Clinical effects of probiotic or azithromycin as an adjunct to scaling and root planning in the treatment of stage III periodontitis: a pilot randomized controlled clinical trial

Alicia Morales, Rafael Contador, Joel Bravo, Paola Carvajal, Nora Silva, Franz-Josef Strauss, Jorge Gamonal, Alicia Morales, Rafael Contador, Joel Bravo, Paola Carvajal, Nora Silva, Franz-Josef Strauss, Jorge Gamonal

Abstract

Background: The aim of this triple-blind placebo-controlled parallel-arm randomized clinical trial was to evaluate the clinical effects of Lactobacillus rhamnosus SP1 or azithromycin as an adjunct to scaling and root planing (SRP) in patients with stage III periodontitis.

Methods: Forty-seven systemically healthy participants with stage III periodontitis were recruited. Following SRP, the participants were randomly assigned to one of three treatment modalities; (1) placebo (n = 15), (2) probiotics (n = 16) and (3) antibiotics-azithromycin (n = 16). The participants were monitored at baseline, 3, 6, 9 and 12 months after therapy. Probing pocket depth (PPD), bleeding on probing (BOP), clinical attachment loss (CAL) and plaque accumulation (PI) were evaluated.

Results: All 47 participants completed the study. At 12 months, all groups showed significant improvements of PPD and PI (p < 0.012) irrespective of the treatment modality and without significant differences between the groups. Probiotics and azithromycin showed no added benefit in terms of CAL. While the placebo (p = 0.002) and the antibiotic-azithromycin (p = 0.002) group showed a significant reduction of BOP, only the placebo group revealed a significant reduction of CAL at 12 months follow-up (p = 0.003). The number of sites and teeth with PPD ≥ 5, ≥ 6 and ≥ 7 mm were significantly reduced in all groups at 12 months follow-up (p < 0.025) irrespective of the treatment regime and without significant differences between the groups.

Conclusion: The use of probiotics or azithromycin as an adjunct to SRP failed to provide additional benefits in the treatment of stage III periodontitis. The benefits of these two treatment regimes as an adjunct to SRP remain unclear.

Trial registration: NCT02839408, 10/28/2017, Clinicaltrial.gov.

Keywords: Azithromycin; Lactobacillus rhamnosus; Periodontitis; Scaling and root planing.

Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Fig. 1
Fig. 1
Flow chart of the study design

