Pre and Probiotics Involved in the Modulation of Oral Bacterial Species: New Therapeutic Leads in Mental Disorders?
Abstract
:1. Introduction
2. Materials and Methods
2.1. Search Strategy
2.2. Study Detection
2.3. Inclusion and Exclusion Criteria
2.4. Data Collection
3. Results
3.1. Study Selection
3.2. Prebiotics
3.3. Probiotics
3.3.1. Modulation of the Oral Microbiome
3.3.2. Antibacterial Activity
3.3.3. Modulation of Immunological or Inflammatory Mediators of Oral Dysbiosis
4. Discussion
5. Limits and Perspectives
6. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Krishnan, K.; Chen, T.; Paster, B.J. A practical guide to the oral microbiome and its relation to health and disease. Oral Dis. 2017, 23, 276–286. [Google Scholar] [CrossRef] [Green Version]
- Marsh, P.D. Microbiology of dental plaque biofilms and their role in oral health and caries. Dent. Clin. N. Am. 2010, 54, 441–454. [Google Scholar] [CrossRef] [PubMed]
- Choi, J.U.; Lee, J.B.; Kim, K.H.; Kim, S.; Seol, Y.J.; Lee, Y.M.; Rhyu, I.C. Comparison of Periodontopathic Bacterial Profiles of Different Periodontal Disease Severity Using Multiplex Real-Time Polymerase Chain Reaction. Diagnostics 2020, 10, 965. [Google Scholar] [CrossRef]
- Bourgeois, D.; Inquimbert, C.; Ottolenghi, L.; Carrouel, F. Periodontal Pathogens as Risk Factors of Cardiovascular Diseases, Diabetes, Rheumatoid Arthritis, Cancer, and Chronic Obstructive Pulmonary Disease—Is There Cause for Consideration? Microorganisms 2019, 7, 424. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lavigne, S.E.; Forrest, J.L. An umbrella review of systematic reviews of the evidence of a causal relationship between perio-dontal disease and cardiovascular diseases: Position paper from the Canadian Dental Hygienists Association. Can. J. Dent. Hyg. 2020, 54, 32–41. [Google Scholar] [PubMed]
- Lafon, A.; Pereira, B.; Dufour, T.; Rigouby, V.; Giroud, M.; Béjot, Y.; Tubert-Jeannin, S. Periodontal disease and stroke: A me-ta-analysis of cohort studie. Eur. J. Neurol. 2014, 9, 1155–1161. [Google Scholar] [CrossRef]
- Lavigne, S.E.; Forrest, J.L. An umbrella review of systematic reviews of the evidence of a causal relationship between perio-dontal disease and adverse pregnancy outcomes: A position paper from the Canadian Dental Hygienists Association. Can. J. Dent. Hyg. 2020, 54, 92–100. [Google Scholar]
- Genco, R.J.; Graziani, F.; Hasturk, H. Effects of periodontal disease on glycemic control, complications, and incidence of dia-betes mellitus. Periodontol. 2000 2020, 83, 59–65. [Google Scholar] [CrossRef] [PubMed]
- Awano, S.; Ansai, T.; Takata, Y.; Soh, I.; Akifusa, S.; Hamasaki, T.; Yoshida, A.; Sonoki, K.; Fujisawa, K.; Takehara, T. Oral health and mortality risk from pneumonia in the elderly. J. Dent. Res. 2008, 87, 334–339. [Google Scholar] [CrossRef]
- Karpiński, T.M. Role of Oral Microbiota in Cancer Development. Microorganisms 2019, 7, 20. [Google Scholar] [CrossRef] [Green Version]
- Yang, Q.; Ding, H.; Wei, W.; Liu, J.; Wang, J.; Ren, J.; Chan, W.; Wang, M.; Hao, L.; Li, J.; et al. Periodontitis aggravates kidney injury by upregulating STAT1 expression in a mouse model of hypertension. FEBS Open Bio 2021, 11, 880–889. [Google Scholar] [CrossRef] [PubMed]
- Maitre, Y.; Micheneau, P.; Delpierre, A.; Mahalli, R.; Guerin, M.; Amador, G.; Denis, F. Did the brain and oral microbiota talk to each other? A review of the literature. J. Clin. Med. 2020, 9, 3876. [Google Scholar] [CrossRef] [PubMed]
- Engevik, M.A.; Luk, B.; Chang-Graham, A.L.; Hall, A.; Herrmann, B.; Ruan, W.; Endres, B.T.; Shi, Z.; Garey, K.W.; Hyser, J.M.; et al. Bifidobacterium dentium Fortifies the Intestinal Mucus Layer via Autophagy and Calcium Signaling Pathways. mBio 2019, 10, e01087-19. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- O’Callaghan, A.; Van Sinderen, D. Bifidobacteria and Their Role as Members of the Human Gut Microbiota. Front. Microbiol. 2016, 7, 925. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hill, C.; Guarner, F.; Reid, G.; Gibson, G.R.; Merenstein, D.J.; Pot, B.; Morelli, L.; Canani, R.B.; Flint, H.J.; Salminen, S.; et al. Expert consensus document. The International Scientific Association for Probiotics and Prebiotics consen-sus statement on the scope and appropriate use of the term probiotic. Nat. Rev. Gastroenterol. Hepatol. 2014, 11, 506–514. [Google Scholar] [CrossRef] [Green Version]
- Gibson, G.R.; Hutkins, R.; Sanders, M.E.; Prescott, S.L.; Reimer, R.A.; Salminen, S.J.; Scott, K.; Stanton, C.; Swanson, K.S.; Cani, P.D.; et al. Expert consensus document: The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nat. Rev. Gastroenterol. Hepatol. 2017, 14, 491–502. [Google Scholar] [CrossRef] [Green Version]
- Ursell, L.K.; Metcalf, J.L.; Parfrey, L.W.; Knight, R. Defining the human microbiome. Nutr. Rev. 2012, 70, 38–44. [Google Scholar] [CrossRef] [Green Version]
- Jenkinson, H.F.; Lamont, R.J. Oral microbial communities in sickness and in health. Trends Microbiol. 2005, 13, 589–595. [Google Scholar] [CrossRef]
- Corby, P.M.; Lyons-Weiler, J.; Bretz, W.A.; Hart, T.C.; Aas, J.A.; Boumenna, T.; Goss, J.; Corby, A.L.; Junior, H.M.; Weyant, R.J.; et al. Microbial risk indicators of early childhood caries. J. Clin. Microbiol. 2005, 43, 5753–5759. [Google Scholar] [CrossRef] [Green Version]
- Belda-Ferre, P.; Alcaraz, L.D.; Cabrera-Rubio, R.; Romero, H.; Simón-Soro, A.; Pignatell, M.; Mira, A. The oral metagenome in health and disease. ISME J. 2012, 6, 46–56. [Google Scholar] [CrossRef] [Green Version]
- Rai, B.; Kaur, J.; Anand, S.C. Possible relationship between periodontitis and dementia in a North Indian old age population: A pilot study. Gerodontology 2010, 29, 200–205. [Google Scholar] [CrossRef] [PubMed]
- Sochocka, M.; Sobczyński, M.; Sender-Janeczek, A.; Zwolinska, K.; Błachowicz, O.; Tomczyk, T.; Leszek, J. Association between Periodontal Health Status and Cognitive Abilities. The Role of Cytokine Profile and Systemic Inflammation. Curr. Alzheimer Res. 2017, 14, 978–990. [Google Scholar] [CrossRef] [Green Version]
