Skip to main content
Log in

Inhibitory effect of Lactobacillus reuteri on periodontopathic and cariogenic bacteria

  • Articles
  • Published:
The Journal of Microbiology Aims and scope Submit manuscript

Abstract

The interaction between Lactobacillus reuteri, a probiotic bacterium, and oral pathogenic bacteria have not been studied adequately. This study examined the effects of L. reuteri on the proliferation of periodontopathic bacteria including Aggregatibacter actinomycetemcomitans, Fusobacterium nucleatum, Porphyromonas gingivalis, and Tannerella forsythia, and on the formation of Streptococcus mutans biofilms. Human-derived L. reuteri strains (KCTC 3594 and KCTC 3678) and rat-derived L. reuteri KCTC 3679 were used. All strains exhibited significant inhibitory effects on the growth of periodontopathic bacteria and the formation of S. mutans biofilms. These antibacterial activities of L. reuteri were attributed to the production of organic acids, hydrogen peroxide, and a bacteriocin-like compound. Reuterin, an antimicrobial factor, was produced only by L. reuteri KCTC 3594. In addition, L. reuteri inhibited the production of methyl mercaptan by F. nucleatum and P. gingivalis. Overall, these results suggest that L. reuteri may be useful as a probiotic agent for improving oral health.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Aas, J.A., B.J. Paster, L.N. Stokes, I. Olsen, and F.E. Dewhirst. 2005. Defining the normal bacterial flora of the oral cavity. J. Clin. Microbiol. 43, 5721–5732.

    Article  PubMed  Google Scholar 

  • Abad, C.L. and N. Safdar. 2009. The role of Lactobacillus probiotics in the treatment or prevention of urogenital infections-a systematic review. J. Chemother. 21, 243–252.

    PubMed  CAS  Google Scholar 

  • Ahola, A.J., H. Yli-Knuuttila, T. Suomalainen, T. Poussa, A. Ahlström, J.H. Meurman, and R. Korpela. 2002. Short-term consumption of probiotic-containing cheese and its effect on dental caries risk factors. Arch. Oral Biol. 47, 799–804.

    Article  PubMed  CAS  Google Scholar 

  • Burton, J.P., C.N. Chilcott, and J.R. Tagg. 2005. The rationale and potential for the reduction of oral malodour using Streptococcus salivarius probiotics. Oral Dis. 11, 29–31.

    Article  PubMed  Google Scholar 

  • Çaglar, E., S.K. Cildir, S. Ergeneli, N. Sandalli, and S. Twetman. 2006. Salivary mutans streptococci and lactobacilli levels after ingestion of the probiotic bacterium Lactobacillus reuteri ATCC 55730 by straws or tablets. Acta Odontol. Scand. 64, 314–318.

    Article  PubMed  Google Scholar 

  • Cleusix, V., C. Lacroix, S. Vollenweider, M. Duboux, and G. Le Blay. 2007. Inhibitory activity spectrum of reuterin produced by Lactobacillus reuteri against intestinal bacteria. BMC Microbiol. 7, 101.

    Article  PubMed  Google Scholar 

  • Coli, J.M. and J. Tonzetich. 1992. Characterization of volatile sulphur compounds production at individual gingival crevicular sites in humans. J. Clin. Dent. 3, 97–103.

    PubMed  CAS  Google Scholar 

  • De Boever, E.H. and W.J. Loesche. 1995. Assessing the contribution of anaerobic microflora of the tongue to oral malodor. J. Am. Dent. Assoc. 126, 1384–1393.

    PubMed  Google Scholar 

  • Doleyres, Y., P. Beck, S. Vollenweider, and C. Lacroix. 2005. Production of 3-hydroxypropionaldehyde using a two-step process with Lactobacillus reuteri. Appl. Microbiol. Biotechnol. 68, 467–474.

    Article  PubMed  CAS  Google Scholar 

  • El-Ziney, M.G., T. van den Tempel, J. Debevere, and M. Jakobsen. 1999. Application of reuterin produced by Lactobacillus reuteri 12002 for meat decontamination and preservation. J. Food Prot. 62, 257–261.

    PubMed  CAS  Google Scholar 

  • Eschenbach, D.A., P.R. Davick, B.L. Williams, S.J. Klebanoff, K. Young-Smith, C.M. Critchlow, and K.K. Holmes. 1989. Prevalence of hydrogen peroxide-producing Lactobacillus species in normal women and women with bacterial vaginosis. J. Clin. Microbiol. 27, 251–256.

    PubMed  CAS  Google Scholar 

  • Gill, H.S., Q. Shu, H. Lin, K.J. Rutherfurd, and M.L. Cross. 2001. Protection against translocating Salmonella typhimurium infection in mice by feeding the immuno-enhancing probiotic Lactobacillus rhamnosus strain HN001. Med. Microbiol. Immunol. 190, 97–104.

