Clinical and microbiological effects of Lactobacillus reuteri probiotics in the treatment of chronic periodontitis: a randomized placebo-controlled study

Wim Teughels, Andaç Durukan, Onur Ozcelik, Martine Pauwels, Marc Quirynen, Mehmet Cenk Haytac, Wim Teughels, Andaç Durukan, Onur Ozcelik, Martine Pauwels, Marc Quirynen, Mehmet Cenk Haytac

Abstract

Aim: The aim of this randomized placebo-controlled clinical trial was to evaluate the effects of Lactobacillus reuteri-containing probiotic lozenges as an adjunct to scaling and root planing (SRP).

Material and methods: Thirty chronic periodontitis patients were recruited and monitored clinically and microbiologically at baseline, 3, 6, 9 and 12 weeks after therapy. All patients received one-stage full-mouth disinfection and randomly assigned over a test (SRP + probiotic, n = 15) or control (SRP + placebo, n = 15) group. The lozenges were used two times a day for 12 weeks.

Results: At week 12, all clinical parameters were significantly reduced in both groups, while there was significantly more pocket depth reduction (p < 0.05) and attachment gain (p < 0.05) in moderate and deep pockets; more Porphyromonas gingivalis reduction was observed in the SRP + probiotic group.

Conclusions: The results indicate that oral administration of L. reuteri lozenges could be a useful adjunct to SRP in chronic periodontitis.

Keywords: Lactobacillus reuteri; microbiology; periodontitis; probiotics; scaling and root planing; treatment.

© 2013 The Authors. Journal of Clinical Periodontology published by John Wiley & Sons Ltd.

