Adjunctive probiotics after periodontal debridement versus placebo: a systematic review and meta-analysis

References

• Tonetti MS, Jepsen S, Jin L, et al. Impact of the global burden of periodontal diseases on health, nutrition and wellbeing of mankind: a call for global action. J Clin Periodontol. 2017;44(5):456–462.
   PubMed Web of Science ®Google Scholar
• Ng E, Tay JRH, Balan P, et al. Metagenomic sequencing provides new insights into the subgingival bacteriome and aetiopathology of periodontitis. J Periodontal Res. 2021.
   PubMed Web of Science ®Google Scholar
• Loos BG, Van Dyke TE. The role of inflammation and genetics in periodontal disease. Periodontology 2000. 2020;83(1):26–39.
   PubMed Web of Science ®Google Scholar
• Preshaw PM, Holliday R, Law H, et al. Outcomes of non-surgical periodontal treatment by dental hygienists in training: impact of site- and patient-level factors. Int J Dent Hyg. 2013;11(4):273–279.
   PubMed Web of Science ®Google Scholar
• Hughes FJ, Syed M, Koshy B, et al. Prognostic factors in the treatment of generalized aggressive periodontitis: I. Clinical features and initial outcome. J Clin Periodontol. 2006;33(9):663–670.
   PubMed Web of Science ®Google Scholar
• Teughels W, Feres M, Oud V, et al. Adjunctive effect of systemic antimicrobials in periodontitis therapy. A systematic review and meta-analysis. J Clin Periodontol. 2020;47(S22):257–281.
   PubMed Web of Science ®Google Scholar
• Herrera D, Matesanz P, Martin C, et al. Adjunctive effect of locally delivered antimicrobials in periodontitis therapy: a systematic review and meta-analysis. J Clin Periodontol. 2020;47 (Suppl 22):239–256.
   PubMed Web of Science ®Google Scholar
• Salvi GE, Stahli A, Schmidt JC, et al. Adjunctive laser or antimicrobial photodynamic therapy to non-surgical mechanical instrumentation in patients with untreated periodontitis: a systematic review and meta-analysis. J Clin Periodontol. 2020;47(S22):176–198.
   PubMed Web of Science ®Google Scholar
• Figuero E, Herrera D, Tobias A, et al. Efficacy of adjunctive anti-plaque chemical agents in managing gingivitis: a systematic review and network meta-analyses. J Clin Periodontol. 2019;46(7):723–739.
   PubMed Web of Science ®Google Scholar
• van Winkelhoff AJ, Herrera D, Oteo A, et al. Antimicrobial profiles of periodontal pathogens isolated from periodontitis patients in The Netherlands and Spain. J Clin Periodontol. 2005;32(8):893–898.
   PubMed Web of Science ®Google Scholar
• Llor C, Sierra N, Hernandez S, et al. The higher the number of daily doses of antibiotic treatment in lower respiratory tract infection the worse the compliance. J Antimicrob Chemother. 2008;63(2):396–399.
   PubMed Web of Science ®Google Scholar
• Matsubara VH, Bandara HM, Ishikawa KH, et al. The role of probiotic bacteria in managing periodontal disease: a systematic review. Expert Rev Anti Infect Ther. 2016;14(7):643–655.
   PubMed Web of Science ®Google Scholar
• Hajishengallis G, Chavakis T, Lambris JD. Current understanding of periodontal disease pathogenesis and targets for host-modulation therapy. Periodontology 2000. 2020;84(1):14–34.
   PubMed Web of Science ®Google Scholar
• Ng E, Tay JRH, Ong MMA, et al. Probiotic therapy for periodontal and peri-implant health - silver bullet or sham? Benef Microbes. 2021.
   PubMed Web of Science ®Google Scholar
• Teughels W, Loozen G, Quirynen M. Do probiotics offer opportunities to manipulate the periodontal oral microbiota? J Clin Periodontol. 2011;38(Suppl 11):159–177.
   PubMed Web of Science ®Google Scholar
• Stamatova I, Meurman JH. Probiotics and periodontal disease. Periodontology 2000. 2009;51:141–151.
   PubMed Web of Science ®Google Scholar
• Haukioja A, Loimaranta V, Tenovuo J. Probiotic bacteria affect the composition of salivary pellicle and streptococcal adhesion in vitro. Oral Microbiol Immunol. 2008;23(4):336–343.
   PubMedGoogle Scholar
• Haukioja A, Yli-Knuuttila H, Loimaranta V, et al. Oral adhesion and survival of probiotic and other lactobacilli and bifidobacteria in vitro. Oral Microbiol Immunol. 2006;21(5):326–332.
   PubMedGoogle Scholar
• Keller MK, Hasslof P, Stecksen-Blicks C, et al. Co-aggregation and growth inhibition of probiotic lactobacilli and clinical isolates of mutans streptococci: an in vitro study. Acta Odontol Scand. 2011;69(5):263–268.