- Qiao, Y.; Wu, M.; Feng, Y.; Zhou, Z.; Chen, L.; Chen, F. Alterations of oral microbiota distinguish children with autism spec-trum disorders from healthy controls. Sci. Rep. 2018, 8, 1597. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Oliveira, A.C.; Paiva, S.M.; Campos, M.R.; Czeresnia, D. Factors associated with malocclusions in children and adolescents with Down syndrome. Am. J. Orthod. Dentofac. Orthop. 2008, 133, 489.e1–489.e8. [Google Scholar] [CrossRef]
- Kuboniwa, M.; Tribble, G.D.; James, C.E.; Kilic, A.O.; Tao, L.; Herzberg, M.C.; Shizukuishi, S.; Lamont, R.J. Streptococcus gordonii utilizes several distinct gene functions to recruit Porphyromonas gingivalis into a mixed community. Mol. Microbiol. 2006, 60, 121–139. [Google Scholar] [CrossRef] [PubMed]
- Tanner, A.C.; Paster, B.J.; Lu, S.C.; Kanasi, E.; Kent, R., Jr.; Van Dyke, T.; Sonis, S.T. Subgingival and tongue microbiota during early periodontitis. J. Dent. Res. 2006, 85, 318–323. [Google Scholar] [CrossRef] [Green Version]
- Ledder, R.G.; Gilbert, P.; Huws, S.A.; Aarons, L.; Ashley, M.P.; Hull, P.S.; McBain, A.J. Molecular analysis of the subgingival microbiota in health and disease. Appl. Environ. Microbiol. 2007, 73, 516–523. [Google Scholar] [CrossRef] [Green Version]
- Colombo, A.P.; Boches, S.K.; Cotton, S.L.; Goodson, J.M.; Kent, R.; Haffajee, A.D.; Socransky, S.S.; Hasturk, H.; Van Dyke, T.E.; Dewhirst, F.; et al. Comparisons of subgingival microbial profiles of refractory periodontitis, severe periodontitis, and periodontal health using the human oral microbe identification microarray. J. Periodontol. 2009, 80, 1421–1432. [Google Scholar] [CrossRef]
- Khocht, A.; Yaskell, T.; Janal, M.; Turner, B.F.; Rams, T.E.; Haffajee, A.D.; Socransky, S.S. Subgingival microbiota in adult Down syndrome periodontitis. J. Periodontal Res. 2012, 47, 500–507. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cunha, F.A.; Cota, L.O.M.; Cortelli, S.C.; Miranda, T.B.; Neves, F.S.; Cortelli, J.R.; Costa, F.O. Periodontal condition and levels of bacteria associated with periodontitis in individuals with bipolar affective disorders: A case-control study. J. Periodontal Res. 2018, 54, 63–72. [Google Scholar] [CrossRef] [Green Version]
- Castro-Nallar, E.; Bendall, M.L.; Pérez-Losada, M.; Sabuncyan, S.; Severance, E.G.; Dickerson, F.B.; Schroeder, J.R.; Yolken, R.H.; Crandall, K.A. Composition, taxonomy and functional diversity of the oropharynx microbiome in individuals with schizophrenia and controls. PeerJ 2015, 3, e1140. [Google Scholar] [CrossRef]
- Riviere, G.R.; Riviere, K.H.; Smith, K.S. Molecular and immunological evidence of oral Treponema in the human brain and their association with Alzheimer’s disease. Oral Microbiol. Immunol. 2002, 17, 113–118. [Google Scholar] [CrossRef] [PubMed]
- Kamer, A.R.; Craig, R.G.; Pirraglia, E.; Dasanayake, A.P.; Norman, R.G.; Boylan, R.J.; Nehorayoff, A.; Glodzik, L.; Brys, M.; De Leon, M.J. TNF-α and antibodies to periodontal bacteria discriminate between Alzheimer’s disease patients and normal sub-jects. J. Neuroimmunol. 2009, 216, 92–97. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Carabotti, M.; Scirocco, A.; Maselli, M.A.; Severi, C. The gut-brain axis: Interactions between enteric microbiota, central and enteric nervous systems. Ann. Gastroenterol. 2015, 28, 203–209. [Google Scholar] [PubMed]
- Moher, D.; Liberati, A.; Tetzlaff, J.; Altman, D.G. Preferred reporting items for systematic reviews and metaanalyses: The PRISMA statement. Int. J. Surg. 2010, 8, 336–341. [Google Scholar] [CrossRef] [Green Version]
- Hooks, K.B.; Konsman, J.P.; O’Malley, M.A. Microbiota-gut-brain research: A critical analysis. Behav. Brain Sci. 2018, 42, 1–40. [Google Scholar] [CrossRef]
- Gasbarrini, G.; Bonvicini, F.; Gramenzi, A. Probiotics History. J. Clin. Gastroenterol. 2016, 50, 13–15. [Google Scholar] [CrossRef]
- Slomka, V.; Hernandez-Sanabria, E.; Herrero, E.R.; Zaidel, L.; Bernaerts, K.; Boon, N.; Quirynen, M.; Teughels, W. Nutritional stimulation of commensal oral bacteria suppresses pathogens: The prebiotic concept. J. Clin. Periodontol. 2017, 44, 344–352. [Google Scholar] [CrossRef]
- Rosier, B.T.; Buetas, E.; Moya-Gonzalvez, E.M.; Artacho, A.; Mira, A. Nitrate as a potential prebiotic for the oral microbiome. Sci. Rep. 2020, 10, 12895. [Google Scholar] [CrossRef] [PubMed]
- Jiménez-Hernández, N.; Serrano-Villar, S.; Domingo, A.; Pons, X.; Artacho, A.; Estrada, V.; Moya, A.; Gosalbes, M.J. Modu-lation of Saliva Microbiota through Prebiotic Intervention in HIV-Infected Individuals. Nutrients 2019, 11, 1346. [Google Scholar] [CrossRef] [Green Version]
- Madhwani, T.; McBain, A.J. Bacteriological effects of a Lactobacillus reuteri probiotic on in vitro oral biofilms. Arch. Oral Biol. 2011, 56, 1264–1273. [Google Scholar] [CrossRef]
- Jiang, Q.; Stamatova, I.; Kainulainen, V.; Korpela, R.; Meurman, J.H. Interactions between Lactobacillus rhamnosus GG and oral micro-organisms in an in vitro biofilm model. BMC Microbiol. 2016, 16, 149. [Google Scholar] [CrossRef] [Green Version]
- Mendi, A.; Köse, S.; Uçkan, D.; Akca, G.; Yilmaz, D.; Aral, L.; Gültekin, S.E.; Eroğlu, T.; Kiliç, E.; Uçkan, S. Lactobacillus rhamnosus could inhibit Porphyromonas gingivalis derived CXCL8 attenuation. J. Appl. Oral Sci. 2016, 24, 67–75. [Google Scholar] [CrossRef] [Green Version]
- Albuquerque-Souza, E.; Balzarini, D.; Ando-Suguimoto, E.S.; Ishikawa, K.H.; Simionato, M.R.L.; Holzhausen, M.; Mayer, M.P.A. Probiotics alter the immune response of gingival epithelial cells challenged by Porphyromonas gingivalis. J. Periodontal Res. 2019, 54, 115–127. [Google Scholar] [CrossRef]
- Jaffar, N.; Ishikawa, Y.; Mizuno, K.; Okinaga, T.; Maeda, T. Mature Biofilm Degradation by Potential Probiotics: Aggregati-bacter actinomycetemcomitans versus Lactobacillus spp. PLoS ONE 2016, 11, e0159466. [Google Scholar] [CrossRef]