    PubMed  CAS  Google Scholar 

  • Gilliland, S.E., C.R. Nelson, and C. Maxwell. 1985. Assimilation of cholesterol by Lactobacillus acidophilus. Appl. Environ. Microbiol. 49, 377–381.

    PubMed  CAS  Google Scholar 

  • Haffajee, A.D. and S.S. Socransky. 1994. Microbial etiological agents of destructive periodontal diseases. Periodontol. 2000 5, 78–111.

    Article  PubMed  CAS  Google Scholar 

  • Haffajee, A.D., R.P. Teles, and S.S. Socransky. 2006. Association of Eubacterium nodatum and Treponema denticola with human periodontitis lesions. Oral Microbiol. Immunol. 21, 269–282.

    Article  PubMed  CAS  Google Scholar 

  • Ishihara, K., H. Miyakawa, A. Hasegawa, I. Takazoe, and Y. Kawai. 1985. Growth inhibition of Streptococcus mutans by cellular extracts of human intestinal lactic acid bacteria. Infect. Immun. 49, 692–694.

    PubMed  CAS  Google Scholar 

  • Kang, M.S., E.K. Choi, D.H. Choi, S.Y. Ryu, H.H. Lee, H.C. Kang, J.T. Koh, and et al. 2008. Antibacterial activity of pyrrolidine dithiocarbamate. FEMS Microbiol. Lett. 280, 250–254.

    Article  PubMed  CAS  Google Scholar 

  • Kang, M.S., J. Chung, S.M. Kim, K.H. Yang, and J.S. Oh. 2006a. Effect of Weissella cibaria isolates on the formation of Streptococcus mutans biofilm. Caries Res. 40, 418–425.

    Article  PubMed  Google Scholar 

  • Kang, M.S., B.G. Kim, J. Chung, H.C. Lee, and J.S. Oh. 2006b. Inhibitory effect of Weissella cibaria isolates on the production of volatile sulphur compounds. J. Clin. Periodontol. 33, 226–232.

    Article  PubMed  CAS  Google Scholar 

  • Kasuga, Y., K. Ishihara, and K. Okuda. 2000. Significance of detection of Porphyromonas gingivalis, Bacteroides forsythus and Treponema denticola in periodontal pockets. Bull. Tokyo Dent. Coll. 41, 109–117.

    Article  PubMed  CAS  Google Scholar 

  • Kawamura, Y., X.G. Hou, F. Sultana, H. Miura, and T. Ezaki. 1995. Determination of 16S rRNA sequences of Streptococcus mitis and Streptococcus gordonii and phylogenetic relationships among members of the genus Streptococcus. Int. J. Syst. Bacteriol. 45, 406–408.

    Article  PubMed  CAS  Google Scholar 

  • Kleinberg, I. and G. Westbay. 1992. Salivary and metabolic factors involved in oral malodor formation. J. Periodontol. 63, 768–775.

    PubMed  CAS  Google Scholar 

  • Köll-Klais, P., R. Mändar, E. Leibur, H. Marcotte, L. Hammarström, and M. Mikelsaar. 2005. Oral lactobacilli in chronic periodontitis and periodontal health: species composition and antimicrobial activity. Oral Microbiol. Immunol. 20, 354–361.

    Article  PubMed  Google Scholar 

  • Lancero, H., J. Niu, and P.W. Johnson. 1996. Exposure of periodontal ligament cells to methyl mercaptan reduces intracellular pH and inhibits cell migration. J. Dent. Res. 75, 1994–2002.

    Article  PubMed  CAS  Google Scholar 

  • Loesche, W.J. 1986. Role of Streptococcus mutans in human dental decay. Microbiol. Rev. 50, 353–380.

    PubMed  CAS  Google Scholar 

  • Lüthi-Peng, Q., S. Schärer, and Z. Puhan. 2002. Production and stability of 3-hydroxypropionaldehyde in Lactobacillus reuteri. Appl. Microbiol. Biotechnol. 60, 73–80.

    Article  PubMed  Google Scholar 

  • Mandell, R.L. 1984. A longitudinal microbiological investigation of Actinobacillus actinomycetemcomitans and Eikenella corrodens in juvenile periodontitis. Infect. Immun. 45, 778–780.

    PubMed  CAS  Google Scholar 

  • Meyer, D.H. and P.M. Fives-Taylor. 1997. The role of Actinobacillus actinomycetemcomitans in the pathogenesis of periodontal disease. Trends Microbiol. 5, 224–228.

    Article  PubMed  CAS  Google Scholar 

  • Nikawa, H., S. Makihira, H. Fukushima, H. Nishimura, Y. Ozaki, and K. Ishida. 2004. Lactobacillus reuteri in bovine milk fermented decreases the oral carriage of mutans streptococci. Int. J. Food Microbiol. 95, 219–223.

