{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,9]],"date-time":"2026-03-09T23:46:08Z","timestamp":1773099968170,"version":"3.50.1"},"reference-count":52,"publisher":"MDPI AG","issue":"6","license":[{"start":{"date-parts":[[2023,5,30]],"date-time":"2023-05-30T00:00:00Z","timestamp":1685404800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Microorganisms"],"abstract":"<jats:p>The aim of this systematic review was to evaluate the actual efficacy of Lactobacillus reuteri (L. reuteri) on the periodontal clinical parameters when used concomitantly to the nonsurgical periodontal treatment. Searches were conducted through PubMed Central, Online Knowledge Library, Science Direct, Scielo, and Cochrane databases from 2012 to 2022. The focused question was \u201cIn patients with periodontitis, will the probiotic L. reuteri, when administrated as an adjunct to nonsurgical periodontal treatment, compared to the nonsurgical periodontal treatment alone, result in better clinical outcomes?\u201d The following information was extracted from the articles: author and year of publication, type of study, follow-up, sample size and number of defects, and clinical characteristics and details. All included studies were qualitatively assessed using the Critical Appraisal tools according to the Joanna Briggs Institute. Twenty-four articles were full-text reading, but only 9 articles were included. The number of patients enrolled was 287, aged between 18 and 56 years. All periodontal parameters were evaluated. The \u201cfollow-up\u201d varied (14, 40, 84, 90, 180, and 360 days). Most articles supported the clinical benefits of L. reuteri as an adjunct to SRP compared to SRP alone. A common finding at the beginning period was thatno statistically different results were observed between the test and control groups; otherwise, at the last period, a significant improvement was found in favor of the probiotic use (p = 0.001) for all the clinical parameters. The use of L. reuteri as an adjunct to nonsurgical periodontal treatment may result in significantly better clinical outcomes than nonsurgical periodontal treatment alone; but the conclusion must be carefully interpreted because of the heterogeneity found among the studies.<\/jats:p>","DOI":"10.3390\/microorganisms11061449","type":"journal-article","created":{"date-parts":[[2023,5,31]],"date-time":"2023-05-31T02:01:15Z","timestamp":1685498475000},"page":"1449","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":15,"title":["Influence of the Probiotic L. reuteri on Periodontal Clinical Parameters after Nonsurgical Treatment: A Systematic Review"],"prefix":"10.3390","volume":"11","author":[{"given":"Carlota","family":"Och\u00f4a","sequence":"first","affiliation":[{"name":"FP-I3ID, FCS, Fernando Pessoa University, 4249-004 Porto, Portugal"}]},{"given":"Filipe","family":"Castro","sequence":"additional","affiliation":[{"name":"FP-I3ID, FCS, Fernando Pessoa University, 4249-004 Porto, Portugal"}]},{"given":"Jos\u00e9 Frias","family":"Bulhosa","sequence":"additional","affiliation":[{"name":"FP-I3ID, FCS, Fernando Pessoa University, 4249-004 Porto, Portugal"}]},{"given":"Concei\u00e7\u00e3o","family":"Manso","sequence":"additional","affiliation":[{"name":"FP-I3ID, FCS, Fernando Pessoa University, 4249-004 Porto, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7603-3544","authenticated-orcid":false,"given":"Juliana Campos Hasse","family":"Fernandes","sequence":"additional","affiliation":[{"name":"Periodontics and Oral Medicine Department, University of Michigan School of Dentistry, Ann Arbor, MI 48109, USA"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3022-4390","authenticated-orcid":false,"given":"Gustavo Vicentis Oliveira","family":"Fernandes","sequence":"additional","affiliation":[{"name":"Periodontics and Oral Medicine Department, University of Michigan School of Dentistry, Ann Arbor, MI 48109, USA"}]}],"member":"1968","published-online":{"date-parts":[[2023,5,30]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Vestman, N.R., Chen, T., Holgerson, P.L., \u00d6hman, C., and Johansson, I. (2015). Oral microbiota shift after 12-week supplementation with Lactobacillus reuteri DSM 17938 and PTA 5289; a randomized control trial. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0125812"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"375","DOI":"10.3920\/BM2018.0150","article-title":"Effects of Lactobacillus reuteri as an adjunct to the treatment of periodontitis in smokers: Randomised clinical trial","volume":"10","author":"Theodoro","year":"2019","journal-title":"Benef. Microbes"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"944","DOI":"10.1902\/jop.2016.150665","article-title":"Clinical Effects of Lactobacillus rhamnosus in Non-Surgical Treatment of Chronic Periodontitis: A Randomized Placebo-Controlled Trial With 1-Year Follow-Up","volume":"87","author":"Morales","year":"2016","journal-title":"J. Periodontol."},{"key":"ref_4","unstructured":"CDC\u2014Centers for Disease Control and Prevention (2022, September 02). Periodontal Disease, Available online: https:\/\/www.cdc.gov\/oralhealth\/conditions\/periodontal-disease.html#periodontal."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"1177","DOI":"10.1002\/JPER.19-0464","article-title":"Effectiveness of scaling and root planing with and without adjunct probiotic therapy in the treatment of chronic periodontitis among shamma users and non-users: A randomized controlled trial","volume":"91","author":"Vohra","year":"2020","journal-title":"J. Periodontol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1411","DOI":"10.1007\/s00784-020-03449-4","article-title":"Probiotic strains of Lactobacillus brevis and Lactobacillus plantarum as adjunct to non-surgical periodontal therapy: 3-month results of a randomized controlled clinical trial","volume":"25","author":"Pudgar","year":"2021","journal-title":"Clin. Oral Investig."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1111\/jcpe.13264","article-title":"Adjunctive effect of systemic antimicrobials in periodontitis therapy: A systematic review and meta-analysis","volume":"47","author":"Teughels","year":"2020","journal-title":"J. Clin. Periodontol."},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Jentsch, H.F.R., Dietrich, M., and Eick, S. (2020). Non-surgical periodontal therapy with adjunctive amoxicillin\/metronidazole or metronidazole when no Aggregatibacter actinomycetemcomitans is detected\u2014A randomized clinical trial. Antibiotics, 9.","DOI":"10.3390\/antibiotics9100686"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"3967","DOI":"10.1007\/s00784-020-03727-1","article-title":"Effects of adjunctive light-activated disinfection and probiotics on clinical and microbiological parameters in periodontal treatment: A randomized, controlled, clinical pilot study","volume":"25","author":"Patyna","year":"2021","journal-title":"Clin. Oral Investig."},{"key":"ref_10","first-page":"66","article-title":"Probiotic Lactobacillus reuteri effect\u2019s on the levels of interleukin-4 in periodontitis patients after scaling and root planing","volume":"12","author":"Sinulingga","year":"2020","journal-title":"Int. J. Appl. Pharm."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"181","DOI":"10.2298\/SGS2104181A","article-title":"Clinical effects of local use of probiotics as an adjunct to non-surgical periodontal therapy","volume":"68","author":"Adamovic","year":"2021","journal-title":"Stomatol. Glas. Srb."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"72","DOI":"10.1034\/j.1600-0757.2002.280104.x","article-title":"Topical antiseptics and antibiotics in the initial therapy of chronic adult periodontitis: Microbiological aspects","volume":"28","author":"Quirynen","year":"2002","journal-title":"Periodontology"},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Canut-Delgado, N., Laura Giovannoni, M., and Chimenos-K\u00fcstner, E. (2021). Are probiotics a possible treatment of periodontitis? Probiotics against periodontal disease: A systematic review. Br. Dent. J., 1\u20137.","DOI":"10.1038\/s41415-021-3624-5"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"506","DOI":"10.1038\/nrgastro.2014.66","article-title":"Expert consensus document: The international