References

    1. Tonetti MS, Greenwell H, Kornman KS. Staging and grading of periodontitis: framework and proposal of a new classification and case definition. J Clin Periodontol. 2018;45(Suppl 20):S149–S161.
    1. Badersten A, Nilveus R, Egelberg J. Effect of nonsurgical periodontal therapy. II. Severely advanced periodontitis. J Clin Periodontol. 1984;11(1):63–76.
    1. Suvan J, Leira Y, Moreno Sancho FM, Graziani F, Derks J, Tomasi C. Subgingival instrumentation for treatment of periodontitis. A systematic review. J Clin Periodontol. 2020;47(Suppl 22):155–175.
    1. Drisko CH. Nonsurgical periodontal therapy. Periodontology. 2000;2001(25):77–88.
    1. Zhang Z, Zheng Y, Bian X. Clinical effect of azithromycin as an adjunct to non-surgical treatment of chronic periodontitis: a meta-analysis of randomized controlled clinical trials. J Periodontal Res. 2016;51(3):275–283.
    1. Herrera D, Sanz M, Jepsen S, Needleman I, Roldan S. A systematic review on the effect of systemic antimicrobials as an adjunct to scaling and root planing in periodontitis patients. J Clin Periodontol. 2002;29(Suppl 3):136–159.
    1. Teughels W, Feres M, Oud V, Martin C, Matesanz P, Herrera D. Adjunctive effect of systemic antimicrobials in periodontitis therapy: a systematic review and meta-analysis. J Clin Periodontol. 2020;47(Suppl 22):257–281.
    1. Parnham MJ, Erakovic Haber V, Giamarellos-Bourboulis EJ, Perletti G, Verleden GM, Vos R. Azithromycin: mechanisms of action and their relevance for clinical applications. Pharmacol Ther. 2014;143(2):225–245.
    1. Matsubara VH, Bandara HM, Ishikawa KH, Mayer MP, Samaranayake LP. The role of probiotic bacteria in managing periodontal disease: a systematic review. Expert Rev Anti Infect Ther. 2016;14(7):643–655.
    1. WHO: World Health Organization. probiotics in food: health and nutritional properties and guidelines for evaluation, vol. vii; 2006.
    1. Morales A BJ, Bedoya J, Gamonal J. Probiotics and Periodontal diseases. In: Insights into various aspects of oral health; 2017.
    1. Bravo J, Morales A, Lefimil C, Galaz C, Gamonal J. Clinical effect of Lactobacillus reuteri in the treatment of gingivitis: a randomized controlled clinical trial. Rev Clin Periodoncia Implantol Rehabil. 2018;11(1):32–35.
    1. Koll-Klais P, Mandar R, Leibur E, Marcotte H, Hammarstrom L, Mikelsaar M. Oral lactobacilli in chronic periodontitis and periodontal health: species composition and antimicrobial activity. Oral Microbiol Immunol. 2005;20(6):354–361.
    1. Teanpaisan R, Piwat S, Dahlen G. Inhibitory effect of oral Lactobacillus against oral pathogens. Lett Appl Microbiol. 2011;53(4):452–459.
    1. Koll P, Mandar R, Marcotte H, Leibur E, Mikelsaar M, Hammarstrom L. Characterization of oral lactobacilli as potential probiotics for oral health. Oral Microbiol Immunol. 2008;23(2):139–147.
    1. Bodera P, Chcialowski A. Immunomodulatory effect of probiotic bacteria. Recent Pat Inflamm Allergy Drug Discov. 2009;3(1):58–64.
    1. Isolauri E, Sutas Y, Kankaanpaa P, Arvilommi H, Salminen S. Probiotics: effects on immunity. Am J Clin Nutr. 2001;73(2 Suppl):444S–450S.
    1. Kekkonen RA, Lummela N, Karjalainen H, Latvala S, Tynkkynen S, Jarvenpaa S, Kautiainen H, Julkunen I, Vapaatalo H, Korpela R. Probiotic intervention has strain-specific anti-inflammatory effects in healthy adults. World J Gastroenterol. 2008;14(13):2029–2036.
    1. Marttinen A, Haukioja A, Karjalainen S, Nylund L, Satokari R, Ohman C, Holgerson P, Twetman S, Soderling E. Short-term consumption of probiotic lactobacilli has no effect on acid production of supragingival plaque. Clin Oral Investig. 2012;16(3):797–803.
    1. Nguyen T, Brody H, Lin GH, Range H, Kuraji R, Ye C, Kamarajan P, Radaic A, Gao L, Kapila Y. Probiotics, including nisin-based probiotics, improve clinical and microbial outcomes relevant to oral and systemic diseases. Periodontology. 2020;82(1):173–185.
    1. Donos N, Calciolari E, Brusselaers N, Goldoni M, Bostanci N, Belibasakis GN. 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(Suppl 22):199–238.
