useful tool for the taxonomic characterization of anaerobic gram-negative bacilli (16). Tunér et al. (23) have successfully used CFA analysis to separate differentFusobacterium species. However, in differentiatingF. nucleatum subspecies, an improved and expanded database that recognizes the National Collection of Type Cultures strains of F. nucleatum is needed. Another problem arises from the vast heterogeneity among F. nucleatumpopulations. The reported overlapping of subspecies (7) has caused uncertainty about whether three or four human subspecies exist. More recently, even the validity of the division of F. nucleatum into subspecies has been questioned (17). In the present study, CFA analysis was performed to presumptively identify the β-lactamase-positive F. nucleatum isolates to the subspecies level. The majority of these isolates were identified asF. nucleatum subsp. polymorphum; however, some were also identified as F. nucleatum subsp.nucleatum and F. nucleatum subsp.vincentii, which in most cases clustered together with indicated type strains. Thus, β-lactamase production seems not to be confined to one subspecies only but is shared by several F. nucleatum subspecies.

Special efforts are needed to test fusobacteria for their antimicrobial susceptibilities. Even by using an NCCLS-approved agar dilution method (18) that allows the addition of blood to the culture medium as an appropriate growth supplement for anaerobic bacteria, the problem of poor or hazy growth arises. “Tailing” of growth occurs due to cell wall-defective variants of Fusobacterium species (10). To solve the problem with exact end-point determination, we used TTC, a viability indicator dye, as an indicator to recognize the demarcation zone of viable growth. TTC has been successfully used to minimize inconsistency in interpreting endpoints for Bilophila wadsworthia (22), a fastidious anaerobic species with tendency to hazy growth on antimicrobial-containing media, a phenomenon identical to that seen with fusobacteria. Brazier et al. (4) compared different culture media for their capacity to support the growth of fusobacteria and found that the enriched culture medium designed especially for anaerobes, FAA, promoted the growth of fusobacteria and reduced their “tailing.” In the present study, we accordingly determined the susceptibilities in tandem by using the NCCLS-recommended supplemented brucella agar and FAA. Both culture media were associated with nearly identical MICs for β-lactamase-positive F. nucleatum isolates. However, we were repeatedly confronted with difficulties in determining MICs due to the poor growth of β-lactamase-negative isolates on brucella agar. According to the previous (4) as well as present results, FAA favors the growth of fusobacteria and, conceivably, promotes the susceptibility testing of F. nucleatum.

In a recent study (14), the penicillin breakpoint of 0.5 μg/ml precisely separated β-lactamase-producingPrevotella melaninogenica isolates from non-β-lactamase-producing isolates; the observation is in accordance with the latest breakpoint determination by NCCLS (18). In the present study, the lowest MIC measured on FAA was 1 μg/ml for β-lactamase-producing F. nucleatum, but the MICs for two β-lactamase-negative F. nucleatumisolates from one child (probably the same strain) were also 1 μg/ml. The MICs of amoxicillin-clavulanic acid, tetracycline hydrochloride, metronidazole, and trovafloxacin were unambiguously below the current susceptible breakpoints approved by NCCLS (18). Trovafloxacin, a novel fluoroquinolone, has shown promising in vitro activity against anaerobes (25, 26). In the present study, the MICs of trovafloxacin and also of metronidazole were similar to MICs for 28 F. nucleatum strains reported by Wexler et al. (26). Although no NCCLS breakpoint for azithromycin has been approved for anaerobes, the low MICs seen in this study indicate that azithromycin has better activity than other macrolides against F. nucleatum.

