In the oral cavities of BALB/c mice, microbial population levels are regulated by multifactorial processes. Factors include the production of inhibitory substances and the exchange of genetic material. In this work, 371 isolates from different sites (saliva, tongue, teeth, and mucosa) of the oral cavities of BALB/c mice were screened for resistance to antibiotics and antimicrobial activity. Antibiotic-resistant strains represented 25% of the total flora. Among the predominant species, all the S. faecalis isolates showed multiresistance, and 23% of the Lactobacillus murinus isolates and 15% of the Staphylococcus aurcus were resistant to at least one antibiotic. Resistance to aminoglycosides (neomycin, streptomycin, kanamycin, and gentamicin) was most frequently encountered. In S. faecalis, high levels of resistance were recorded to neomycin and streptomycin but not to gentamicin or kanamycin. Macrolides (M), lincosamides (L), streptogramin B (S), tetracycline (Tc), and chloramphenicol (Cm) resistance was also present in multiresistance patterns, especially among S. faecalis isolates. Hemolytic (Hly+) streptococci were less resistant to MLS, Tc, and Cm than were non-hemolytic (Hly-) isolates. Resistance to β-lactam antibiotics was detected only among staphylococci and with a low prevalence (4%). The frequencies of strains producing antimicrobial substances against the indicator strains (S. mutans LG-1, S. sanguis Ny 101, and A. viscosus Ny 1) were high for L. murinus (76%) and S. faecalis (57% for Hly- and 90% for Hly+), but low for S. aurcus (7%). These results indicate that the indigenous oral flora could interfere with colonization by allochthonous micro-organisms and that resistance patterns should be taken into account for the elimination of the oral indigenous flora by antibiotic treatment. The indigenous oral flora could thus interfere with dental caries assays in mice.
Get full access to this article
View all access options for this article.
References
1.
Afonsky, D.A. (1957): Experimental Caries in the Mouse, IADR Prog & Abst67: No. 175.
2.
Anonymous (1979): Drugs in Live Stock Feed, Vol. 1, Technical report. Office of Technology Assessment, Congress of the United States, Washington , 67 pp.
3.
Atlas, R.M. and Bartha, R. (1987): Microbial Ecology. Fundamentals and Applications . Philippines: Addison-Wesley Publishing Company.
4.
Baer, P.N. and Newton, W.L. (1960): Studies on Periodontal Disease in the Mouse. III. The Germfree Mouse and its Conventional Control, Oral Surg Oral Med Oral Path12:1134-1144.
5.
Baer, P.N.; Newton, W.L.; and White, C.I. (1964): Studies on Periodontal Diseases in the Mouse. VI. The Older Germfree Control, J Periodontol35:22-30.
6.
Barefoot, S.F. and Klaenhammer, T.R. (1983): Detection and Activity of Lactacin B. A Bactcriocin Produced by Lactobacillus acidophilus, App Environ Microbiol45:1808-1815.
7.
Bismuth, R. (1985): Cocci a Gram Positif ct Aminosides. In: L'Antibiogramme, 1st ed., P. Courvalin , F. Goldstein, A. Philipon , and J. Sirot, Eds., Paris: mpc-Videom, pp. 29-39.
8.
Bowden, G.H. and Hamilton, I.R. (1987): Environmental pH as a Factor in the Competition Between Strains of the Oral Streptococci Streptococus mutans, S. sanguis, and "S. mitior" Growing in Continuous Culture, Can J Microbiol33:824-827.
9.
Bryan, L.E. (1984): Aminoglycoside Resistance. In: Antimicrobial Drug Resistance, L.E. Bryan , Ed., Orlando: Academic Press Inc., pp. 241-277.
10.
Clewell, D.B. (1981): Plasmids, Drug Resistance, and Gene Transfer in the Genus Streptococcus, Microbiol Rev45:409-436.
11.
Courvalin, P.; Carlier, C.; and Collatz, E. (1980): Plasmid-mediated Resistance to Aminocyclitol Antibiotics in Group D Streptococci, J Bacteriol143:541-551.
12.
Datta, N. (1984): Plasmids of Enteric Bacteria. In: Antimicrobial Drug Resistance, L.E. Bryan , Ed., Orlando: Academic Press, Inc., pp. 487-496.