- Oliveira, L.F.; Salvador, S.L.; Silva, P.H.; Furlaneto, F.A.; Figueiredo, L.; Casarin, R.; Ervolino, E.; Palioto, D.B.; Souza, S.L.; Taba, M., Jr.; et al. Benefits of Bifidobacterium animalis subsp. lactis Probiotic in Experimental Peri-odontitis. J. Periodontol. 2017, 88, 197–208. [Google Scholar] [CrossRef]
- Invernici, M.M.; Furlaneto, F.A.C.; Salvador, S.L.; Ouwehand, A.C.; Salminen, S.; Mantziari, A.; Vinderola, G.; Ervolino, E.; Santana, S.I.; Silva, P.H.F.; et al. Bifidobacterium animalis subsp lactis HN019 presents antimicrobial potential against periodontopathogens and modulates the immunological response of oral mucosa in periodontitis patients. PLoS ONE 2020, 15, e0238425. [Google Scholar]
- Dassi, E.; Ballarini, A.; Covello, G.; Quattrone, A.; Jousson, O.; De Sanctis, V.; Bertorelli, R.; Denti, M.A.; Segata, N. Enhanced microbial diversity in the saliva microbiome induced by short-term probiotic intake revealed by 16S rRNA sequencing on the IonTorrent PGM platform. J. Biotechnol. 2014, 190, 30–39. [Google Scholar] [CrossRef]
- Dassi, E.; Ferretti, P.; Covello, G.; Bertorelli, R.; Denti, M.A.; DeSanctis, V.; Tett, A.; Segata, N. The short-term impact of pro-biotic consumption on the oral cavity microbiome. Sci. Rep. 2018, 8, 10476. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Becirovic, A.; Abdi-Dezfuli, J.F.; Hansen, M.F.; Lie, S.A.; Vasstrand, E.N.; Bolstad, A.I. The effects of a probiotic milk drink on bacterial composition in the supra- and subgingival biofilm: A pilot study. Benef. Microbes 2018, 9, 865–874. [Google Scholar] [CrossRef] [PubMed]
- Tada, H.; Masaki, C.; Tsuka, S.; Mukaibo, T.; Kondo, Y.; Hosokawa, R. The effects of Lactobacillus reuteri probiotics com-bined with azithromycin on peri-implantitis: A randomized placebo-controlled study. J. Prosthodont. Res. 2018, 62, 89–96. [Google Scholar] [CrossRef] [PubMed]
- Kõll, P.; Mändar, R.; Marcotte, H.; Leibur, E.; Mikelsaar, M.; Hammarström, L. Characterization of oral lactobacilli as poten-tial probiotics for oral health. Oral Microbiol. Immunol. 2008, 23, 139–147. [Google Scholar] [CrossRef]
- Teanpaisan, R.; Piwat, S.; Dahlén, G. Inhibitory effect of oral Lactobacillus against oral pathogens. Lett. Appl. Microbiol. 2011, 53, 452–459. [Google Scholar] [CrossRef]
- Van Essche, M.; Loozen, G.; Godts, C.; Boon, N.; Pauwels, M.; Quirynen, M.; Teughels, W. Bacterial antagonism against peri-odontopathogens. J. Periodontol. 2013, 84, 801–811. [Google Scholar] [CrossRef] [PubMed]
- Chen, Y.T.; Hsieh, P.S.; Ho, H.H.; Hsieh, S.H.; Kuo, Y.W.; Yang, S.F.; Lin, C.W. Antibacterial activity of viable and heat-killed probiotic strains against oral pathogens. Lett. Appl. Microbiol. 2020, 70, 310–317. [Google Scholar] [CrossRef]
- Shin, H.S.; Baek, D.H.; Lee, S.H. Inhibitory effect of Lactococcus lactis on the bioactivity of periodontopathogens. J. Gen. Appl. Microbiol. 2018, 64, 55–61. [Google Scholar] [CrossRef] [Green Version]
- Higuchi, T.; Suzuki, N.; Nakaya, S.; Omagari, S.; Yoneda, M.; Hanioka, T.; Hirofuji, T. Effects of Lactobacillus salivarius WB21 combined with green tea catechins on dental caries, periodontitis, and oral malodor. Arch. Oral Biol. 2019, 98, 243–247. [Google Scholar] [CrossRef] [PubMed]
- Zhu, Y.; Xiao, L.; Shen, D.; Hao, Y. Competition between yogurt probiotics and periodontal pathogens in vitro. Acta Odontol. Scand. 2010, 68, 261–268. [Google Scholar] [CrossRef]
- Tobita, K.; Watanabe, I.; Tomokiyo, M.; Saito, M. Effects of heat-treated Lactobacillus crispatus KT-11 strain consumption on improvement of oral cavity environment: A randomised double-blind clinical trial. Benef. Microbes 2018, 9, 585–592. [Google Scholar] [CrossRef]
- Iniesta, M.; Herrera, D.; Montero, E.; Zurbriggen, M.; Matos, A.R.; Marín, M.J.; Sánchez-Beltrán, M.C.; Llama-Palacio, A.; Sanz, M. Probiotic effects of orally administered Lactobacillus reuteri-containing tablets on the subgingival and salivary mi-crobiota in patients with gingivitis. A randomized clinical trial. J. Clin. Periodontol. 2012, 39, 736–744. [Google Scholar] [CrossRef]
- Teughels, W.; Durukan, A.; Ozcelik, O.; Pauwels, M.; Quirynen, M.; Haytac, M.C. Clinical and microbiological effects of Lactobacillus reuteri probiotics in the treatment of chronic periodontitis: A randomized placebo-controlled study. J. Clin. Periodontol. 2013, 40, 1025–1035. [Google Scholar] [CrossRef] [Green Version]
- Montero, E.; Iniesta, M.; Rodrigo, M.; Marín, M.J.; Figuero, E.; Herrera, D.; Sanz, M. Clinical and microbiological effects of the adjunctive use of probiotics in the treatment of gingivitis: A randomized controlled clinical trial. J. Clin. Periodontol. 2017, 44, 708–716. [Google Scholar] [CrossRef]
- Imran, F.; Das, S.; Padmanabhan, S.; Rao, R.; Suresh, A.; Bharath, D. Evaluation of the efficacy of a probiotic drink contain-ing Lactobacillus casei on the levels of periodontopathic bacteria in periodontitis: A clinico-microbiologic study. Indian J. Dent. Res. 2015, 26, 462–468. [Google Scholar] [CrossRef]
- Sarmento, É.G.; Cesar, D.E.; Martins, M.L.; De Oliveira Góis, E.G.; Furtado Martins, E.M.; Da Rocha Campos, A.N.; Del’Duca, A.; De Oliveira Martins, A.D. Effect of probiotic bacteria in composition of children’s saliva. Food Res. Int. 2019, 116, 1282–1288. [Google Scholar] [CrossRef] [PubMed]
- Mayanagi, G.; Kimura, M.; Nakaya, S.; Hirata, H.; Sakamoto, M.; Benno, Y.; Shimauchi, H. Probiotic effects of orally admin-istered Lactobacillus salivarius WB21-containing tablets on periodontopathic bacteria: A double-blinded, placebo-controlled, randomized clinical trial. J. Clin. Periodontol. 2009, 36, 506–513. [Google Scholar] [CrossRef]
- Sajedinejad, N.; Paknejad, M.; Houshmand, B.; Sharafi, H.; Jelodar, R.; Shahbani Zahiri, H.; Noghabi, K.A. Lactobacillus salivarius NK02: A Potent Probiotic for Clinical Application in Mouthwash. Probiotics Antimicrob. Proteins 2018, 10, 485–495. [Google Scholar] [CrossRef]
- Zahradnik, R.T.; Magnusson, I.; Walker, C.; McDonell, E.; Hillman, C.H.; Hillman, J.D. Preliminary assessment of safety and effectiveness in humans of ProBiora3, a probiotic mouthwash. J. Appl. Microbiol. 2009, 107, 682–690. [Google Scholar] [CrossRef]