The clinical significance of fusobacteria in pediatric infections has recently been pointed out by Brook (5). In fact,F. nucleatum was the Fusobacterium species most frequently isolated from these infections. According to our preliminary experience, F. nucleatum might play a role in the pathogenesis of acute otitis media in infancy, as it was the anaerobic species most frequently isolated from the nasopharynx during bouts of ear infection (12). As seen in the present study, penicillin resistance due to β-lactamase production by oralF. nucleatum occurs frequently in childhood. This phenomenon is not confined to F. nucleatum subsp.polymorphum but seems to be a characteristic of several other F. nucleatum subspecies. As beta-lactams are among the antimicrobials most commonly used in bacterial pediatric infections, routine β-lactamase testing of multiple isolates from such infections could be of benefit.

In conclusion, the reported high resistance rates among oral anaerobic species in childhood can have a significant impact on the treatment practices and outcomes of pediatric infections that originate in the oral cavity.

ACKNOWLEDGMENTS

This study was supported in part by grants (E. Könönen) from the Finnish Cultural Foundation and the Finnish Dental Society.

The technical assistance of Marja Piekkola is gratefully acknowledged.

FOOTNOTES

    • Received 4 August 1998.
    • Returned for modification 23 November 1998.
    • Accepted 12 February 1999.
  • Copyright © 1999 American Society for Microbiology