13.
Davis, C.P. and Savage, D.W. (1976): Effect of Penicillin on the Succession, Attachment, and Morphology of Segmented, Filamentous Microbes in the Murine Small Bowel , Infect Immun13:180-188.
14.
Deslauriers, N.; Trudel, L.; St-Amand, L.; Seguin, J.; and Lavoie, M.C. (1986): The Mouse as an Experimental Model in Oral Health and Disease, J Dent Res65:785, Abst. No. 535.
15.
Dhillon, T.S. and Dhillon, E.K.S. (1981): Incidence of Lysogeny, Colicinogeny and Drug Resistance in Enterobacteria Isolated from Sewage and from Rectum of Humans and some Domesticated Species, App Environ Microbiol41:894-902.
16.
Donoghue, H.D. and Tyler, J.E. (1975): Antagonisms among Streptococci Isolated from the Human Oral Cavity, Arch Oral Biol20:381-387.
17.
Ducluzeau, R.; Dubos, F.; Raibaud, P.; and Abrams, G.D. (1976): Inhibition of Clostridium perfringens by an Antibiotic Substance Produced by Bacillus licheniformis in the Digestive Tract of Gnotobiotic Mice: Effect on other Bacteria from the Digestive Tract, Antimicrob Agents Chemother9:20-25.
18.
Dumas, C.; Champagne, A.; and Lavoie, M.C. (1987): Proteolytic Activity of Bacteria Isolated from the Oral Cavity of BALB/c Mice Toward Salivary Proteins, J Dent Res66:62-64.
19.
Fitzgerald, R.J. and Fitzgerald, D.B. (1981): The Microbiologic Status of Test Animals in Relation to Caries Research. In: Proceedings, Symposium on Animal Models in Cariology, J.M. Tanzer, Ed. Sp. Supp. Microbiol Abstr, New York: Information Retrieval, Inc., pp. 89-95.
20.
Freter, R. (1976): Factors Controlling the Composition of the Intestinal Microflora. In: Proceedings, Microbial Aspects of Dental Caries , H.N. Stiles, W.J. Loesche, and T.C. O'Brien, Eds., Sp. Supp. Microbiol Abst Vol. 1, Washington : Information Retrieval, Inc., pp. 109-120.
21.
Freter, R.; Brickner, H.; Bottney, M.; Cleven, M.D.; and Aranki, A. (1983): Mechanisms that Control Bacterial Populations in Continuous Flow Culture Models of Mouse Large Intestinal Flora, Infect Immun39:677-685.
22.
Galvez, A.; Maqueda, M.; Valdivia, E.; Quesada, A.; and Mon-Toya, E. (1986): Characterization and Partial Purification of Broad Spectrum Antibiotic AS-48 Produced by Streptococcus faecalis. Can J Microbiol32:765-771.
23.
Gauthier, L.; Vadeboncoeur, C.; and Mayrand, D. (1984): Loss of Sensitivity to Xylitol by Streptococcus mutans LG-1, Caries Res18 :289-295.
24.
Gibbons, R.J. and Socransky, S.S. (1966): Enhancement of Alveolar Bone Loss in Gnotobiotic Mice Harbouring Human Gingival Bacteria, Arch Oral Biol11:847-848.
25.
Horaud, T.; LE Bouguenec, C.; and Pepper, K. (1985): Molecular Genetics of Resistance to Macrolidcs, Lincosamides and Streptogramin B (MLS) in Streptococci, Antimicrob Agents Chemother16:11-135.
26.
Hubert, W.G. (1971): The Impact of Antibiotic Drugs and Residues, Adv Vet Sci Comp Med15:101-132.
27.
Huis In't Veld, J.H.J.; Drost, J.S.; and Havenaar, R. (1982): Establishment and Localization of Mixtures of Streptococcus mutans Serotypes in the Oral Cavity of the Rat, J Dent Res61:1199-1205.
28.
Ike, Y. and Clewell, D.B. (1987): High Incidence of Hemolysin Production by Streptococcus faecalis Strains Associated with Human Parenteral Infections: Structures of Hemolysin Plasmids. In: Streptococcal Genetics , J.J. Ferretti and R. Curtiss III, Eds., Washington: American Society for Microbiology, pp. 159-164.
29.