    Article  PubMed  CAS  Google Scholar 

  • Paster, B.J., S.K. Boches, J.L. Galvin, R.E. Ericson, C.N. Lau, V.A. Levanos, A. Sahasrabudhe, and F.E. Dewhirst. 2001. Bacterial diversity in human subgingival plaque. J. Bacteriol. 183, 3770–3783.

    Article  PubMed  CAS  Google Scholar 

  • Paster, B.J., I. Olsen, J.A. Aas, and F.E. Dewhirst. 2006. The breadth of bacterial diversity in the human periodontal pocket and other oral sites. Periodontol. 2000 42, 80–87.

    Article  Google Scholar 

  • Persson, S., M.B. Edlund, R. Claesson, and J. Carlsson. 1990. The formation of hydrogen sulfide and methyl mercaptan by oral bacteria. Oral Microbiol. Immunol. 5, 195–201.

    Article  PubMed  CAS  Google Scholar 

  • Reid, G., J. Burton, and E. Devillard. 2004. The rationale for probiotics in female urogenital healthcare. MedGenMed. 6, 49.

    PubMed  Google Scholar 

  • Saavedra, J. 2000. Probiotics and infectious diarrhea. Am. J. Gastroenterol. 95, 16–18.

    Article  Google Scholar 

  • Scully, C., M. el-Maaytah, S.R. Porter, and J. Greenman. 1997. Breath odor: etiopathogenesis, assessment and management. Eur. J. Oral Sci. 105, 287–293.

    Article  PubMed  CAS  Google Scholar 

  • Shornikova, A.V., I.A. Casas, H. Mykkänen, E. Salo, and T. Vesikari. 1997. Bacteriotherapy with Lactobacillus reuteri in rotavirus gastroenteritis. Pediatr. Infect. Dis. J. 16, 1103–1107.

    Article  PubMed  CAS  Google Scholar 

  • Slininger, P.J., R.J. Bothast, and K.L. Smiley. 1983. Production of 3-hydroxypropionaldehyde from glycerol. Appl. Environ. Microbiol. 46, 62–67.

    PubMed  CAS  Google Scholar 

  • Slots, J. and M. Ting. 1999. Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis in human periodontal disease: occurrence and treatment. Periodontol. 2000 20, 82–121.

    Article  PubMed  CAS  Google Scholar 

  • Socransky. S.S., A.D. Haffajee, M.A. Cugini, C. Smith, and R.L. Kent, Jr. 1998. Microbial complexes in subgingival plaque. J. Clin. Periodontol. 25, 134–144.

    Article  PubMed  CAS  Google Scholar 

  • Spinler, J.K., M. Taweechotipatr, C.L. Rognerud, C.N. Ou, S. Tumwasorn, and J. Versalovic. 2008. Human-derived probiotic Lactobacillus reuteri demonstrate antimicrobial activities targeting diverse enteric bacterial pathogens. Anaerobe 14, 166–171.

    Article  PubMed  CAS  Google Scholar 

  • Szajewska, H. and J.Z. Mrukowicz. 2005. Use of probiotics in children with acute diarrhea. Paediatr. Drugs 7, 111–122.

    Article  PubMed  Google Scholar 

  • Talarico, T.L., I.A. Casas, T.C. Chung, and W.J. Dobrogosz. 1988. Production and isolation of reuterin, a growth inhibitor produced by Lactobacillus reuteri. Antimicrob. Agents Chemother. 32, 1854–1858.

    PubMed  CAS  Google Scholar 

  • Taniguchi, M., H. Nakazawa, O. Takeda, T. Kaneko, K. Hoshino, and T. Tanaka. 1998. Production of a mixture of antimicrobial organic acids from lactose by co-culture of Bifidobacterium longum and Propionibacterium freudenreichii. Biosci. Biotechnol. Biochem. 62, 1522–1527.

    Article  PubMed  CAS  Google Scholar 

  • Tonzetich, J. 1971. Direct gas chromatographic analysis of sulphur compounds in mouth air in man. Arch. Oral Biol. 16, 587–597.

    Article  PubMed  CAS  Google Scholar 

  • van Winkelhoff, A.J., B.G. Loos, W.A. van der Reijden, and U. van der Velden. 2002. Porphyromonas gingivalis, Bacteroides forsythus and other putative periodontal pathogens in subjects with and without periodontal destruction. J. Clin. Periodontol. 29, 1023–1028.

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Seon-Mi Kim.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kang, MS., Oh, JS., Lee, HC. et al. Inhibitory effect of Lactobacillus reuteri on periodontopathic and cariogenic bacteria. J Microbiol. 49, 193–199 (2011). https://doi.org/10.1007/s12275-011-0252-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12275-011-0252-9

Keywords

Navigation