REFERENCES

  1. 1.↵
    1. Aldridge K. E.,
    2. Sanders C. V.,
    3. Lewis A. C.,
    4. Marier R. L.
    Susceptibility of anaerobic bacteria to beta-lactam antibiotics and beta-lactamase production. J. Med. Microbiol. 16 1983 75 82
    OpenUrlCrossRefPubMedWeb of Science
  2. 2.↵
    1. Appelbaum P. C.,
    2. Spangler S. K.,
    3. Jacobs M. R.
    β-Lactamase production and susceptibilities to amoxicillin, amoxicillin-clavulanate, ticarcillin, ticarcillin-clavulanate, cefoxitin, imipenem, and metronidazole of 320 non-Bacteroides fragilis Bacteroides isolates and 129 fusobacteria from 28 U.S. centers. Antimicrob. Agents Chemother. 34 1990 1546 1550
    OpenUrlAbstract/FREE Full Text
  3. 3.↵
    1. Bourgault A.-M.,
    2. Harding G. K.,
    3. Smith J. A.,
    4. Horsman G. B.,
    5. Marrie T. J.,
    6. Lamothe F.
    Survey of anaerobic susceptibility patterns in Canada. Antimicrob. Agents Chemother. 30 1986 798 801
    OpenUrlAbstract/FREE Full Text
  4. 4.↵
    1. Brazier J. S.,
    2. Goldstein E. J. C.,
    3. Citron D. M.,
    4. Ostovari M. I.
    Fastidious anaerobe agar compared with Wilkins-Chalgren agar, brain heart infusion agar, and brucella agar for susceptibility testing of Fusobacterium species. Antimicrob. Agents Chemother. 34 1990 2280 2282
    OpenUrlAbstract/FREE Full Text
  5. 5.↵
    1. Brook I.
    Fusobacterial infections in children. J. Infect. 28 1994 155 165
    OpenUrlCrossRefPubMedWeb of Science
  6. 6.↵
    1. Dzink J. L.,
    2. Sheenan M. T.,
    3. Socransky S. S.
    Proposal of three subspecies of Fusobacterium nucleatum Knorr 1922: Fusobacterium nucleatum subsp. nucleatum subsp. nov., comb. nov.; Fusobacterium nucleatum subsp. polymorphum subsp. nov., nom. rev., comb. nov.; and Fusobacterium nucleatum subsp. vincentii subsp. nov., nom. rev., comb. nov. Int. J. Syst. Bacteriol. 40 1990 74 78
    OpenUrlCrossRefPubMed
  7. 7.↵
    1. Gharbia S. E.,
    2. Shah H. N.
    Fusobacterium nucleatum subsp. fusiforme subsp. nov. and Fusobacterium nucleatum subsp. animalis subsp. nov. as additional subspecies within Fusobacterium nucleatum. Int. J. Syst. Bacteriol. 42 1992 296 298
    OpenUrlCrossRefPubMed
  8. 8.↵
    1. Gharbia S. E.,
    2. Shah H. N.,
    3. Lawson P. A.,
    4. Haapasalo M.
    The distribution and frequency of Fusobacterium nucleatum subspecies in the human oral cavity. Oral Microbiol. Immunol. 5 1990 324 327
    OpenUrlCrossRefPubMed
  9. 9.↵
    1. Goldstein E. J. C.,
    2. Summanen P. H.,
    3. Citron D. M.,
    4. Rosove M. H.,
    5. Finegold S. M.
    Fatal sepsis due to a β-lactamase-producing strain of Fusobacterium nucleatum subspecies polymorphum. Clin. Infect. Dis. 20 1995 797 800
    OpenUrlCrossRefPubMedWeb of Science
  10. 10.↵
    1. Johnson C. C.,
    2. Wexler H. M.,
    3. Becker S.,
    4. Garcia M.,
    5. Finegold S. M.
    Cell-wall-defective variants of Fusobacterium. Antimicrob. Agents Chemother. 33 1989 369 372
    OpenUrlAbstract/FREE Full Text
  11. 11.↵
    1. Könönen E.,
    2. Asikainen S.,
    3. Saarela M.,
    4. Karjalainen J.,
    5. Jousimies-Somer H.
    The oral gram-negative anaerobic microflora in young children: longitudinal changes from edentulous to dentate mouth. Oral Microbiol. Immunol. 9 1994 136 141
    OpenUrlCrossRefPubMedWeb of Science
  12. 12.↵
    Könönen, E., A. Kanervo, A. Bryk, A. Takala, R. Syrjänen, and H. Jousimies-Somer. Anaerobes in the nasopharynx during acute otitis media episodes in infancy. Anaerobe, in press.
  13. 13.↵
    1. Könönen E.,
    2. Nyfors S.,
    3. Mättö J.,
    4. Asikainen S.,
    5. Jousimies-Somer H.
    β-Lactamase production by oral pigmented Prevotella species isolated from young children. Clin. Infect. Dis. 25 (Suppl. 2) 1997 S272 S274
    OpenUrl
  14. 14.↵
    1. Könönen E.,
    2. Saarela M.,
    3. Kanervo A.,
    4. Karjalainen J.,
    5. Asikainen S.,
    6. Jousimies-Somer H.
    β-Lactamase production and penicillin susceptibility among different ribotypes of Prevotella melaninogenica simultaneously colonizing the oral cavity. Clin. Infect. Dis. 20 (Suppl. 2) 1995 S364 S366
    OpenUrl
  15. 15.↵
    1. Könönen E.,
    2. Väisänen M.-L.,