- Alanzi, A.; Honkala, S.; Honkala, E.; Varghese, A.; Tolvanen, M.; Söderling, E. Effect of Lactobacillus rhamnosus and Bifidobacterium lactis on gingival health, dental plaque, and periodontopathogens in adolescents: A randomised placebo-controlled clinical trial. Benef. Microbes 2018, 9, 593–602. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- Kobayashi, R.; Kobayashi, T.; Sakai, F.; Hosoya, T.; Yamamoto, M.; Kurita-Ochiai, T. Oral administration of Lactobacillus gasseri SBT2055 is effective in preventing Porphyromonas gingivalis-accelerated periodontal disease. Sci. Rep. 2017, 7, 545. [Google Scholar] [CrossRef]
- Maekawa, T.; Hajishengallis, G. Topical treatment with probiotic Lactobacillus brevis CD2 inhibits experimental periodontal inflammation and bone loss. J. Periodontal Res. 2014, 49, 785–791. [Google Scholar] [CrossRef] [Green Version]
- Keller, M.K.; Brandsborg, E.; Holmstrøm, K.; Twetman, S. Effect of tablets containing probiotic candidate strains on gingival inflammation and composition of the salivary microbiome: A randomised controlled trial. Benef. Microbes 2018, 9, 487–494. [Google Scholar] [CrossRef]
- Braathen, G.; Ingildsen, V.; Twetman, S.; Ericson, D.; Jørgensen, M.R. Presence of Lactobacillus reuteri in saliva coincide with higher salivary IgA in young adults after intake of probiotic lozenges. Benef. Microbes 2017, 8, 17–22. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jørgensen, M.R.; Keller, M.K.; Kragelund, C.; Hamberg, K.; Ericson, D.; Nielsen, C.H.; Twetman, S. Lactobacillus reuteri supplements do not affect salivary IgA or cytokine levels in healthy subjects: A randomized, double-blind, placebo-controlled, cross-over trial. Acta Odontol. Scand. 2016, 74, 399–404. [Google Scholar] [CrossRef] [PubMed]
- 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, 60–66. [Google Scholar] [CrossRef] [PubMed]
- Huang, R.; Li, M.; Gregory, R.L. Bacterial interactions in dental biofilm. Virulence 2011, 2, 435–444. [Google Scholar] [CrossRef] [PubMed]
- Silva, D.R.; Orlandi Sardi, J.d.C.; Pitangui, N.d.S.; Roque, S.M.; Da Silva, B.A.C.; Rosalen, P.L. Probiotics as an alternative antimicrobial therapy: Current reality and future directions. J. Funct. Foods 2020, 73, 104080. [Google Scholar] [CrossRef]
- Ramesh, G.; MacLean, A.G.; Philipp, M.T. Cytokines and chemokines at the crossroads of neuroinflammation, neurodegener-ation, and neuropathic pain. Mediat. Inflamm. 2013, 2013, 480739. [Google Scholar] [CrossRef] [Green Version]
- Suganya, K.; Koo, B.S. Gut-Brain Axis: Role of Gut Microbiota on Neurological Disorders and How Probiotics/Prebiotics Ben-eficially Modulate Microbial and Immune Pathways to Improve Brain Functions. Int. J. Mol Sci. 2020, 21, 7551. [Google Scholar] [CrossRef]
- Markowiak, P.; Śliżewska, K. Effects of Probiotics, Prebiotics, and Synbiotics on Human Health. Nutrients 2017, 9, 1021. [Google Scholar]
- Ansari, F.; Pourjafar, H.; Tabrizi, A.; Homayouni, A. The Effects of Probiotics and Prebiotics on Mental Disorders: A Review on Depression, Anxiety, Alzheimer, and Autism Spectrum Disorders. Curr. Pharm. Biotechnol. 2020, 21, 555–565. [Google Scholar] [CrossRef]
- Roberfroid, M. Prebiotics: The concept revisited. J. Nutr. 2007, 137, 830–837. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gibson, G.R.; Probert, H.M.; Loo, J.V.; Rastall, R.A.; Roberfroid, M.B. Dietary modulation of the human colonic microbiota: Updating the concept of prebiotics. Nutr. Res. Rev. 2004, 17, 259–275. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pandey, K.R.; Naik, S.R.; Vakil, B.V. Probiotics, prebiotics and synbiotics—A review. J. Food Sci. Technol. 2015, 52, 7577–7587. [Google Scholar] [CrossRef]
- Fijan, S. Microorganisms with claimed probiotic properties: An overview of recent literature. Int. J. Environ. Res. Public Health 2014, 11, 4745–4767. [Google Scholar] [CrossRef] [PubMed]
- Bermudez-Brito, M.; Plaza-Díaz, J.; Muñoz-Quezada, S.; Gómez-Llorente, C.; Gil, A. Probiotic mechanisms of action. Ann. Nutr. Metab. 2012, 61, 160–174. [Google Scholar] [CrossRef]
- Cornejo Ulloa, P.; Van der Veen, M.H.; Krom, B.P. Review: Modulation of the oral microbiome by the host to promote ecolog-ical balance. Odontology 2019, 107, 437–448. [Google Scholar] [CrossRef] [Green Version]
- Kisely, S. No Mental Health without Oral Health. Can. J. Psychiatry. 2016, 61, 277–282. [Google Scholar] [CrossRef] [Green Version]
- Coelho, J.M.F.; Miranda, S.S.; Da Cruz, S.S.; Dos Santos, D.N.; Trindade, S.C.; Cerqueira, E.M.M.; Passos-Soares, J.S.; Costa, M.D.C.N.; Figueiredo, A.C.M.G.; Hintz, A.M.; et al. Common mental disorder is associated with periodontitis. J. Periodontal Res. 2020, 55, 221–228. [Google Scholar] [CrossRef]
- Fratto, G.; Manzon, L. Use of psychotropic drugs and associated dental diseases. Int. J. Psychiatry Med. 2014, 48, 185–197. [Google Scholar] [CrossRef]
- Lamont, R.J.; Koo, H.; Hajishengallis, G. The oral microbiota: Dynamic communities and host interactions. Nat. Rev. Genet. 2018, 16, 745–759. [Google Scholar] [CrossRef] [PubMed]
- Holt, S.C.; Ebersole, J.L. Porphyromonas gingivalis, Treponema denticola, and Tannerella forsythia: The ‘red complex’, a prototype polybacterial pathogenic consortium in periodontitis. Periodontol. 2000 2005, 38, 72–122. [Google Scholar] [CrossRef] [PubMed]
- Dominy, S.S.; Lynch, C.; Ermini, F.; Benedyk, M.; Marczyk, A.; Konradi, A.; Nguyen, M.; Haditsch, U.; Raha, D.; Griffin, C.; et al. Porphyromonas gingivalis in Alzheimer’s disease brains: Evidence for disease causation and treatment with small-molecule inhibitors. Sci. Adv. 2019, 5, eaau3333. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shokryazdan, P.; Faseleh Jahromi, M.; Navidshad, B.; Liang, J.B. Effects of prebiotics on immune system and cytokine expres-sion. Med. Microbiol. Immunol. 2017, 206, 1–9. [Google Scholar] [CrossRef]
