[en] AIM: To examine the adjunctive effect of a Lactobacillus reuteri probiotic (ATCC PTA 5289 & DSM 17938) on the re-instrumentation of residual pockets. MATERIALS AND METHODS: This randomized, double-blind, placebo-controlled study included 39 previously non-surgically treated periodontitis patients. A re-instrumentation was carried out, and probiotic and/or placebo drops were applied according to the study protocoll. Patients afterwards received lozenges to use 2×/day for 12 weeks. Probing pocket depth (PPD), recession, bleeding on probing and plaque levels were analysed, next to the microbiological impact. RESULTS: No effects of the probiotic drops could be found. However, after 24 weeks, the overall PPD in the probiotic lozenges group (2.64 ± 0.33 mm) was significantly lower compared to the control lozenges (2.92 ± 0.42 mm). This difference was even more pronounced in moderate (4-6 mm) and deep (≥7 mm) pockets. In the probiotic lozenges group, there were also significantly more pockets converting from ≥4 mm at baseline to ≤3 mm at 24 weeks (67 ± 18% versus 54 ± 17%) and less sites in need for surgery (4 ± 4% versus 8 ± 6%). However, the probiotic products did not influence the microbiological counts of the periodontopathogens. CONCLUSION: The adjunctive consumption of L. reuteri lozenges after re-instrumentation improved the PPD reduction, without an impact on pocket colonization with periodontopathogens.
Research Center/Unit :
d‐BRU - Dental Biomaterials Research Unit - ULiège
Disciplines :
Dentistry & oral medicine
Author, co-author :
Laleman, Isabelle ; Centre Hospitalier Universitaire de Liège - CHU > > Service de parodontologie, chirurgie bucco-dentaire et chirurgie implantaire ; Department of Oral Health Sciences, KU Leuven & Dentistry, University Hospitals
Pauwels, Martine; Department of Oral Health Sciences, KU Leuven & Dentistry, University Hospitals
Quirynen, Marc; Department of Oral Health Sciences, KU Leuven & Dentistry, University Hospitals
Teughels, Wim; Department of Oral Health Sciences, KU Leuven & Dentistry, University Hospitals
Language :
English
Title :
A dual-strain Lactobacilli reuteri probiotic improves the treatment of residual pockets: A randomized controlled clinical trial.
Armitage, G. C. (1999). Development of a classification system for periodontal diseases and conditions. Annals of Periodontology, 4, 1–6. https://doi.org/10.1902/annals.1999.4.1.1
Becker, W., Becker, B. E., Caffesse, R., Kerry, G., Ochsenbein, C., Morrison, E., & Prichard, J. (2001). A longitudinal study comparing scaling, osseous surgery, and modified Widman procedures: Results after 5 years. Journal of Periodontology, 72, 1675–1684. https://doi.org/10.1902/jop.2001.72.12.1675
Campos, G. N., Pimentel, S. P., Ribeiro, F. V., Casarin, R. C., Cirano, F. R., Saraceni, C. H., & Casati, M. Z. (2013). The adjunctive effect of photodynamic therapy for residual pockets in single-rooted teeth: A randomized controlled clinical trial. Lasers in Medical Science, 28, 317–324. https://doi.org/10.1007/s10103-012-1159-3
Cappuyns, I., Cionca, N., Wick, P., Giannopoulou, C., & Mombelli, A. (2012). Treatment of residual pockets with photodynamic therapy, diode laser, or deep scaling. A randomized, split-mouth controlled clinical trial. Lasers in Medical Science, 27, 979–986. https://doi.org/10.1007/s10103-011-1027-6
Carvalho, V. F., Andrade, P. V., Rodrigues, M. F., Hirata, M. H., Hirata, R. D., Pannuti, C. M., … Conde, M. C. (2015). Antimicrobial photodynamic effect to treat residual pockets in periodontal patients: A randomized controlled clinical trial. Journal of Clinical Periodontology, 42, 440–447. https://doi.org/10.1111/jcpe.12393