Jacob, A. and Hobbs, S.J. (1974): Conjugal Transfer of Plasmid-borne Multiple Antibiotic Resistance in Streptococcus faecalis var zymogenes, J Bacteriol117:360-372.
30.
Kadis, V.W. (1983): Biocides in Milk. In: Proceedings of the XXI International Dairy Congress, Vol. 2, Moscow : Mir Publishers, pp. 277-283.
31.
Kamp, E.M.; Drost, J.; Huis I,n't Veld, J.H.J.; Van Palenstein-Helderman, W.H.; and Backer Dirks , O. (1983): Reproducibility of Dental Caries in BALB/c Mice Induced by the Bacterium Streptococcus mutans, Arch Oral Biol28:153-158.
32.
Kamp, E.M.; Huis In't Veld, J.H.J.; Havenaar, R.; and Backer Dirks, O. (1981): Experimental Dental Caries in Mice. In: Proceedings, Symposium on Animal Models in Cariology, J.M. Tanzer, Ed., Sp. Supp. Microbiol Abst, Washington: Information Retrieval, Inc., pp. 121-130.
33.
Kelstrup, J. and Gibbons, R.J. (1969): Bacteriocins from Human and Rodent Streptococci , Arch Oral Biol14:251-258.
34.
Klein, J.; Figueroa, F.; and David, C.S. (1983): H-2 Haplotypes, Genes and Antigens: Second Listing. II. The H-2 Complex, Immunogenetics17 :553-596.
35.
Lampert, L.M. (1975): Modern Dairy Products, 3rd cd., New York: Chemical Publishing Company, Inc., 437 pp.
36.
Lancini, G. and Parenti, F. (1982): Antibiotics. An Integrated View, M.P. Starr, Ed., New York: Springer-Verlag, pp. 124-137.
37.
LeBien, T.W. and Bromel, M.C. (1975): Antibacterial Properties of a Peroxidogenic Strain of Streptococcus mitior (mitis), Can J Microbiol21:101-103.
38.
LeBlanc, D.J.; Inamine, J.M.; and Lee, L.N. (1986): Broad Geographical Distribution of Homologous Erythromycin, Kanamycin and Streptomycin Resistance Determinants among Group D Streptococci of Human and Animal Origin, Antimicrob Agents Chemother29:549-555.
39.
LeBlanc, D.J.; Lee, L.N.; Banai, M.; Rollins, L.D.; and Inamine, J.M. (1987): Dissemination of Streptococcal Antibiotic Resistance Determinants in the Natural Environment. In: Streptococcal Genetics, J.J. Ferretti and R. Curtiss III, Eds., Washington : American Society for Microbiology, pp. 43-53.
40.
LeBlanc, D.J.; Lee, L.N.; Clewell, D.B.; and Behnke, D. (1983): Broad Geographical Distribution of Cytotoxin Gene Mediating Bcta-Hemolysis and Bactcriocin Activity among Streptococcus faecalis Strains, Infect Immun40:1015-1022.
41.
Malke, H.; Stanke, R.; Jacob, H.E.; and Kohler, W. (1974): Bacteriocin-like Activity of Group A Streptococci due to the Production of Peroxide, J Med Microbiol7:367-374.
42.
McDermid, A.S.; McKee, A.S.; Ellwood, D.C.; and Marsh, P.D. (1986): The Effect of Lowering the pH on the Composition and Metabolism of a Community of Nine Oral Bacteria Grown in a Chemostat, J Gen Microbiol132:1205-1214.
43.
Michalek, S.M. and McGhee, J.R. (1977): Virulence of Streptococcus mutans: An Antibiotic-suppressed Rat Model for Studies of Pathogenesis, J Dent Res56:205-211.
44.
Murray, B. (1987): Plasmid-mediated Beta-Lactamase in Enterococcus faecalis. In: Streptococcal Genetics, J.J. Ferretti and R. Curtiss III, Eds. Washington: American Society for Microbiology, pp. 83-86.
45.
Nakamura, T.; Yamazaki, N.; Taniguchi, H.; and Fujimura, S. (1983): Production, Purification, and Properties of a Bacteriocin from Staphylococcus aureus Isolated from Saliva, Infect Immun39:609-614.
46.