- Wan, L.Y.; Chen, Z.J.; Shah, N.P.; El-Nezami, H. Modulation of Intestinal Epithelial Defense Responses by Probiotic Bacteria. Crit. Rev. Food Sci. Nutr. 2016, 56, 2628–2641. [Google Scholar] [CrossRef]
- Pujari, R.; Banerjee, G. Impact of prebiotics on immune response: From the bench to the clinic. Immunol. Cell Biol. 2021, 99, 255–273. [Google Scholar] [CrossRef]
- Pape, K.; Tamouza, R.; Leboyer, M.; Zipp, F. Immunoneuropsychiatry-novel perspectives on brain disorders. Nat. Rev. Neurol. 2019, 15, 317–328. [Google Scholar] [CrossRef]
- Denis, F.; Siu-Paredes, F.; Maitre, Y.; Amador, G.; Rude, N. A qualitative study on experiences of persons with schizophrenia in oral-health-related quality of life. Braz. Oral Res. 2021, 35, e050. [Google Scholar] [CrossRef]
Reference(s) | Study Design | Prebiotic Compound | Objectives | Prebiotic Administration | Mains Results and Limitations * |
---|---|---|---|---|---|
Slomka et al. (2017) [38] | In vitro | m-inositol, lactitol, alpha-methyl-d-galactoside, beta-methyl-d-galactoside, turanose, N-acetyl-d-manno-samine, Met-Pro, Phe-Glu, l-aspartic acid andsuccinic acid. | Identification of potential oral prebiotics that selectively stimulate commensal albeit beneficial bacteria of the resident oral microbial community while suppressing the growth of pathogenic bacteria | Not relevant | Beta-methyl-d-galactoside and N- acetyl-d-mannosamine could be identified as potential oral prebiotic compounds, triggering selectively beneficial oral bacteria throughout the experiments and shifting dual species biofilm communities towards a beneficial dominating composition. Beta-methyl-d-galactoside selectively stimulated S. salivarius causing a decrease of F. nucleatum and of P. gingivalis in the biofilm. N-acetyl-d-mannosamine was the only compound that in all beneficial-pathogen combinations did not lead to an outgrowth of any of the pathogenic species. Besides, S. mitis and S. sanguinis were significantly stimulated causing a reduction of A. actinomycetemcomitans and S. sobrinus * in vitro, oral prebiotic compounds need to be confirmed in multi-species environments |
Rosier et al. (2020) [39] | In vitro | Nitrate | Evaluation of the short-term effect of a single dose of nitrate on pH, oral biofilm growth and bacterial composition | Not relevant | Signifcantly higher levels of the oral health-associated nitrate (6.5 mM) -reducing genera Neisseria (3.1×) and Rothia (2.9×) were detected in the nitrate condition already after 5 h. Periodontitis-associated genera (Porphyromonas, Fusobacterium, Leptotrichia, Prevotella, and Alloprevotella) were significantly reduced after 5 h and 9 h. The addition of 6.5 mM nitrate did not show signifcant changes in real-time impedance measurements of bioflm formation compared to the control condition. * in vitro study |
Jiménez-Hernández et al. (2019) [40] | Cross sectional study (n = 32) | Mixture of short-chain galacto-oligosaccharides, long-chain fructo-oligosaccharides and glutamine | Characterization of the compositional changes associated with prebiotic intervention on salivary microbiota in HIV-infected individuals. Study of the interplay between oral and gut microbiota determining the bacterial co-occurrences in both habitats. | Daily consumption of mixture of short-chain galacto-oligosaccharides (5 g), long-chain fructo-oligosaccharides (10 g), and glutamine (5 g) provided for 6 weeks. | Prebiotic intervention modified the microbiota structure Drastic decrease in alpha diversity parameters, as well as a change of beta diversity, without a clear directionality toward a healthy microbiota. * Sample size, study design |
Reference(s) | Study Design | Probiotics | Objectives | Probiotic Administration | Mains Results and Limitations * |
---|---|---|---|---|---|
Madhwani et al. (2011) [41] | In vitro | L. reuteri ATCC 55730 L. reuteri ATCC PTA 5289 | Investigation of the effects of an oral probiotic bacterium, Lactobacillus reuteri on the composition of nascent plaques (grown in short-term hydroxyapatite disc models) and in steady-state, continuous culture, in vitro dental plaques. Determination of the ecological fate of the probiotic bacterium in continuous culture in vitro plaques. | Not relevant | The introduction of L. reuteri bacteria to in vitro oral models resulted in alterations in both nascent and developed plaque ecosystems, which included increases in numbers of exogenous lactobacilli but also in increases in streptococci and Gram-negative anaerobes. L. reuteri bacteria persisted and potentially integrated into continuous culture dental plaque biofilms for at least 20 days following cessation of dosing. * In vitro study |
Jiang et al. (2016) [42] | In vitro | L. rhamnosus GG | Investigation of the ability of probiotic Lactobacillus rhamnosus GG to integrate in oral biofilm and affect its species composition. | Not relevant | L. rhamnosus lowered the biofilm-forming ability of F. nucleatum and successfully integrated in all oral biofilms. L. rhamnosus reduced the counts of S. sanguinis and C. albicans L. rhamnosus only slightly reduced the adhesion of S. mutans. C. albicans significantly promoted the growth of L.GG. * In vitro study |
Mendi et al. (2016) [43] | In vitro | L. rhamnosus ATCC9595 | Determination of P. gingivalis modulatory effects on the inflammatory response of gingival stromal stem cells (G-MSSCs), including the release of CXCL8, and the expression of TLRs Determination of the L. rhamnosus preventive effect on CXCL8 inhibition in experimental inflammation. | Not relevant | L. rhamnosus showed higher adhesive properties than P. gingivalis on G-MSSCs. When G-MSSCs were pretreated with L. rhamnosus before P. gingivalis stimulation, CXCL8 secretions were found to increase. * In vitro study |