   PubMed Web of Science ®Google Scholar
• Soderling EM, Marttinen AM, Haukioja AL. Probiotic lactobacilli interfere with Streptococcus mutans biofilm formation in vitro. Curr Microbiol. 2011;62(2):618–622.
   PubMed Web of Science ®Google Scholar
• Waters CM, Bassler BL. Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol. 2005;21:319–346.
   PubMed Web of Science ®Google Scholar
• Le KY, Otto M. Quorum-sensing regulation in staphylococci-an overview. Front Microbiol. 2015;6:1174.
   PubMed Web of Science ®Google Scholar
• Li J, Wang W, Xu SX, et al. Lactobacillus reuteri-produced cyclic dipeptides quench agr-mediated expression of toxic shock syndrome toxin-1 in staphylococci. Proc Natl Acad Sci USA 2011;108(8):3360–3365.
   PubMed Web of Science ®Google Scholar
• Piewngam P, Zheng Y, Nguyen TH, et al. Pathogen elimination by probiotic Bacillus via signaling interference. Nature 2018;562(7728):532–537.
   PubMed Web of Science ®Google Scholar
• Haukioja A, Soderling E, Tenovuo J. Acid production from sugars and sugar alcohols by probiotic lactobacilli and bifidobacteria in vitro. Caries Res. 2008;42(6):449–453.
   PubMed Web of Science ®Google Scholar
• Alakomi HL, Skytta E, Saarela M, et al. Lactic acid permeabilizes gram-negative bacteria by disrupting the outer membrane. Appl Environ Microbiol. 2000;66(5):2001–2005.
   PubMed Web of Science ®Google Scholar
• Marttinen A, Haukioja A, Karjalainen S, et al. Short-term consumption of probiotic lactobacilli has no effect on acid production of supragingival plaque. Clin Oral Investig. 2012;16(3):797–803.
   PubMed Web of Science ®Google Scholar
• Ryan CS, Kleinberg I. Bacteria in human mouths involved in the production and utilization of hydrogen peroxide. Arch Oral Biol. 1995;40(8):753–763.
   PubMed Web of Science ®Google Scholar
• Gupta R, Srivastava S. Antifungal effect of antimicrobial peptides (AMPs LR14) derived from Lactobacillus plantarum strain LR/14 and their applications in prevention of grain spoilage. Food Microbiol. 2014;42:1–7.
   PubMed Web of Science ®Google Scholar
• Gillor O, Etzion A, Riley MA. The dual role of bacteriocins as anti- and probiotics. Appl Microbiol Biotechnol. 2008;81(4):591–606.
   PubMed Web of Science ®Google Scholar
• Schaefer L, Auchtung TA, Hermans KE, et al. The antimicrobial compound reuterin (3-hydroxypropionaldehyde) induces oxidative stress via interaction with thiol groups. Microbiology 2010;156(Pt 6):1589–1599.
   PubMed Web of Science ®Google Scholar
• Cleusix V, Lacroix C, Vollenweider S, et al. Inhibitory activity spectrum of reuterin produced by Lactobacillus reuteri against intestinal bacteria. BMC Microbiol. 2007;7:101.
   PubMed Web of Science ®Google Scholar
• Khalaf H, Nakka SS, Sanden C, et al. Antibacterial effects of Lactobacillus and bacteriocin PLNC8 αβ on the periodontal pathogen Porphyromonas gingivalis. BMC Microbiol. 2016;16(1):188.
   PubMed Web of Science ®Google Scholar
• Jaffar N, Ishikawa Y, Mizuno K, et al. Mature biofilm degradation by potential probiotics: Aggregatibacter actinomycetemcomitans versus Lactobacillus spp. PLOS One 2016;11(7):e0159466.
   PubMed Web of Science ®Google Scholar
• Teanpaisan R, Piwat S, Dahlen G. Inhibitory effect of oral Lactobacillus against oral pathogens. Lett Appl Microbiol. 2011;53(4):452–459.
   PubMed Web of Science ®Google Scholar
• Zheng J, Ganzle MG, Lin XB, et al. Diversity and dynamics of bacteriocins from human microbiome. Environ Microbiol. 2015;17(6):2133–2143.
   PubMed Web of Science ®Google Scholar
• Takeda K, Suzuki T, Shimada SI, et al. Interleukin-12 is involved in the enhancement of human natural killer cell activity by Lactobacillus casei Shirota. Clin Exp Immunol. 2006;146(1):109–115.
   PubMed Web of Science ®Google Scholar
• Pelto L, Isolauri E, Lilius EM, et al. Probiotic bacteria down-regulate the milk-induced inflammatory response in milk-hypersensitive subjects but have an immunostimulatory effect in healthy subjects. Clin Exp Allergy 1998;28(12):1474–1479.