Figures

Figure 1
Figure 1
Flow chart

References

    1. Adams CA. The probiotic paradox: live and dead cells are biological response modifiers. Nutritional Research Reviews. 2010;23:37–46.
    1. Boutaga K, van Winkelhoff AJ, Vandenbroucke-Grauls CM, Savelkoul PH. Comparison of real-time PCR and culture for detection of Porphyromonas gingivalis in subgingival plaque samples. Journal of Clinical Microbiology. 2003;41:4950–4954.
    1. Boutaga K, van Winkelhoff AJ, Vandenbroucke-Grauls CM, Savelkoul PH. Periodontal pathogens: a quantitative comparison of anaerobic culture and real-time PCR. FEMS Immunology and Medical Microbiology. 2005;45:191–199.
    1. Broekaert IJ, Walker WA. Probiotics and chronic disease. Journal of Clinical Gastroenterology. 2006;40:270–274.
    1. Caglar E, Topcuoglu N, Cildir SK, Sandalli N, Kulekci G. Oral colonization by Lactobacillus reuteri ATCC 55730 after exposure to probiotics. International Journal of Paediatric Dentistry. 2009;19:377–381.
    1. Cionca N, Giannopoulou C, Ugolotti G, Mombelli A. Amoxicillin and metronidazole as an adjunct to full-mouth scaling and root planing of chronic periodontitis. Journal of Periodontology. 2009;80:364–371.
    1. Darveau RP, Hajishengallis G, Curtis MA. Porphyromonas gingivalis as a potential community activist for disease. Journal of Dental Research. 2012;91:816–820.
    1. Dommels YE, Kemperman RA, Zebregs YE, Draaisma RB, Jol A, Wolvers DA, Vaughan EE, Albers R. Survival of Lactobacillus reuteri DSM 17938 and Lactobacillus rhamnosus GG in the human gastrointestinal tract with daily consumption of a low-fat probiotic spread. Applied Environmental Microbiology. 2009;75:6198–6204.
    1. Feres M, Soares GM, Mendes JA, Silva MP, Faveri M, Teles R, Socransky SS, Figueiredo LC. Metronidazole alone or with amoxicillin as adjuncts to non-surgical treatment of chronic periodontitis: a 1-year double-blinded, placebo-controlled, randomized clinical trial. Journal of Clinical Periodontology. 2012;39:1149–1158.
    1. Haffajee AD, Teles RP, Socransky SS. The effect of periodontal therapy on the composition of the subgingival microbiota. Periodontology 2000. 2006;42:219–258.
    1. Hallstrom H, Lindgren S, Yucel-Lindberg T, Dahlen G, Renvert S, Twetman S. Effect of probiotic lozenges on inflammatory reactions and oral biofilm during experimental gingivitis. Acta Odontologica Scandinavia. 2013;71:828–833.
    1. Harini PM, Anegundi RT. Efficacy of a probiotic and chlorhexidine mouth rinses: a short-term clinical study. Journal of the Indian Society of Pedodontics and Preventive Dentistry. 2010;28:179–182.
    1. Iniesta M, Herrera D, Montero E, Zurbriggen M, Matos AR, Marin MJ, Sanchez-Beltran MC, Llama-Palacio A, Sanz M. Probiotic effects of orally administered Lactobacillus reuteri-containing tablets on the subgingival and salivary microbiota in patients with gingivitis. A randomized clinical trial. Journal of Clinical Periodontology. 2012;39:736–744.
    1. Ishikawa H, Aiba Y, Nakanishi M, Oh-hashi Y, Koga Y. Suppression of periodontal pathogenic bacteria in the saliva of humans by the administration of Lactobacillus salivarius TI 2711. Journal of the Japanese Society of Periodontology. 2003;45:105–112.
    1. Jacobsen CN, Rosenfeldt NV, Hayford AE, Moller PL, Michaelsen KF, Paerregaard A, Sandstrom B, Tvede M, Jakobsen M. Screening of probiotic activities of forty-seven strains of Lactobacillus spp. by in vitro techniques and evaluation of the colonization ability of five selected strains in humans. Applied Environmental Microbiology. 1999;65:4949–4956.
    1. Kang MS, Chung J, Kim SM, Yang KH, Oh JS. Effect of Weissella cibaria isolates on the formation of Streptococcus mutans biofilm. Caries Research. 2006;40:418–425.
    1. Krasse P, Carlsson B, Dahl C, Paulsson A, Nilsson A, Sinkiewicz G. Decreased gum bleeding and reduced gingivitis by the probiotic Lactobacillus reuteri. Swedish Dental Journal. 2005;30:55–60.
    1. Lang NP, Tonetti MS. Periodontal risk assessment (PRA) for patients in supportive periodontal therapy (SPT) Oral Health and Preventive Dentistry. 2003;1:7–16.
    1. Löe H, Silness J. Periodontal disease in pregnancy I. Prevalence and severity. Acta Odontologica Scandinavia. 1963;21:533–551.
    1. Matsuoka T, Sugano N, Takigawa S, Takane M, Yoshinuma N, Ito K, Koga Y. Effect of oral Lactobacillus salivarius TI 2711 administration on periodontopathic bacteria in subgingival plaque. Journal of the Japanese Society of Periodontology. 2006;48:315–324.
    1. Mayanagi G, Kimura M, Nakaya S, Hirata H, Sakamoto M, Benno Y, Shimauchi H. Probiotic effects of orally administered Lactobacillus salivarius WB21-containing tablets on periodontopathic bacteria: a double-blinded, placebo-controlled, randomized clinical trial. Journal of Clinical Periodontology. 2009;36:506–513.