Albuquerque-Souza et al. (2019) [44] | In vitro | L. reuteri DSM 17938, L. rhamnosus Lr-32™, L. rhamnosus HN001™, L. acidophilus LA-5™, L. acidophilus NCFM®, L. casei 324 m, Bifidobacterium longum subsp. infantis ATCC15697, B. animalis subsp. lactis BB-12™, B. breve 1101A, B. longum 51A, B. pseudolongum 1191A, B. bifidum | Evaluation of the effect of several clinical isolates and commercially available Lactobacillus sp. and Bifidobacterium sp. On gingival epithelial cells (GECs) challenged by P. gingivalis. | Not relevant | Probiotics may prevent cell death and reduce bacterial adhesion and invasion by P.gingivalis. Probiotics can modulate the inflammatory response mediated by P. gingivalis in GECs IL-1β and TNF-α synthesis stimulation decreases when co-culture with P. gingivalis and L. rhamnosus or bifidocteria (B.longum, B. animalis, B. pseudolongum, B. bifidum) or L. salivarius. CXCL8 secretion increases when co-culture with P. gingivalis and L. salivarius or L. rhamnosus. * In vitro study |
Jaffar et al. (2016) [45] | In vitro | L. acidophilus JCM, L. casei subsp. rhamnosus NBRC 3831, L. delbrueckii subsp. casei JCM 1012, L. fermentum JCM 1137, L. fermentum NBRC 15885, Lactococcus lactis NBRC 12007, L. casei NBRC 15883, Leuconostoc fructosum NBRC 3516, Leuconostoc mesenteroides IAM 1046, L. plantarum NBRC 15891, L. johnsonii NBRC 13952, L. sake NBRC 3541, L. paracasei subsp. paracasei NBRC 3533 | Evaluation of the potential of probiotic bacteria as a degrading agent against the periodontal pathogen A. actinomycetemcomitans and elucidation of the mechanisms underlying the observations made. | Not relevant | Probiotic bacteria demonstrate a robust degradation activity on A. actinomycetemcomitans Y4 and OMZ 534 strain, and a moderate effect against SUNY 75 strain Lipase enzyme from probiotic strains might be an influential factor in the biofilm degradation against A. actinomycetemcomitans Y4 and OMZ 534 strains. * No measurement of biofilm viability, In vitro study |
Oliveira et al. (2017) [46] | Experimental study in rats (n = 32; 8 controls without EP, 8 EP only, 8 control + probiotic, 8 EP + probiotic group) | Bifidobacterium animalis subsp. lactis HN019 | Evaluation of effects of topical administration of probiotic bacteria of the genus Bifidobacterium on experimental periodontitis (EP) in rats | Subgingival irrigation with 1 mL of suspension containing 1.9 × 109 CFU of B. lactis HN019 on days 0, 3, and 7. | Compared with group EP, group EP-HN019 presented lower proportions of some Gram-negative anaerobic bacteria-like species involved in the pathogenesis of periodontal diseases Group EP-HN019 presented levels of IL-1b and an IL-1b/IL-10 ratio that were significantly reduced compared with group EP. * No identification of the subgingival microbiota before EP. |
Invernici et al. (2020) [47] | randomized placebo-controlled study (n = 30, 15 Scaling root planning + placebo and 15 Scaling root planning + probiotic) | Bifidobacterium animalis subsp. lactis HN019 | Evaluation of the effects of B. lactis HN019 in non-surgical periodontal therapy in generalized chronic periodontitis patients. Investigation of the oral epithelial cell adhesion and antimicrobial properties of B. lactis HN019. | Lozenge (109 CFU) intake 30 days after non-surgical periodontal therapy. | B. lactis HN019 reduced the adhesion of P. gingivalis to buccal epithelial cells. B. lactis HN019 inhibit the growth of P. gingivalis, P. intermedia, F. nucleatum and A. actinomycetemcomitans in in vitro sensitivity tests. * Sample size |
Dassi et al. (2014) [48] | placebo-controlled, parallel study (n = 12; 5 in control group, 7 in probiotic group) | Lactobacillus delbrueckii subsp. bulgaricus, Lactobacillus paracasei | Assessment of the impact on the overall saliva microbiome structure of a short-term probiotic intervention | 100 g of a commercial probiotic product containing milk fermented (1 day). | Short-term probiotic intake significantly increases the complexity of the community with Steptococcus and Actinomyces as the most involved genera. Absence of significant changes detected in the metabolic structure of probiotic versus control samples. The two Lactobacillus strains present in the probiotic product were not detected in probiotic-intake samples. * Short probiotic intake, Sample size (n = 12) |
Dassi et al. (2018) [49] | Cross sectional study (n = 21) | Lactobacillus delbrueckii subsp. bulgaricus, Lactobacillus paracasei | Verification of the hypothesis that the intake of commercially available probiotic products has a directly effect on the diversity and composition of the saliva microbiome. | 100 g of a commercial probiotic product containing milk fermented (1 day). | The intake of commercially available probiotic products has a directly effect on the diversity and composition of the saliva microbiome, at least at short timescales. The overall taxonomic and abundance distribution of bacterial genera is however minimally influenced by probiotic intake. * Study design, sample size |
Becirovic et al. (2018) [50] | Cross sectional study (n = 60) | Lactobacillus acidophilus La-5, Bifidobacterium Bb-12, Lactobacillus rhamnosus GG | Assessment of the effect of daily intake of a probiotic milk drink on the composition of bacterial species in dental supra- and subgingival biofilms. | 200 mL probiotic milk beverage each day during 3 weeks | Influence of probiotics on bacteria in subgingival plaque was less than in supragingival plaque. The probiotic has led to a decrease in bacteria Aggregatibacter actinomycetemcomitans, Actinomyces israelii, Actinomyces viscosus, Campylobacter rectus, Eikenella corrodens, Eubacterium saburreum, Fusobacterium nucleatum ssp. nucleatum, Porphyromonas endodontalis, Prevotella intermedia, Porphyromonas gingivalis, Parvimonas micra, Prevotella nigrescens, Streptococcus intermedius, Treponema denticola, Tannerella forsythia in supragingival plaque. In the subgingival plaque a decrease of Actinomyces viscosus, Fusobacterium nucleatum ssp. nucleatum, Treponema socranskii ssp. Socranskii * Study design, sample size |