   PubMed Web of Science ®Google Scholar
• Perdigon G, Maldonado Galdeano C, Valdez JC, et al. Interaction of lactic acid bacteria with the gut immune system. Eur J Clin Nutr. 2002;56(S4):S21–S6.
   PubMed Web of Science ®Google Scholar
• Esteban-Fernandez A, Ferrer MD, Zorraquin-Pena I, et al. In vitro beneficial effects of Streptococcus dentisani as potential oral probiotic for periodontal diseases. J Periodontol. 2019;90(11):1346–1355.
   PubMed Web of Science ®Google Scholar
• Staab B, Eick S, Knofler G, et al. The influence of a probiotic milk drink on the development of gingivitis: A pilot study. J Clin Periodontol. 2009;36(10):850–856.
   PubMed Web of Science ®Google Scholar
• Ince G, Gürsoy H, Ipçi ŞD, et al. Clinical and biochemical evaluation of lozenges containing Lactobacillus reuteri as an adjunct to non-surgical periodontal therapy in chronic periodontitis. J Periodontol. 2015;86(6):746–754.
   PubMed Web of Science ®Google Scholar
• Jaffar N, Okinaga T, Nishihara T, et al. Enhanced phagocytosis of Aggregatibacter actinomycetemcomitans cells by macrophages activated by a probiotic Lactobacillus strain. J Dairy Sci. 2018;101(7):5789–5798.
   PubMed Web of Science ®Google Scholar
• Kobayashi R, Kobayashi T, Sakai F, et al. Oral administration of Lactobacillus gasseri SBT2055 is effective in preventing Porphyromonas gingivalis-accelerated periodontal disease. Sci Rep. 2017;7(1):545.
   PubMed Web of Science ®Google Scholar
• Martin-Cabezas R, Davideau JL, Tenenbaum H, et al. Clinical efficacy of probiotics as an adjunctive therapy to non-surgical periodontal treatment of chronic periodontitis: a systematic review and meta-analysis. J Clin Periodontol. 2016;43(6):520–530.
   PubMed Web of Science ®Google Scholar
• Yanine N, Araya I, Brignardello-Petersen R, et al. Effects of probiotics in periodontal diseases: a systematic review. Clin Oral Investig. 2013;17(7):1627–1634.
   PubMed Web of Science ®Google Scholar
• Vives-Soler A, Chimenos-Kustner E. Effect of probiotics as a complement to non-surgical periodontal therapy in chronic periodontitis: a systematic review. Med Oral Patol Oral Cir Bucal. 2020;25(2):e161–e167.
   PubMed Web of Science ®Google Scholar
• Ikram S, Hassan N, Raffat MA, et al. Systematic review and meta-analysis of double-blind, placebo-controlled, randomized clinical trials using probiotics in chronic periodontitis. J Investig Clin Dent. 2018;9(3):e12338.
   PubMed Web of Science ®Google Scholar
• Moher D, Liberati A, Tetzlaff J, et al. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLOS Med. 2009;6(7):e1000097.
   PubMed Web of Science ®Google Scholar
• Cionca N, Giannopoulou C, Ugolotti G, et al. Amoxicillin and metronidazole as an adjunct to full-mouth scaling and root planing of chronic periodontitis. J Periodontol. 2009;80(3):364–371.
   PubMed Web of Science ®Google Scholar
• Teughels W, Durukan A, Ozcelik O, et al. Clinical and microbiological effects of Lactobacillus reuteri probiotics in the treatment of chronic periodontitis: a randomized placebo-controlled study. J Clin Periodontol. 2013;40(11):1025–1035.
   PubMed Web of Science ®Google Scholar
• Lang NP, Tonetti MS. Periodontal risk assessment (PRA) for patients in supportive periodontal therapy (SPT). Oral Health Prev Dent. 2003;1(1):7–16.
   PubMedGoogle Scholar
• Higgins J, Thomas J, Chandler J, et al. Cochrane Handbook for Systematic Reviews of Interventions version 6.0 The Cochrane Collaboration [cited 13 Feb 2020]. Available from: www.handbook.cochrane.org
   Google Scholar
• Morales A, Carvajal P, Silva N, et al. Clinical effects of Lactobacillus rhamnosus in non-surgical treatment of chronic periodontitis: a randomized placebo-controlled trial with 1-year follow-up. J Periodontol. 2016;87(8):944–952.
   PubMed Web of Science ®Google Scholar
• Morales A, Gandolfo A, Bravo J, et al. Microbiological and clinical effects of probiotics and antibiotics on nonsurgical treatment of chronic periodontitis: a randomized placebo- controlled trial with 9-month follow-up. J Appl Oral Sci. 2018;26:e20170075.