scientific association for probiotics and prebiotics consensus statement on the scope and appropriate use of the term probiotic","volume":"11","author":"Hill","year":"2014","journal-title":"Nat. Rev. Gastroenterol. Hepatol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1217","DOI":"10.1111\/jcpe.13191","article-title":"A double-blind, paralleled-arm, placebo-controlled and randomized clinical trial of the effectiveness of probiotics as an adjunct in periodontal care","volume":"46","author":"Pelekos","year":"2019","journal-title":"J. Clin. Periodontol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"2015","DOI":"10.1007\/s00784-019-03065-x","article-title":"Clinical efficacy of Lactobacillus reuteri-containing lozenges in the supportive therapy of generalized periodontitis stage III and IV, grade C: 1-year results of a double-blind randomized placebo-controlled pilot study","volume":"24","author":"Grusovin","year":"2020","journal-title":"Clin. Oral Investig."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"84","DOI":"10.1111\/clr.13555","article-title":"The usage of a lactobacilli probiotic in the non-surgical therapy of peri-implantitis: A randomized pilot study","volume":"31","author":"Laleman","year":"2020","journal-title":"Clin. Oral Implant. Res."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"495","DOI":"10.1007\/s00005-014-0277-y","article-title":"Effect of Oral Administration Involving a Probiotic Strain of Lactobacillus reuteri on Pro-Inflammatory Cytokine Response in Patients with Chronic Periodontitis","volume":"62","author":"Szkaradkiewicz","year":"2014","journal-title":"Arch. Immunol. Et Ther. Exp."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"777","DOI":"10.7326\/M14-2385","article-title":"The PRISMA extension statement for reporting of systematic reviews incorporating network meta-analyses of health care interventions: Checklist and explanations","volume":"162","author":"Hutton","year":"2015","journal-title":"Ann. Intern. Med."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"n71","DOI":"10.1136\/bmj.n71","article-title":"The PRISMA 2020 statement: An updated guideline for reporting systematic reviews","volume":"372","author":"Page","year":"2021","journal-title":"BMJ"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1025","DOI":"10.1111\/jcpe.12155","article-title":"Clinical and microbiological effects of Lactobacillus reuteri probiotics in the treatment of chronic periodontitis: A randomized placebo-controlled study","volume":"40","author":"Teughels","year":"2013","journal-title":"J. Clin. Periodontol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"363","DOI":"10.1111\/jcpe.12387","article-title":"Clinical and microbiological effects of probiotic lozenges in the treatment of chronic periodontitis: A 1-year follow-up study","volume":"42","author":"Tekce","year":"2015","journal-title":"J. Clin. Periodontol."},{"key":"ref_23","first-page":"31","article-title":"Clinical Efficacy of Probiotics as an Adjunct to Scaling and Root Planning in The Treatment of Chronic Periodontitis","volume":"24","author":"Ikram","year":"2019","journal-title":"Ann. ASH KMDC"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1098","DOI":"10.1111\/jcpe.13329","article-title":"Effects of adjunctive probiotic L. reuteri lozenges on S\/RSD outcomes at molar sites with deep pockets","volume":"47","author":"Pelekos","year":"2020","journal-title":"J. Clin. Periodontol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"41","DOI":"10.2478\/bjdm-2021-0003","article-title":"Effects of Lactobacillus reuteri lozenges (Prodentis) as adjunctive therapeutic agent in non-surgical therapy of periodontitis","volume":"25","year":"2021","journal-title":"Balk. J. Dent. Med."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"525","DOI":"10.4103\/jisp.jisp_114_21","article-title":"The adjunctive effect of probiotics to nonsurgical treatment of chronic periodontitis: A randomized controlled clinical trial","volume":"25","author":"Shoukheba","year":"2021","journal-title":"J. Indian Soc. Periodontol."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Sufaru, I.G., Lazar, L., Sincar, D.