    3. Finegold S. M.,
    4. Heine R.,
    5. Jousimies-Somer H.
    Cellular fatty acid analysis and enzyme profiles of Porphyromonas catoniae—a frequent colonizer of the oral cavity in children. Anaerobe 2 1996 329 335
    OpenUrlCrossRef
  16. 16.↵
    1. Moore L. V. H.,
    2. Bourne D. M.,
    3. Moore W. E. C.
    Comparative distribution and taxonomic value of cellular fatty acids in thirty-three genera of anaerobic gram-negative bacilli. Int. J. Syst. Bacteriol. 44 1994 338 347
    OpenUrlCrossRefPubMed
  17. 17.↵
    1. Morris M. L.,
    2. Andrews R. H.,
    3. Rogers A. H.
    Investigations of the taxonomy and systematics of Fusobacterium nucleatum using allozyme electrophoresis. Int. J. Syst. Bacteriol. 47 1997 103 110
    OpenUrlCrossRefPubMed
  18. 18.↵
    National Committee for Clinical Laboratory Standards Methods for antimicrobial susceptibility testing of anaerobic bacteria 4th ed. 1997 Approved standard M11-A4. National Committee for Clinical Laboratory Standards, Wayne, Pa.
  19. 19.↵
    Nyfors, S., E. Könönen, A. Takala, and H. Jousimies-Somer. β-Lactamase production by oral gram-negative anaerobes during the first year of infant’s life in relation to antibiotic treatment. Submitted for publication.
  20. 20.↵
    1. O’Callaghan C. H.,
    2. Morris A.,
    3. Kirby S. M.,
    4. Shingler A. H.
    Novel method for detection of β-lactamases by using a chromogenic cephalosporin substrate. Antimicrob. Agents Chemother. 1 1972 283 288
    OpenUrlAbstract/FREE Full Text
  21. 21.↵
    1. Summanen P.,
    2. Baron E. J.,
    3. Citron D. M.,
    4. Strong C. A.,
    5. Wexler H. M.,
    6. Finegold S. M.
    Wadsworth anaerobic bacteriology manual 5th ed. 1993 Star Publishing Belmont, Calif
  22. 22.↵
    1. Summanen P.,
    2. Wexler H. M.,
    3. Finegold S. M.
    Antimicrobial susceptibility testing of Bilophila wadsworthia by using triphenyltetrazolium chloride to facilitate endpoint determination. Antimicrob. Agents Chemother. 36 1992 1658 1664
    OpenUrlAbstract/FREE Full Text
  23. 23.↵
    1. Tunér K.,
    2. Baron E. J.,
    3. Summanen P.,
    4. Finegold S. M.
    Cellular fatty acids in Fusobacterium species as a tool for identification. J. Clin. Microbiol. 30 1992 3225 3229
    OpenUrlAbstract/FREE Full Text
  24. 24.↵
    1. Tunér K.,
    2. Lindquist L.,
    3. Nord C. E.
    Characterization of a new β-lactamase from Fusobacterium nucleatum by substrate profiles and chromatofocusing patterns. J. Antimicrob. Chemother. 16 1985 23 30
    OpenUrlCrossRefPubMed
  25. 25.↵
    1. Väisänen M.-L.,
    2. Mättö J.,
    3. Salminen K.,
    4. Jousimies-Somer H.
    In vitro activity of trovafloxacin against anaerobic bacteria. Rev. Med. Microbiol. 8 (Suppl. 1) 1997 S81 S83
    OpenUrl
  26. 26.↵
    1. Wexler H. M.,
    2. Molitoris E.,
    3. Molitoris D.,
    4. Finegold S. M.
    In vitro activities of trovafloxacin against 557 strains of anaerobic bacteria. Antimicrob. Agents Chemother. 40 1996 2232 2235
    OpenUrlAbstract/FREE Full Text
  27. 27.↵
    1. Xie H.,
    2. Gibbons R. J.,
    3. Hay D. I.
    Adhesive properties of strains of Fusobacterium nucleatum of the subspecies nucleatum,vincentii and polymorphum. Oral Microbiol. Immunol. 6 1991 257 263
    OpenUrlPubMedWeb of Science
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β-Lactamase Production and Antimicrobial Susceptibility of Oral Heterogeneous Fusobacterium nucleatum Populations in Young Children
E. Könönen, A. Kanervo, K. Salminen, H. Jousimies-Somer
Antimicrobial Agents and Chemotherapy May 1999, 43 (5) 1270-1273; DOI: 10.1128/AAC.43.5.1270

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β-Lactamase Production and Antimicrobial Susceptibility of Oral Heterogeneous Fusobacterium nucleatum Populations in Young Children
E. Könönen, A. Kanervo, K. Salminen, H. Jousimies-Somer
Antimicrobial Agents and Chemotherapy May 1999, 43 (5) 1270-1273; DOI: 10.1128/AAC.43.5.1270
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KEYWORDS

Anti-Bacterial Agents
fluoroquinolones
Fusobacterium nucleatum
beta-lactamases

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Print ISSN: 0066-4804; Online ISSN: 1098-6596