CC BY 4.0 · Eur J Dent
DOI: 10.1055/s-0043-1777822
Original Article

Limosilactobacillus reuteri as an Adjuvant in the Treatment of Peri-implant Mucositis in Total Rehabilitation: An Exploratory Study

Gonçalo J.G. Parreira
1   Universidade de Lisboa, Faculdade de Medicina Dentária, Unidade de Investigação em Ciências Orais e Biomédicas (UICOB), Lisboa, Portugal
2   Oral Hygiene Department, Maló Clinic, Lisbon, Portugal
3   Universidade de Lisboa, Faculdade de Medicina Dentária, Rede de Higienistas Orais para o Desenvolvimento da Ciência (RHODes), Lisboa, Portugal
,
2   Oral Hygiene Department, Maló Clinic, Lisbon, Portugal
4   Research and Development Department, Maló Clinic, Lisbon, Portugal
5   Clínica Universitária de Estomatologia, Faculdade de Medicina, Universidade de Lisboa, Portugal
,
André G.C.R. Moreira
1   Universidade de Lisboa, Faculdade de Medicina Dentária, Unidade de Investigação em Ciências Orais e Biomédicas (UICOB), Lisboa, Portugal
,
1   Universidade de Lisboa, Faculdade de Medicina Dentária, Unidade de Investigação em Ciências Orais e Biomédicas (UICOB), Lisboa, Portugal
3   Universidade de Lisboa, Faculdade de Medicina Dentária, Rede de Higienistas Orais para o Desenvolvimento da Ciência (RHODes), Lisboa, Portugal
6   Center for Innovative Care and Health Technology (ciTechcare), Polytechnic of Leiria, Leiria, Portugal
› Author Affiliations

Abstract

Objectives Mechanical debridement is the traditional method for the treatment of peri-implant mucositis (P-im) and its success depends on the patient's correct oral hygiene. It is believed that probiotics may help by their ability to modulate the oral biofilm, resulting in anti-inflammatory and antibacterial plaque action. The aim of this study was to evaluate the adjuvant effect of the probiotic Limosilactobacillus reuteri (LR) in the mechanical treatment of P-im.

Materials and Methods This exploratory study included 29 subjects with implant-supported total rehabilitation and P-im, divided into test (TG) and control (CG) groups, equally subjected to professional mechanical debridement, with the administration of a daily GUM PerioBalance lozenge for 30 days added to the TG. The modified Plaque Index (mPlI) modified Sulcus Bleeding Index (mBI) and pocket depth (PD) were evaluated before the intervention (baseline) and 6 and 10 weeks later.

Statistical Analysis Parametric and nonparametric tests with 5% significance level were used in the statistical analysis, using IBM SPSS Statistics 27.0 software.

Results Both treatments resulted in reduced mPlI, mBI, and PD at 6 weeks; while from 6 to 10 weeks there was an increase in mPlI and mBI and maintenance of PD. Compared with baseline, differences were close to statistical significance in the reduction in PD at 10 weeks in the CG (p = 0.018), after Bonferroni correction, and statistically significant in the mPlI at 6 weeks in the CG (p = 0.004) and in the TG (p = 0.002) as well as at 10 weeks in the TG (p = 0.016). Comparing the groups in the postintervention assessments, no statistically significant differences were found.

Conclusion LR adjuvant mechanical treatment of P-im does not show a clear benefit compared with mechanical treatment alone, with both interventions achieving similar clinical results. Further prospective and long-term studies are needed.



Publication History

Article published online:
31 March 2024

© 2024. The Author(s). This is an open access article published by Thieme under the terms of the Creative Commons Attribution License, permitting unrestricted use, distribution, and reproduction so long as the original work is properly cited. (https://creativecommons.org/licenses/by/4.0/)