Tada et al. (2018) [51] | Randomized placebo-controlled study (n = 30; 15 placebo group, 15 probiotic group) | L. reuteri DSM 17938, L. reuteri ATCC PTA 5289 | Investigation of the effects of a probiotic tablet containing Lactobacillus reuteri in peri-implantitis patients. | One tablet a day for 6 months with 1 × 108 CFU L. reuteri strains DSM 17938 and ATCC PTA 5289. | Negligible changes were observed in the bacterial flora around implants * Sample size, No evaluation of L. reuteri colonization. |
Kõll et al. (2008) [52] | In vitro | L. acidophilus, L. crispatus, L. delbrueckii, L. gasseri, L. salivarius, L. paracasei, L. plantarum, L. rhamnosus, L. fermentum, L. oris | Characterization of oral lactobacilli for their potential probiotic properties according to the international guidelines for the evaluation of probiotics. Selection of oral lactobacilli strains that could eventually be used as probiotics for oral health. | Not relevant | Several human oral lactobacilli possess good functional probiotic properties like antimicrobial activity against oral pathogens as well as high tolerance of environmental stress factors. These beneficial properties are better expressed in L. plantarum, L. paracasei, and L. rhamnosus, L. salivarius strains. The strains of L. plantarum differ from the natural resistance pattern of lactobacilli and therefore, should be considered non-safe * In vitro study |
Teanpaisan et al. (2011) [53] | In vitro | L. paracasei, L casei, L. salivarius, L. plantarum, L. rhamnosus, L. fermentum, L. gasseri, L.mucosae, L. oris, L. vaginalis | Determination of the inhibitory effect of oral Lactobacillus against putative oral pathogens. | Not relevant | L. paracasei, L. casei, L. salivarius, L. plantarum, L. rhamnosus, L. fermentum have a strong inhibitory effect against S. mutans and Streptococcus sobrinus, as well as, Gram-negative periodontal pathogens Porphyromonas gingivalis and Aggregatibacter actinomycetemcomitans. * In vitro study |
Van Essche et al. (2013) [54] | In vitro | L. rhamnosus, L. casei, L. fermentum, L. paracasei | Assessment of the antagonistic potential of oral bacteria on periodontal pathogens. Evaluation of the inhibitory effect of some commercial dietary probiotics on periodontopathogens and comparison with the inhibitory effect of orally derived beneficial bacteria. | Not relevant | The commensal oral microbiota is considered to induce a beneficial oral immune response or to interfere with periodontopathogen colonization. Probiotics showed a stronger inhibition of P. gingivalis and P. intermedia, and the oral isolated strains showed a clearly stronger inhibition of F. nucleatum and A. actinomycetemcomitans. * In vitro study |
Chen et al. (2020) [55] | In vitro | L.salivarius subsp. salicinius AP-32, L. rhamnosus CT-53, L. paracasei ET-66, Bifidobacterium animalis subsp. lactis CP-9, L. acidophilus TYCA02 | Evaluation of the antipathogenic efficacy of different probiotic species and their potential roles in developing functional foods to improve oral health | Not relevant | Lactobacillus salivarius subsp. salicinius AP-32, L. rhamnosus CT-53, L. paracasei ET-66 and B. animalis subsp. lactis CP-9 displayed strong antibacterial activity against the oral pathogens S. mutans, P. gingivalis, F. nucleatum and A. actinomycetemcomitans. * In vitro study |
Shin et al. (2018) [56] | In vitro | Lactococcus lactis HY449 | Investigation of the inhibitory effects of L. lactis on the bioactivity of periodontopathogens. | Not relevant | L. lactis has antimicrobial activity against periodontopathogens, such as F. nucleatum, P. gingivalis, T. forsythia, and T. denticola. L. lactis neutralized and inhibited inflammatory cytokines induced by lipopolysaccharides derived from these pathogens. * In vitro study |
Higuchi et al. (2019) [57] | In vitro | Lactobacillus salivarius WB21 combined with green tea catechins | Evaluation of the combined use of Lactobacillus salivarius WB21 and epigallocatechin gallate for oral health maintenance. | Not relevant | Growth of P. gingivalis was strongly inhibited by co-culture with L. salivarius WB21 combined with green tea catechins * In vitro study |
Zhu et al. (2010) [58] | In vitro | L. bulgaricus, S. thermophilus, L. acidophilus, Bifidobacterium | Investigation of the competition between probiotics and periodontal pathogens in vitro. | Not relevant | Probiotics are capable of inhibiting specific periodontal pathogens but have no effect on the periodontal protective bacteria (S. sanguinis). Competition between probiotics and periodontal pathogens depended on the sequence of inoculation. * In vitro study |
Tobita et al. (2018) [59] | Randomized double blind placebo-controlled study (n = 16; 8 control, 8 probiotic group) | L. crispatus KT-11 (KT11) | Examination of the effects of KT-11 consumption on the oral environment in healthy volunteers. | A KT-11 food tablet (1.2 × 1010 KT-11 cells) every day for 4 weeks | Daily KT-11 intake can prevent periodontal disease through the improvement of oral conditions. KT-11 makes P. gingivalis numbers decrease. * Sample size |
Iniesta et al. (2012) [60] | placebo-controlled, parallel study (n = 40; 20 control, 20 probiotic group) | L. reuteri ATCC-PTA-5289, L. reuteri DSM-17938 | Investigation of the effects of an orally administered probiotic on the oral microbiota. | one tablet per day, during 28 days One tablet per day, during 28 days with L. reuteri DSM-17938 and ATCC PTA5289 at a dose of 2 × 108CFU/tablet. | L. reuteri administered in tablets resulted in a reduction in the number of Prevotella intermedia and Porphyromonas gingivalis in the subgingival microbiota, without an associated clinical impact. L. reuteri containing probiotic tablets are able to colonize the saliva and the subgingival habitat. * Differences between groups that, although not significant, may have influenced the outcomes, short time evaluation (follow up 8 weeks) |