Caton, J. G., Armitage, G., Berglundh, T., Chapple, I. L. C., Jepsen, S., Kornman, K. S., … Tonetti, M. S. (2018). A new classification scheme for periodontal and peri-implant diseases and conditions – Introduction and key changes from the 1999 classification. Journal of Periodontology, 89(Suppl 1), S1–S8. https://doi.org/10.1002/jper.18-0157
Claffey, N., & Egelberg, J. (1995). Clinical indicators of probing attachment loss following initial periodontal treatment in advanced periodontitis patients. Journal of Clinical Periodontology, 22, 690–696. https://doi.org/10.1111/j.1600-051X.1995.tb00828.x
Della Riccia, D. N., Bizzini, F., Perilli, M. G., Polimeni, A., Trinchieri, V., Amicosante, G., & Cifone, M. G. (2007). Anti-inflammatory effects of Lactobacillus brevis (CD2) on periodontal disease. Oral Diseases, 13, 376–385. https://doi.org/10.1111/j.1601-0825.2006.01291.x
Feng, H. S., Bernardo, C. C., Sonoda, L. L., Hayashi, F., Romito, G. A., De Lima, L. A., … Pannuti, C. M. (2011). Subgingival ultrasonic instrumentation of residual pockets irrigated with essential oils: A randomized controlled trial. Journal of Clinical Periodontology, 38, 637–643. https://doi.org/10.1111/j.1600-051X.2011.01725.x
Hallstrom, H., Lindgren, S., Widen, C., Renvert, S., & Twetman, S. (2016). Probiotic supplements and debridement of peri-implant mucositis: A randomized controlled trial. Acta Odontologica Scandinavica, 74, 60–66. https://doi.org/10.3109/00016357.2015.1040065
Hallstrom, H., Lindgren, S., Yucel-Lindberg, T., Dahlen, G., Renvert, S., & Twetman, S. (2013). Effect of probiotic lozenges on inflammatory reactions and oral biofilm during experimental gingivitis. Acta Odontologica Scandinavia, 71, 828–833. https://doi.org/10.3109/00016357.2012.734406
Harini, P. M., & Anegundi, R. T. (2010). Efficacy of a probiotic and chlorhexidine mouth rinses: A short-term clinical study. Journal of Indian Society of Pedodontics and Preventive Dentistry, 28, 179–182. https://doi.org/10.4103/0970-4388.73799
Heitz-Mayfield, L. J. (2005). How effective is surgical therapy compared with nonsurgical debridement? Periodontology 2000, 37, 72–87. https://doi.org/10.1111/j.1600-0757.2004.03797.x
Hill, C., Guarner, F., Reid, G., Gibson, G. R., Merenstein, D. J., Pot, B., … Sanders, M. E. (2014). Expert consensus document. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nature Reviews Gastroenterology & Hepatology, 11, 506–514. https://doi.org/10.1038/nrgastro.2014.66
Ince, G., Gursoy, H., Ipci, S. D., Cakar, G., Emekli-Alturfan, E., & Yilmaz, S. (2015). Clinical and biochemical evaluation of lozenges containing lactobacillus reuteri as an adjunct to non-surgical periodontal therapy in chronic periodontitis. Journal of Periodontology, 86, 746–754. https://doi.org/10.1902/jop.2015.140612
Iniesta, M., Herrera, D., Montero, E., Zurbriggen, M., Matos, A. R., Marin, M. J., … Sanz, M. (2012). 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, 39, 736–744.
Jenkins, W. M., Said, S. H., Radvar, M., & Kinane, D. F. (2000). Effect of subgingival scaling during supportive therapy. Journal of Clinical Periodontology, 27, 590–596. https://doi.org/10.1034/j.1600-051x.2000.027008590.x
Konig, J., Schwahn, C., Fanghanel, J., Plotz, J., Hoffmann, T., & Kocher, T. (2008). Repeated scaling versus surgery in young adults with generalized advanced periodontitis. Journal of Periodontology, 79, 1006–1013. https://doi.org/10.1902/jop.2008.070380
Krasse, P., Carlsson, B., Dahl, C., Paulsson, A., Nilsson, A., & Sinkiewicz, G. (2005). Decreased gum bleeding and reduced gingivitis by the probiotic Lactobacillus reuteri. Swedish Dental Journal, 30, 55–60.