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  • References

  • 1 Alam MK, Rahman SA, Basri R, Sing Yi TT, Si-Jie JW, Saha S. Dental implants - perceiving patients' satisfaction in relation to clinical and electromyography study on implant patients. PLoS One 2015; 10 (10) e0140438
  • 2 Jung RE, Zembic A, Pjetursson BE, Zwahlen M, Thoma DS. Systematic review of the survival rate and the incidence of biological, technical, and aesthetic complications of single crowns on implants reported in longitudinal studies with a mean follow-up of 5 years. Clin Oral Implants Res 2012; 23 (Suppl. 06) 2-21
  • 3 Lang NP, Wilson TG, Corbet EF. Biological complications with dental implants: their prevention, diagnosis and treatment. Clin Oral Implants Res 2000; 11 (Suppl. 01) 146-155
  • 4 Belibasakis GN. Microbiological and immuno-pathological aspects of peri-implant diseases. Arch Oral Biol 2014; 59 (01) 66-72
  • 5 de Araújo Nobre M, Maló P. Prevalence of periodontitis, dental caries, and peri-implant pathology and their relation with systemic status and smoking habits: Results of an open-cohort study with 22009 patients in a private rehabilitation center. J Dent 2017; 67: 36-42
  • 6 Salvi GE, Cosgarea R, Sculean A. Prevalence of periimplant diseases. Implant Dent 2019; 28 (02) 100-102
  • 7 Derks J, Tomasi C. Peri-implant health and disease. A systematic review of current epidemiology. J Clin Periodontol 2015; 42 (Suppl. 16) S158-S171
  • 8 Claffey N, Clarke E, Polyzois I, Renvert S. Surgical treatment of peri-implantitis. J Clin Periodontol 2008; 35 (08) 316-332
  • 9 Renvert S, Roos-Jansåker AM, Claffey N. Non-surgical treatment of peri-implant mucositis and peri-implantitis: a literature review. J Clin Periodontol 2008; 35 (08) 305-315
  • 10 Salvi GE, Aglietta M, Eick S, Sculean A, Lang NP, Ramseier CA. Reversibility of experimental peri-implant mucositis compared with experimental gingivitis in humans. Clin Oral Implants Res 2012; 23 (02) 182-190
  • 11 Schwarz F, Jepsen S, Herten M, Sager M, Rothamel D, Becker J. Influence of different treatment approaches on non-submerged and submerged healing of ligature induced peri-implantitis lesions: an experimental study in dogs. J Clin Periodontol 2006; 33 (08) 584-595
  • 12 Wunderlich RC, Singelton M, O'Brien WJ, Caffesse RG. Subgingival penetration of an applied solution. Int J Periodontics Restorative Dent 1984; 4 (05) 64-71
  • 13 Abi Nader S, Eimar H, Momani M, Shang K, Daniel NG, Tamimi F. Plaque accumulation beneath maxillary all-on-4™ implant-supported prostheses. Clin Implant Dent Relat Res 2015; 17 (05) 932-937
  • 14 Nutrition Division. Probiotics in food: Health and nutritional properties and guidelines for evaluation. Food and Agriculture Organization of the United Nations. Published 2006 . Accessed November 24, 2023 at: https://www.fao.org/documents/card/en/c/7c102d95-2fd5-5b22-8faf-f0b2e68dfbb6/
  • 15 Comelli EM, Guggenheim B, Stingele F, Neeser JR. Selection of dairy bacterial strains as probiotics for oral health. Eur J Oral Sci 2002; 110 (03) 218-224
  • 16 Çaglar E, Kargul B, Tanboga I. Bacteriotherapy and probiotics' role on oral health. Oral Dis 2005; 11 (03) 131-137
  • 17 Selvaraj K, Bharath N, Natarajan R, Dinesh S, Murugesan S, Selvaraj S. Comparative evaluation of antimicrobial efficacy of toothpastes containing probiotic and neem as primary ingredient on salivary Streptococcus mutans in Melmaruvathur population: an in vivo study. J Pharm Bioallied Sci 2020; 12 (Suppl. 01) S595-S600
  • 18 Cannon ML, Vorachek A, Le C, White K. Retrospective review of oral probiotic therapy. J Clin Pediatr Dent 2019; 43 (06) 367-371