   PubMed Web of Science ®Google Scholar
• Invernici MM, Salvador SL, Silva PHF, et al. Effects of Bifidobacterium probiotic on the treatment of chronic periodontitis: a randomized clinical trial. J Clin Periodontol. 2018;45(10):1198–1210.
   PubMed Web of Science ®Google Scholar
• Soares LG, Carvalho EB, Tinoco EMB. Clinical effect of Lactobacillus on the treatment of severe periodontitis and halitosis: a double-blinded, placebo-controlled, randomized clinical trial. Am J Dent. 2019;32(1):9–13.
   PubMed Web of Science ®Google Scholar
• Penala S, Kalakonda B, Pathakota KR, et al. Efficacy of local use of probiotics as an adjunct to scaling and root planing in chronic periodontitis and halitosis: a randomized controlled trial. J Res Pharm Pract. 2016;5(2):86–93.
   PubMed Web of Science ®Google Scholar
• Quirynen M, De Soete M, Boschmans G, et al. Benefit of "one-stage full-mouth disinfection" is explained by disinfection and root planing within 24 hours: a randomized controlled trial. J Clin Periodontol. 2006;33(9):639–647.
   PubMed Web of Science ®Google Scholar
• Laleman I, Yilmaz E, Ozcelik O, et al. The effect of a streptococci containing probiotic in periodontal therapy: A randomized controlled trial. J Clin Periodontol. 2015;42(11):1032–1041.
   PubMed Web of Science ®Google Scholar
• Tekce M, Ince G, Gursoy H, et al. Clinical and microbiological effects of probiotic lozenges in the treatment of chronic periodontitis: a 1-year follow-up study. J Clin Periodontol. 2015;42(4):363–372.
   PubMed Web of Science ®Google Scholar
• Pelekos G, Ho SN, Acharya A, et al. A double-blind, paralleled-arm, placebo-controlled and randomized clinical trial of the effectiveness of probiotics as an adjunct in periodontal care. J Clin Periodontol. 2019;46(12):1217–1227.
   PubMed Web of Science ®Google Scholar
• Matuliene G, Pjetursson BE, Salvi GE, et al. Influence of residual pockets on progression of periodontitis and tooth loss: results after 11 years of maintenance. J Clin Periodontol. 2008;35(8):685–695.
   PubMed Web of Science ®Google Scholar
• Eickholz P, Kaltschmitt J, Berbig J, et al. Tooth loss after active periodontal therapy. 1: Patient-related factors for risk, prognosis, and quality of outcome. J Clin Periodontol. 2008;35(2):165–174.
   PubMed Web of Science ®Google Scholar
• Ho SN, Acharya A, Sidharthan S, et al. A Systematic review and meta-analysis of clinical, immunological, and microbiological shift in periodontitis after nonsurgical periodontal therapy with adjunctive use of probiotics. J Evid Based Dent Pract. 2020;20(1):101397.
   PubMed Web of Science ®Google Scholar
• Donos N, Calciolari E, Brusselaers N, et al. The adjunctive use of host modulators in non-surgical periodontal therapy. A systematic review of randomized, placebo-controlled clinical studies. J Clin Periodontol. 2020;47(S22):199–238.
   PubMed Web of Science ®Google Scholar
• Loos BG, Needleman I. Endpoints of active periodontal therapy. J Clin Periodontol. 2020;47(S22):61–71.
   PubMed Web of Science ®Google Scholar
• Gruner D, Paris S, Schwendicke F. Probiotics for managing caries and periodontitis: systematic review and meta-analysis. J Dent. 2016;48:16–25.
   PubMed Web of Science ®Google Scholar
• Seminario-Amez M, Lopez-Lopez J, Estrugo-Devesa A, et al. Probiotics and oral health: a systematic review. Med Oral Patol Oral Cir Bucal. 2017;22(3):e282–e288.
   PubMed Web of Science ®Google Scholar
• Szkaradkiewicz AK, Stopa J, Karpiński TM. Effect of oral administration involving a probiotic strain of Lactobacillus reuteri on pro-inflammatory cytokine response in patients with chronic periodontitis. Arch Immunol Ther Exp. 2014;62(6):495–500.
   PubMed Web of Science ®Google Scholar
• Twetman S, Derawi B, Keller M, et al. Short-term effect of chewing gums containing probiotic Lactobacillus reuteri on the levels of inflammatory mediators in gingival crevicular fluid. Acta Odontol Scand. 2009;67(1):19–24.
   PubMed Web of Science ®Google Scholar
• Vivekananda MR, Vandana KL, Bhat KG. Effect of the probiotic Lactobacilli reuteri (Prodentis) in the management of periodontal disease: a preliminary randomized clinical trial. J Oral Microbiol. 2010;2. DOI:https://doi.org/10.3402/jom.v2i0.5344
   PubMedGoogle Scholar