Laleman, I., Cortellini, S., De Winter, S., Rodriguez Herrero, E., Dekeyser, C., Quirynen, M., & Teughels, W. (2017). Subgingival debridement: End point, methods and how often? Periodontol 2000, 75(1):189–204. https://doi.org/10.1111/prd.12204. Review. PMID:28758304.
Laleman, I., Yilmaz, E., Ozcelik, O., Haytac, C., Pauwels, M., Herrero, E. R., … Teughels, W. (2015). The effect of a streptococci containing probiotic in periodontal therapy: A randomized controlled trial. Journal of Clinical Periodontology, 42, 1032–1041. https://doi.org/10.1111/jcpe.12464
Martin-Cabezas, R., Davideau, J. L., Tenenbaum, H., & Huck, O. (2016). Clinical efficacy of probiotics as an adjunctive therapy to non-surgical periodontal treatment of chronic periodontitis: A systematic review and meta-analysis. Journal of Clinical Periodontology, 43, 520–530. https://doi.org/10.1111/jcpe.12545
Matuliene, G., Pjetursson, B. E., Salvi, G. E., Schmidlin, K., Bragger, U., Zwahlen, M., & Lang, N. P. (2008). Influence of residual pockets on progression of periodontitis and tooth loss: Results after 11 years of maintenance. Journal of Clinical Periodontology, 35, 685–695. https://doi.org/10.1111/j.1600-051X.2008.01245.x
Mendonca, A. C., Santos, V. R., Ribeiro, F. V., Lima, J. A., Miranda, T. S., Feres, M., & Duarte, P. M. (2012). Surgical and non-surgical therapy with systemic antimicrobials for residual pockets in type 2 diabetics with chronic periodontitis: A pilot study. Journal of Clinical Periodontology, 39, 368–376. https://doi.org/10.1111/j.1600-051X.2012.01860.x
Patel, A. M., Richards, P. S., Wang, H. L., & Inglehart, M. R. (2006). Surgical or non-surgical periodontal treatment: Factors affecting patient decision making. Journal of Periodontology, 77, 678–683. https://doi.org/10.1902/jop.2006.050206
Salvi, G. E., Mombelli, A., Mayfield, L., Rutar, A., Suvan, J., Garrett, S., & Lang, N. P. (2002). Local antimicrobial therapy after initial periodontal treatment. Journal of Clinical Periodontology, 29, 540–550.
Schlagenhauf, U., Jakob, L., Eigenthaler, M., Segerer, S., Jockel-Schneider, Y., & Rehn, M. (2016). Regular consumption of Lactobacillus reuteri-containing lozenges reduces pregnancy gingivitis: An RCT. Journal of Clinical Periodontology, 43, 948–954. https://doi.org/10.1111/jcpe.12606
Serino, G., Rosling, B., Ramberg, P., Hellstrom, M. K., Socransky, S. S., & Lindhe, J. (2001a). The effect of systemic antibiotics in the treatment of patients with recurrent periodontitis. Journal of Clinical Periodontology, 28, 411–418. https://doi.org/10.1034/j.1600-051x.2001.028005411.x
Serino, G., Rosling, B., Ramberg, P., Socransky, S. S., & Lindhe, J. (2001b). Initial outcome and long-term effect of surgical and non-surgical treatment of advanced periodontal disease. Journal of Clinical Periodontology, 28, 910–916. https://doi.org/10.1034/j.1600-051x.2001.028010910.x
Shimauchi, H., Mayanagi, G., Nakaya, S., Minamibuchi, M., Ito, Y., Yamaki, K., & Hirata, H. (2008). Improvement of periodontal condition by probiotics with Lactobacillus salivarius WB21: A randomized, double-blind, placebo-controlled study. Journal of Clinical Periodontology, 35, 897–905.