  • 19 Çaglar E, Cildir SK, Ergeneli S, Sandalli N, Twetman S. Salivary mutans streptococci and lactobacilli levels after ingestion of the probiotic bacterium Lactobacillus reuteri ATCC 55730 by straws or tablets. Acta Odontol Scand 2006; 64 (05) 314-318
  • 20 Mendonça FHBP, Santos SS, Faria IdaS, Gonçalves e Silva CR, Jorge AOC, Leão MVP. Effects of probiotic bacteria on Candida presence and IgA anti-Candida in the oral cavity of elderly. Braz Dent J 2012; 23 (05) 534-538
  • 21 Li D, Li Q, Liu C. et al. Efficacy and safety of probiotics in the treatment of Candida-associated stomatitis. Mycoses 2014; 57 (03) 141-146
  • 22 Lee DS, Lee SA, Kim M, Nam SH, Kang MS. Reduction of Halitosis by a tablet containing Weissella cibaria CMU: a randomized, double-blind, placebo-controlled study. J Med Food 2020; 23 (06) 649-657
  • 23 Yoo JI, Shin IS, Jeon JG, Yang YM, Kim JG, Lee DW. The effect of probiotics on halitosis: a systematic review and meta-analysis. Probiotics Antimicrob Proteins 2019; 11 (01) 150-157
  • 24 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
  • 25 Ng E, Tay JRH, Saffari SE, Lim LP, Chung KM, Ong MMA. Adjunctive probiotics after periodontal debridement versus placebo: a systematic review and meta-analysis. Acta Odontol Scand 2022; 80 (02) 81-90
  • 26 Alshareef A, Attia A, Almalki M. et al. Effectiveness of probiotic lozenges in periodontal management of chronic periodontitis patients: clinical and immunological study. Eur J Dent 2020; 14 (02) 281-287
  • 27 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 (04) 363-372
  • 28 Flichy-Fernández AJ, Ata-Ali J, Alegre-Domingo T. et al. The effect of orally administered probiotic Lactobacillus reuteri-containing tablets in peri-implant mucositis: a double-blind randomized controlled trial. J Periodontal Res 2015; 50 (06) 775-785
  • 29 Alqahtani F, Alqahtani M, Shafqat SS, Akram Z, Al-Kheraif AA, Javed F. Efficacy of mechanical debridement with adjunctive probiotic therapy in the treatment of peri-implant mucositis in cigarette-smokers and never-smokers. Clin Implant Dent Relat Res 2019; 21 (04) 734-740
  • 30 Arbildo-Vega HI, Panda S, Bal A. et al. Clinical effectiveness of Lactobacillus reuteri in the treatment of peri-implant diseases: a systematic review and meta-analysis. J Biol Regul Homeost Agents 2021; 35 (2, Suppl. 1): 79-88
  • 31 Twetman S, Derawi B, Keller M, Ekstrand K, Yucel-Lindberg T, Stecksén-Blicks C. 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 (01) 19-24
  • 32 Krasse P, Carlsson B, Dahl C, Paulsson A, Nilsson A, Sinkiewicz G. Decreased gum bleeding and reduced gingivitis by the probiotic Lactobacillus reuteri. Swed Dent J 2006; 30 (02) 55-60
  • 33 Li J, Zhao G, Zhang HM, Zhu FF. Probiotic adjuvant treatment in combination with scaling and root planning in chronic periodontitis: a systematic review and meta-analysis. Benef Microbes 2023; 14 (02) 95-107
  • 34 Axelsson LT, Chung TC, Dobrogosz WJ, Lindgren SE. Production of a broad spectrum antimicrobial substance by lactobacillus reuteri. Microb Ecol Health Dis 1989; 2: 131-136
  • 35 Widyarman AS, Theodorea CF. Novel indigenous probiotic Lactobacillus reuteri strain produces anti-biofilm Reuterin against pathogenic periodontal bacteria. Eur J Dent 2022; 16 (01) 96-101
  • 36 Mu Q, Tavella VJ, Luo XM. Role of Lactobacillus reuteri in human health and diseases. Front Microbiol 2018; 9: 757
  • 37 Mombelli A, van Oosten MAC, Schürch Jr E, Land NP. The microbiota associated with successful or failing osseointegrated titanium implants. Oral Microbiol Immunol 1987; 2 (04) 145-151
  • 38 Maló P, Rangert B, Dvärsäter L. Immediate function of Brånemark implants in the esthetic zone: a retrospective clinical study with 6 months to 4 years of follow-up. Clin Implant Dent Relat Res 2000; 2 (03) 138-146