    1. Morales A, Gandolfo A, Bravo J, Carvajal P, Silva N, Godoy C, Garcia-Sesnich J, Hoare A, Diaz P, Gamonal J. 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.
    1. Cohen RE, Research S Therapy Committee AAoP: Position paper: periodontal maintenance. J Periodontol. 2003;74(9):1395–1401.
    1. Lang NP, Tonetti MS. Periodontal risk assessment (PRA) for patients in supportive periodontal therapy (SPT) Oral Health Prev Dent. 2003;1(1):7–16.
    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. J Periodontol. 2009;80(3):364–371.
    1. Haffajee AD, Socransky SS. Attachment level changes in destructive periodontal diseases. J Clin Periodontol. 1986;13(5):461–475.
    1. Teughels W, Durukan A, Ozcelik O, Pauwels M, Quirynen M, Haytac MC. 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.
    1. Laleman I, Yilmaz E, Ozcelik O, Haytac C, Pauwels M, Herrero ER, Slomka V, Quirynen M, Alkaya B, Teughels W. The effect of a streptococci containing probiotic in periodontal therapy: a randomized controlled trial. J Clin Periodontol. 2015;42(11):1032–1041.
    1. Morales A, Carvajal P, Silva N, Hernandez M, Godoy C, Rodriguez G, Cabello R, Garcia-Sesnich J, Hoare A, Diaz PI, 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.
    1. Pelekos G, Ho SN, Acharya A, Leung WK, McGrath C. 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.
    1. Tekce M, Ince G, Gursoy H, Dirikan Ipci S, Cakar G, Kadir T, Yilmaz S. 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.
    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. J Oral Microbiol. 2010;2:5344.
    1. Shimauchi H, Mayanagi G, Nakaya S, Minamibuchi M, Ito Y, Yamaki K, Hirata H. Improvement of periodontal condition by probiotics with Lactobacillus salivarius WB21: a randomized, double-blind, placebo-controlled study. J Clin Periodontol. 2008;35(10):897–905.
    1. İnce G, Gürsoy H, İpçi SD, Cakar G, Emekli-Alturfan E, Yılmaz S. Clinical and biochemical evaluation of lozenges containing as an adjunct to non-surgical periodontal therapy in chronic periodontitis. J Periodontol. 2015;86(6):746–754.
    1. Invernici MM, Salvador SL, Silva PHF, Soares MSM, Casarin R, Palioto DB, Souza SLS, Taba M, Jr, Novaes AB, Jr, Furlaneto FAC, et al. Effects of Bifidobacterium probiotic on the treatment of chronic periodontitis: a randomized clinical trial. J Clin Periodontol. 2018;45(10):1198–1210.
    1. Sanders ME. Probiotics: definition, sources, selection, and uses. Clin Infect Dis. 2008;46(Suppl 2):S58–61.
    1. Kaila M, Isolauri E, Soppi E, Virtanen E, Laine S, Arvilommi H. Enhancement of the circulating antibody secreting cell response in human diarrhea by a human Lactobacillus strain. Pediatr Res. 1992;32(2):141–144.
    1. Majamaa H, Isolauri E. Probiotics: a novel approach in the management of food allergy. J Allergy Clin Immunol. 1997;99(2):179–185.
    1. Majamaa H, Isolauri E, Saxelin M, Vesikari T. Lactic acid bacteria in the treatment of acute rotavirus gastroenteritis. J Pediatr Gastroenterol Nutr. 1995;20(3):333–338.
    1. Han B, Emingil G, Ozdemir G, Tervahartiala T, Vural C, Atilla G, Baylas H, Sorsa T. Azithromycin as an adjunctive treatment of generalized severe chronic periodontitis: clinical, microbiologic, and biochemical parameters. J Periodontol. 2012;83(12):1480–1491.
    1. Sampaio E, Rocha M, Figueiredo LC, Faveri M, Duarte PM, Gomes Lira EA, Feres M. Clinical and microbiological effects of azithromycin in the treatment of generalized chronic periodontitis: a randomized placebo-controlled clinical trial. J Clin Periodontol. 2011;38(9):838–846.
    1. Martande SS, Pradeep AR, Singh SP, Kumari M, Naik SB, Suke DK, Singh P. Clinical and microbiological effects of systemic azithromycin in adjunct to nonsurgical periodontal therapy in treatment of Aggregatibacter actinomycetemcomitans associated periodontitis: a randomized placebo-controlled clinical trial. J Investig Clin Dent. 2016;7(1):72–80.

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