-C., Martu, M.-A., Pasarin, L., Luca, E.-O., Stefanescu, A., Froicu, E.-M., and Solomon, S.-M. (2022). Clinical Effects of Locally Delivered Lactobacillus reuteri as Adjunctive Therapy in Patients with Periodontitis: A Split-Mouth Study. Appl. Sci., 12.","DOI":"10.3390\/app12052470"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"747","DOI":"10.1126\/science.147.3659.747","article-title":"Probiotics: Growth-Promoting Factors Produced by Microorganisms","volume":"147","author":"Lilly","year":"1965","journal-title":"Science"},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Kang, J.H., Yun, S.I., Park, M.H., Park, J.H., Jeong, S.Y., and Park, H.O. (2013). Anti-Obesity Effect of Lactobacillus gasseri BNR17 in High-Sucrose Diet-Induced Obese Mice. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0054617"},{"key":"ref_30","first-page":"224","article-title":"In-Vitro Characterization of the Anti-Cancer Activity of the Probiotic Bacterium Lactobacillus fermentum NCIMB 5221 and Potential Against Colorectal Cancer","volume":"7","author":"Kahouli","year":"2015","journal-title":"J. Cancer Sci. Ther."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1186\/1757-4749-4-15","article-title":"Probiotics for Human Health\u2014New Innovations and Emerging Trends","volume":"4","author":"Sunita","year":"2012","journal-title":"Gut Pathog."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"60","DOI":"10.1016\/j.jff.2014.04.013","article-title":"Antiallergic Activity of Probiotics from Mongolian Dairy Products on Type I Allergy in Mice and Mode of Antiallergic Action","volume":"9","author":"Takeda","year":"2014","journal-title":"J. Funct. Foods"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"5","DOI":"10.4103\/0976-7800.83253","article-title":"Role of Probiotics in Urogenital Healthcare","volume":"2","author":"Waigankar","year":"2011","journal-title":"J. Mid-Life Health"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"746","DOI":"10.1902\/jop.2015.140612","article-title":"Clinical and Biochemical Evaluation of Lozenges Containing Lactobacillus reuteri as an Adjunct to Non-Surgical Periodontal Therapy in Chronic Periodontitis","volume":"86","author":"Ince","year":"2015","journal-title":"J. Periodontol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"10","DOI":"10.3389\/fmicb.2016.00010","article-title":"Therapeutic Application of Synbiotics, a Fusion of Probiotics and Prebiotics, and Biogenics as a New Concept for Oral Candida Infections: A Mini Review","volume":"7","author":"Ohshima","year":"2016","journal-title":"Front. Microbiol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"150","DOI":"10.1007\/s12602-017-9351-1","article-title":"The Effect of Probiotics on Halitosis: A Systematic Review and Meta-Analysis","volume":"11","author":"Yoo","year":"2019","journal-title":"Probiotics Antimicrob. Proteins"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1300","DOI":"10.1007\/s12602-020-09652-9","article-title":"A Review of the Role of Probiotic Supplementation in Dental Caries","volume":"12","author":"Sivamaruthi","year":"2020","journal-title":"Probiotics Antimicrob. Proteins"},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Mahasneh, S.A., and Mahasneh, A.M. (2017). Probiotics: A Promising Role in Dental Health. Dent. J., 5.","DOI":"10.3390\/dj5040026"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1007\/s40496-017-0159-6","article-title":"Use of Probiotics and Oral Health","volume":"4","author":"Allaker","year":"2017","journal-title":"Curr. Oral Health Rep."