  • 39 Albrektsson T, Zarb G, Worthington P, Eriksson AR. The long-term efficacy of currently used dental implants: a review and proposed criteria of success. Int J Oral Maxillofac Implants 1986; 1 (01) 11-25
  • 40 Lang NP, Berglundh T. Periimplant diseases: Where are we now? - Consensus of the Seventh European Workshop on Periodontology. J Clin Periodontol 2011; 38 (suppl 11): S178-S181
  • 41 Galofré M, Palao D, Vicario M, Nart J, Violant D. Clinical and microbiological evaluation of the effect of Lactobacillus reuteri in the treatment of mucositis and peri-implantitis: a triple-blind randomized clinical trial. J Periodontal Res 2018; 53 (03) 378-390
  • 42 Mongardini C, Pilloni A, Farina R, Di Tanna G, Zeza B. Adjunctive efficacy of probiotics in the treatment of experimental peri-implant mucositis with mechanical and photodynamic therapy: a randomized, cross-over clinical trial. J Clin Periodontol 2017; 44 (04) 410-417
  • 43 Hallström H, Lindgren S, Widén C, Renvert S, Twetman S. Probiotic supplements and debridement of peri-implant mucositis: a randomized controlled trial. Acta Odontol Scand 2016; 74 (01) 60-66
  • 44 Peña M, Barallat L, Vilarrasa J, Vicario M, Violant D, Nart J. Evaluation of the effect of probiotics in the treatment of peri-implant mucositis: a triple-blind randomized clinical trial. Clin Oral Investig 2019; 23 (04) 1673-1683
  • 45 Candotto V, Gabrione F, Oberti L, Lento D, Severino M. The role of implant-abutment connection in preventing bacterial leakage: a review. J Biol Regul Homeost Agents 2019; 33 (3, Suppl. 1): 129-134
  • 46 Lauritano D, Moreo G, Lucchese A, Viganoni C, Limongelli L, Carinci F. The impact of implant-abutment connection on clinical outcomes and microbial colonization: a narrative review. Materials (Basel) 2020; 13 (05) 1131
  • 47 Pontoriero R, Tonelli MP, Carnevale G, Mombelli A, Nyman SR, Lang NP. Experimentally induced peri-implant mucositis. A clinical study in humans. Clin Oral Implants Res 1994; 5 (04) 254-259
  • 48 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
  • 49 Zhao R, Hu H, Wang Y, Lai W, Jian F. Efficacy of probiotics as adjunctive therapy to nonsurgical treatment of peri-implant mucositis: a systematic review and meta-analysis. Front Pharmacol 2021; 11: 541752
  • 50 Barootchi S, Ravidà A, Tavelli L, Wang HL. Nonsurgical treatment for peri-implant mucositis: a systematic review and meta-analysis. Int J Oral Implantol (New Malden) 2020; 13 (02) 123-139
  • 51 Gao J, Yu S, Zhu X, Yan Y, Zhang Y, Pei D. Does probiotic lactobacillus have an adjunctive effect in the nonsurgical treatment of peri-implant diseases? a systematic review and meta-analysis. J Evid Based Dent Pract 2020; 20 (01) 101398
  • 52 İnce G, Gürsoy H, İpçi ŞD, Cakar G, Emekli-Alturfan E, Yılmaz S. Clinical and biochemical evaluation of lozenges containing Lactobacillus reuteri as an adjunct to non-surgical periodontal therapy in chronic periodontitis. J Periodontol 2015; 86 (06) 746-754
  • 53 Skorupka W, Zurek K, Kokot T. et al. Assessment of oral hygiene in adults. Cent Eur J Public Health 2012; 20 (03) 233-236
  • 54 Su S, Lipsky MS, Licari FW, Hung M. Comparing oral health behaviours of men and women in the United States. J Dent 2022; 122: 104157
  • 55 Lipsky MS, Su S, Crespo CJ, Hung M. Men and oral health: a review of sex and gender differences. Am J Men Health 2021; 15 (03) 15 579883211016361
  • 56 Emecen-Huja P, Eubank TD, Shapiro V, Yildiz V, Tatakis DN, Leblebicioglu B. Peri-implant versus periodontal wound healing. J Clin Periodontol 2013; 40 (08) 816-824
  • 57 Hariton E, Locascio JJ. Randomised controlled trials - the gold standard for effectiveness research: study design: randomised controlled trials. BJOG 2018; 125 (13) 1716