Navia, J.M. and Hunt, C.E. (1972): The PBB Mouse: A New Model for Caries Research , IADR Prog & Abst51:249, Abst. No. 807.
47.
Navia, J.M. and Narkates, A.J. (1980): Dental Research. In: The Laboratory Rat, Vol. II, Research Application, American College of Laboratory Animal Medicine Series, H.J. Baker, J.R. Lindsey, and S.H. Weibrogh , Eds., Toronto: Academic Press , pp. 59-74.
48.
Niemi, M.; Sikabor, M.; and Niemela, S. (1983): Antibiotic Resistance among Different Species of Fecal Coliforms Isolated from Water Samples, App Environ Microbiol45:79-83.
49.
Pepper, K.; LE Bouguenec, C.; DE Cespedes, G.; Colmar, I.; and Horaud, T. (1987): Dissemination of a Plasmid-borne Chloramphenicol Resistance Gene in Streptococcal and Enterococcal Clinical Isolates. In: Streptococcal Genetics, J.J. Ferretti and R. Curtiss III, Eds., Washington: American Society for Microbiology, pp. 79-82.
50.
Reeves, P. (1972): The Bacteriocins. Molecular Biology, Biochemistry and Biophysics, Vol. 11, New York: Springer-Verlag, 142 pp.
51.
Rogul, M. and Carr, S.R. (1972): Variable Ammonia Production Among Smooth and Rough Strains of Pseudomonas pseudomallei: Resemblance to Bacteriocin Production , J Bacteriol112:372-380.
52.
Rosen, S. and Williams, H.J. (1969): Comparison of Caries Activity in Gnotobiotic Rats and Mice, IADR Prog & Abst55: Abst No. 57.
53.
Savage, D.C. (1977): Microbial Ecology of the Gastrointestinal Tract , Ann Rev Microbiol31:107-133.
54.
Sharawy, A.M. and Socransky, S.S. (1967): Effect of Human Streptococcus Strain GS-5 on Caries and Alveolar Bone Loss in Conventional Mice and Rats, J Dent Res46:1385.
Stralfors, A.; Carlsson, J.; and Sundqvist, G. (1970): Caries Activity and Prevalence of Streptococcus mutans in Mice Caged Together with Caries Active Hamsters, Caries Res4:124-130.
57.
Tagg, J.R.; Dajani, A.S.; and Wannamaker, L.W. (1976): Bacteriocins of Gram-positive Bacteria, Bacteriol Rev40:722-756.
58.
Tramer, J. (1966): Inhibitory Effect of Lactobacillus acidophilus , Nature (London) 211:204-205.
59.
Trudel, L.; Arriaga-Alba, M.; and Lavoie, M.C. (1984): Survey of Drug and Phage Resistance and Colicin and Hemolysin Production among Coliforms Isolated in the Ivory Coast, App Environ Microbiol48:905-907.
60.
Trudel, L.; St-Amand, L.; Bareil, M.; Cardinal, P.; and Lavoie, M.C. (1986): Bacteriology of the Oral Cavity of BALB/c Mice , Can J Microbiol32:673-678.
61.
Van Der Hoeven, J.S.; De Jong, H.H.; Camp, P.J.M.; and Van Den Kieboom, A. (1985): Competition between Oral Streptococcus Species in the Chemostat under Alternating Conditions of Glucose Limitations and Excess, FEMS Microb Ecol31:313-379.
62.
Van Der Hoeven, J.S. and Rogers, A.H. (1979): Stability of the Resident Microflora and Bacteriocinogeny of Streptococcus mutans as Factors Affecting its Establishment in Specific Pathogen Free Rats, Infect Immun23:206-212.
63.
Walstad, D.L.; Reitz, R.C.; and Sparling, P.F. (1974): Growth Inhibition among Strains of Neisseria gonorrheae due to the Production of Inhibitory Free Fatty Acids and Lysophosphatidyl Ethanolamine: Absence of Bacteriocins, Infect Immun10:481-488.
64.
Watanabe, T. (1960): Transferable Drug Resistance: the Nature of the Problem. In: Bacterial Episomes and Plasmids, G.E.W. Wolstcnholme and M. O'Connor, Eds., Ciba Foundation Symposium, London: J. and A. Churchill Ltd., pp. 81-97.