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"3944","DOI":"10.1128\/JCM.43.8.3944-3955.2005","article-title":"Identification of Candidate Periodontal Pathogens and Beneficial Species by Quantitative 16s Clonal Analysis","volume":"43","author":"Kumar","year":"2005","journal-title":"J. Clin. Microbiol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"409","DOI":"10.1111\/j.2041-1014.2012.00663.x","article-title":"Beyond the Red Complex and Into More Complexity: The Polymicrobial Synergy and Dysbiosis (PSD) Model of Periodontal Disease Etiology","volume":"27","author":"Hajishengallis","year":"2012","journal-title":"Mol. Oral Microbiol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1115","DOI":"10.1902\/jop.2017.170213","article-title":"The Influence of a Bifidobacterium Animalis Probiotic on Gingival Health: A Randomized Controlled Clinical Trial","volume":"88","author":"Kuru","year":"2017","journal-title":"J. Periodontol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1038\/sj.ebd.6401270","article-title":"Limited Evidence Shows Short-Term Benefit of Probiotics When Used as an Adjunct to Scaling and Root Planing in the Treatment of Chronic Periodontitis","volume":"18","author":"Kumar","year":"2017","journal-title":"Evid. Based Dent."},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"Jansen, P.M., Abdelbary, M.M.H., and Conrads, G. (2021). A Concerted Probiotic Activity to Inhibit Periodontitis-Associated Bacteria. PLoS ONE, 16.","DOI":"10.1371\/journal.pone.0248308"},{"key":"ref_45","doi-asserted-by":"crossref","unstructured":"Stevens, M., Vollenweider, S., Lacroix, C., and Zurich, E.T.H. (2011). The Potential of Reuterin Produced by Lactobacillus reuteri as a Broad Spectrum Preservative in Food, Woodhead Publishing.","DOI":"10.1533\/9780857090522.1.129"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1111\/jre.12704","article-title":"Heat-Killed Lactobacillus reuteri and Cell-Free Culture Supernatant Have Similar Effects to Viable Probiotics During Interaction with Porphyromonas gingivalis","volume":"55","author":"Geraldo","year":"2020","journal-title":"J. Periodontal Res."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"ftaa044","DOI":"10.1093\/femspd\/ftaa044","article-title":"Interaction Between Lactobacillus reuteri and Periodontopathogenic Bacteria Using In Vitro and In Vivo (G. mellonella) Approaches","volume":"78","author":"Santos","year":"2020","journal-title":"Pathog. Dis."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"999","DOI":"10.3389\/fmicb.2020.00999","article-title":"Mitigation of the Toxic Effects of Periodontal Pathogens by Candidate Probiotics in Oral Keratinocytes, and in an Invertebrate Model","volume":"11","author":"Moman","year":"2020","journal-title":"Front. Microbiol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1016\/j.carbpol.2015.12.037","article-title":"Exopolysaccharides of Lactobacillus reuteri: Their Influence on Adherence of E. Coli to Epithelial Cells and Inflammatory Response","volume":"141","author":"Csank","year":"2016","journal-title":"Carbohydr. Polym."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"9","DOI":"10.4167\/jbv.2011.41.1.9","article-title":"Effect of Weissella Cibaria on Fusobacterium Nucleatum-Induced Interleukin-6 and Interleukin-8 Production in KB Cells","volume":"41","author":"Kang","year":"2011","journal-title":"J. Bacteriol. Virol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"1198","DOI":"10.1111\/jcpe.12995","article-title":"Effects of Bifidobacterium Probiotic on the Treatment of Chronic Periodontitis: A Randomized Clinical Trial","volume":"45","author":"Invernici","year":"2018","journal-title":"J. Clin. Periodontol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"378","DOI":"10.1111\/jre.12523","article-title":"Clinical and Microbiological Evaluation of the Effect of Lactobacillus reuteri in the Treatment of Mucositis and Peri-Implantitis: A Triple-Blind Randomized Clinical Trial","volume":"53","author":"Palao","year":"2018","journal-title":"J. Periodontal. Res."}],"container-title":["Microorganisms"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2607\/11\/6\/1449\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T19:45:32Z","timestamp":1760125532000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2607\/11\/6\/1449"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,5,30]]},"references-count":52,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2023,6]]}},"alternative-id":["microorganisms11061449"],"URL":"https:\/\/doi.org\/10.3390\/microorganisms11061449","relation":{},"ISSN":["2076-2607"],"issn-type":[{"value":"2076-2607","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,5,30]]}}}