Shiovitz, T. M., Bain, E. E., McCann, D. J., Skolnick, P., Laughren, T., Hanina, A., & Burch, D. (2016). Mitigating the effects of nonadherence in clinical trials. Journal of Clinical Pharmacology, 56, 1151–1164. https://doi.org/10.1002/jcph.689
Smiley, C. J., Tracy, S. L., Abt, E., Michalowicz, B. S., John, M. T., Gunsolley, J., … Hanson, N. (2015). Systematic review and meta-analysis on the nonsurgical treatment of chronic periodontitis by means of scaling and root planing with or without adjuncts. Journal of the American Dental Association, 146, 508–524.e505. https://doi.org/10.1016/j.adaj.2015.01.028
Szkaradkiewicz, A. K., Stopa, J., & Karpinski, T. M. (2014). Effect of oral administration involving a probiotic strain of Lactobacillus reuteri on pro-inflammatory cytokine response in patients with chronic periodontitis. Archivum Immunolgiae Et Therapiae Experimentalis, 62, 495–500. https://doi.org/10.1007/s00005-014-0277-y
Tekce, M., Ince, G., Gursoy, H., Dirikan Ipci, S., Cakar, G., Kadir, T., & Yilmaz, S. (2015). Clinical and microbiological effects of probiotic lozenges in the treatment of chronic periodontitis: A 1-year follow-up study. Journal of Clinical Periodontology, 42, 363–372. https://doi.org/10.1111/jcpe.12387
Teughels, W., Durukan, A., Ozcelik, O., Pauwels, M., Quirynen, M., & Haytac, M. C. (2013). Clinical and microbiological effects of Lactobacillus reuteri probiotics in the treatment of chronic periodontitis: A randomized placebo-controlled study. Journal of Clinical Periodontology, 40, 1025–1035.
Tomasi, C., Koutouzis, T., & Wennstrom, J. L. (2008). Locally delivered doxycycline as an adjunct to mechanical debridement at retreatment of periodontal pockets. Journal of Periodontology, 79, 431–439. https://doi.org/10.1902/jop.2008.070383
Tonetti, M. S., Greenwell, H., & Kornman, K. S. (2018). Staging and grading of periodontitis: Framework and proposal of a new classification and case definition. Journal of Clinical Periodontology, 45, S149–S161. https://doi.org/10.1111/jcpe.12945
Twetman, S., Derawi, B., Keller, M., Ekstrand, K., Yucel-Lindberg, T., & Stecksen-Blicks, C. (2009). Short-term effect of chewing gums containing probiotic Lactobacillus reuteri on the levels of inflammatory mediators in gingival crevicular fluid. Acta Odontologica Scandinavica, 67, 19–24. https://doi.org/10.1080/00016350802516170
Vicario, M., Santos, A., Violant, D., Nart, J., & Giner, L. (2013). Clinical changes in periodontal subjects with the probiotic Lactobacillus reuteri Prodentis: A preliminary randomized clinical trial. Acta Odontologica Scandinavica, 71, 813–819. https://doi.org/10.3109/00016357.2012.734404
Vivekananda, M. R., Vandana, K. L., & Bhat, K. G. (2010). Effect of the probiotic Lactobacilli reuteri (Prodentis) in the management of periodontal disease: A preliminary randomized clinical trial. Journal of Oral Microbiology, 2.
Wennstrom, J. L., Tomasi, C., Bertelle, A., & Dellasega, E. (2005). Full-mouth ultrasonic debridement versus quadrant scaling and root planing as an initial approach in the treatment of chronic periodontitis. Journal of Clinical Periodontology, 32, 851–859. https://doi.org/10.1111/j.1600-051X.2005.00776.x