    1. Mestnik MJ, Feres M, Figueiredo LC, Soares G, Teles RP, Fermiano D, Duarte PM, Faveri M. The effects of adjunctive metronidazole plus amoxicillin in the treatment of generalized aggressive periodontitis: a 1-year double-blinded, placebo-controlled, randomized clinical trial. Journal of Clinical Periodontology. 2012;39:955–961.
    1. Meurman JH. Probiotics: do they have a role in oral medicine and dentistry? European Journal of Oral Sciences. 2005;113:188–196.
    1. Pham LC, van Spanning RJ, Roling WF, Prosperi AC, Terefework Z, Ten Cate JM, Crielaard W, Zaura E. Effects of probiotic Lactobacillus salivarius W24 on the compositional stability of oral microbial communities. Archives of Oral Biology. 2009;54:132–137.
    1. Quirynen M, De Soete M, Boschmans G, Pauwels M, Coucke W, Teughels W, van Steenberghe D. Benefit of “one-stage full-mouth disinfection” is explained by disinfection and root planing within 24 hours: a randomized controlled trial. Journal of Clinical Periodontology. 2006;33:639–647.
    1. Quirynen M, Teughels W, De Soete M, van Steenberghe D. Topical antiseptics and antibiotics in the initial therapy of chronic adult periodontitis: microbiological aspects. Periodontology 2000. 2002;28:72–90.
    1. Riccia DN, Bizzini F, Perilli MG, Polimeni A, Trinchieri V, Amicosante G, Cifone MG. Anti-inflammatory effects of Lactobacillus brevis (CD2) on periodontal disease. Oral Diseases. 2007;13:376–385.
    1. Romani VN, Hasslof P, Keller MK, Granstrom E, Roos S, Twetman S, Stecksen-Blicks C. Lactobacillus reuteri influences regrowth of Mutans streptococci after Full-Mouth Disinfection: a double-blind, randomised controlled trial. Caries Research. 2013;47:338–345.
    1. Salvi GE, Lang NP. The effects of non-steroidal anti-inflammatory drugs (selective and non-selective) on the treatment of periodontal diseases. Current Pharmaceutical Design. 2005;11:1757–1769.
    1. Sanz M, Quirynen M. Advances in the aetiology of periodontitis. Group A consensus report of the 5th European Workshop in Periodontology. Journal of Clinical Periodontology. 2005;32(Suppl. 6):54–56.
    1. Sanz M, van Winkelhoff AJ. Periodontal infections: understanding the complexity–consensus of the Seventh European Workshop on Periodontology. Journal of Clinical Periodontology. 2011;38(Suppl. 11):3–6.
    1. Shelburne CE, Prabhu A, Gleason RM, Mullally BH, Coulter WA. Quantitation of Bacteroides forsythus in subgingival plaque comparison of immunoassay and quantitative polymerase chain reaction. Journal of Microbiological Methods. 2000;39:97–107.
    1. Silness J, Löe H. Periodontal disease in pregnancy. II. Correlation between oral hygiene and periodontal condition. Acta Odontologica Scandinavia. 1964;22:121–135.
    1. Slots J, Rams TE. New views on periodontal microbiota in special patient categories. Journal of Clinical Periodontology. 1991;18:411–420.
    1. Socransky SS, Haffajee AD. The bacterial etiology of destructive periodontal disease: current concepts. Journal of Periodontology. 1992;63:322–331.
    1. Socransky SS, Haffajee AD. Dental biofilms: difficult therapeutic targets. Periodontology 2000. 2002;28:12–55.
    1. Sugano N, Ito K. Nicotine switches the form of H(2)O(2)-induced cell death from apoptosis to necrosis in U937 cells. Immunology Letters. 2000;72:163–166.
    1. Teughels W, Loozen G, Quirynen M. Do probiotics offer opportunities to manipulate the periodontal oral microbiota? Journal of Clinical Periodontology. 2011;38(Suppl. 11):159–177.
    1. Teughels W, Newman MG, Coucke W, Haffajee AD, van der Mei HC, Haake SK, Schepers E, Cassiman JJ, Van Eldere J, van Steenberghe D, Quirynen M. Guiding periodontal pocket recolonization: a proof of concept. Journal of Dental Research. 2007;86:1078–1082.
    1. Teughels W, Van Essche M, Sliepen I, Quirynen M. Probiotics and oral healthcare. Periodontology 2000. 2008;48:111–147.
    1. Twetman S, Derawi B, Keller M, Ekstrand K, Yucel-Lindberg T, Stecksen-Blicks C. Short-term effect of chewing gums containing probiotic Lactobacillus reuteri on the levels of inflammatory mediators in gingival crevicular fluid. Acta Odontologica Scandinavia. 2009;67:19–24.
    1. Van Assche N, Van Essche M, Pauwels M, Teughels W, Quirynen M. Do periodontopathogens disappear after full-mouth tooth extraction? Journal of Clinical Periodontology. 2009;36:1043–1047.
    1. Van der Velden U. Purpose and problems of periodontal disease classification. Periodontology 2000. 2005;39:13–21.
    1. Vivekananda MR, Vandana KL, Bhat KG. Effect of the probiotic Lactobacilli reuteri (Prodentis) in the management of periodontal disease: a preliminary randomized clinical trial. Journal of Oral Microbiology. 2010;2:5344. doi: .
    1. Wolff L, Dahlen G, Aeppli D. Bacteria as risk markers for periodontitis. Journal of Periodontology. 1994;65:498–510.
    1. Zahradnik RT, Magnusson I, Walker C, McDonell E, Hillman CH, Hillman JD. Preliminary assessment of safety and effectiveness in humans of ProBiora(3), a probiotic mouthwash. Journal of Applied Microbiology. 2009;107:682–690.

Source: PubMed

Sponsors and Collaborators

Medical Conditions

Drug Interventions

3
Subscribe