Teughels et al. (2017) [61] | Randomized placebo-controlled study (n = 30; 15 control, 15 probiotic group) | L. reuteri DSM17938, L. reuteri ATCC PTA-5289 | Evaluation of the effects of L. reuteri as an adjunct to scaling and root planning. | One lozenge at the morning and one at the night during 12 weeks (L. reuteri 1 × 108 CFU for each strain) | L. reuteri lozenges resulted in significant additional clinical improvements primarily for initially moderate to deep pockets when compared to SRP alone. The microbiological differences were more moderate and primarily restricted to P. gingivalis numbers. * Sample size, No evaluation of L. reuteri colonization. |
Montero et al. (2015) [62] | Randomized double blind placebo-controlled study (n = 59 patients; 29 tests, 30 placebos) | L. plantarum, L. brevis, P. acidilactici | Evaluation of the efficacy of a probiotic combination in the treatment of gingivitis Assessments of the impact of a probiotic combination on the subgingival microbiota | One lozenge at the morning and one at the night during 12 weeks (L. reuteri 1 × 103 CFU for each strain) | Use of probiotic tablets containing L. plantarum, L. brevis and P. acidilactici did not lead to significant changes in mean gingival index; although a significant reduction occurred in the number of sites with severe inflammation. The adjunctive use of the probiotic also demonstrated a significant microbiological impact by reducing the counts of T. forsythia. |
Imran et al. (2015) [63] | Cross sectional study (n = 42) | L. casei Shirota | Evaluation of the impact of Probiotic drink containing Lactobacillus casei Shirota on the bacterial population in subgingival plaque in patient with chronic generalized mild to moderate periodontitis. | 65 mL of probiotic milk (Yakult©) once daly for one month (108 CFU/mL of L. casei strain Shirota). | Oral administration of the probiotic lactobacilli reduced the numerical sum of A. actinomycetemcomitans, P. intermedia, P. gingivalis. No statistically significant changes were observed in the gingival index and plaque index scores. * Sample size |
Sarmento et al. (2019) [64] | Randomized placebo-controlled study (n = 41; 20 control group, 21 probiotic group) | L. casei | Evaluation of the effect of petit-Suisse plus probiotic on the microbiota of children’s saliva. | 50g of petit-suisse cheese daily from Monday to Friday, and the following week from Monday to Thursday (3% de L. casei) | The product with added L. casei was shown to be able to reduce A. actinomycetemcomitans, and able to maintain lower density of P. gingivalis in post treatment two weeks later. * No evaluation of probiotic change after introduction in food. |
Mayanagi et al. (2009) [65] | Randomized placebo-controlled study (n = 36; 32 control group, 34 probiotic group) | L. salivarius WB21 | Evaluation of the impact of oral administration of lactobacilli on the bacterial population in supra/subgingival plaque. | One tablet containing L. salivarius WB21 (6.7 × 108 CFU/tab) and xylitol (280 mg/tab) three times per day during 8 weeks. | L. salivarius WB21 administration successfully decreased the numerical sum of A. actinomycetemcomitans, P. intermedia, P. gingivalis, T. denticola, and T. forsythia in subgingival plaque at 4 weeks. No significant difference between the WB21 and the placebo groups in the direct count of any specific periodontopathic bacteria at 8 weeks. * Sample size |
Sajedinejad et al. (2018) [66] | Randomized placebo-controlled study (n = 50; 50 control group, 50 probiotic group) | Lactobacillus salivarius NK02 | Evaluation of the effects of probiotic mouthwash and scaling and root planning (SRP) on clinical and microbiological parameters of moderate to severe periodontitis. | Bottle of 20 mL of mouthwash was used twice a day after brushing the teeth for 28 days (108 CFU/mL of L. salivarius NK02) | Probiotic mouthwash was able to inhibit the bacterial growth on both saliva and sub-gingival crevice and exhibited antibacterial activity against A. actinomycetemcomitans. * No long term follow up |
Zahradnik et al. (2009) [67] | Cross sectional pilot study (n = 12) | S. oralis KJ3sm, S. uberis KJ2sm, S. rattus JH145 | Test the ability of a probiotic mouthwash, ProBiora3, to affect the levels of Streptococcus mutans and certain known periodontal pathogens in the mouth. | Bottle of 20 mL of mouthwash was used twice a day after brushing the teeth for 28 days (108 CFU/mL of S. oralis KJ3sm, S. uberis KJ2sm, S. rattus JH145). | The probiotic mouthwash was able to substantially affect the levels of dental pathogens in saliva (S.mutans) and periodontal pathogens in subgingival plaque (C. rectus and P.gingivalis) * Sample size, Young and orally healthy adults poupulation |
Alanzi et al. (2018) [68] | Randomized placebo-controlled study (n = 108, 54 placebo group, 54 probiotic group) | L. rhamnosus GG, B lactis BB12 | Determination of the effect of a probiotic combination on the gingival health, dental plaque accumulation, and the oral carriage of four putative periodontal pathogens in healthy adolescents | Lozenges twice a day during a four-week period (probiotic lozenge contained LGG 4.4 × 108 CFU and BB-12 4.8 × 108 CFU) | The short-term daily consumption of LGG and BB-12 probiotic lozenges improved the gingival health in adolescents The short-term daily consumption of LGG and BB-12 probiotic lozenges decreased levels of A. actinomycetemcomitans and F. nucleatum both in saliva and plaque and decreased P. gingivalis count in plaque. * Sample size, short term evaluation |
Morales et al. (2018) [69] | Randomized placebo-controlled study (n = 47, 16 SRP + probiotic, 16 SRP + antibiotic, 15 SRP + placebo) | L. rhamnosus SP1 | Evaluation of the effects of Lactobacillus rhamnosus SP1-containing probiotic sachet and azithromycin tablets as an adjunct to nonsurgical therapy in clinical parameters and in presence and levels of Tannerella forsythia, Porphyromonas gingivalis and Aggregatibacter actinomycetemcomitans. | 1 sachet in water (150 mL) ingested once a day after brushing their teeth (2 × 107 CFU/day) | All groups showed improvements in clinical and microbiological parameters at all time points evaluated. Probiotic and antibiotic groups showed greater reductions in cultivable microbiota compared with baseline. The placebo group showed greater reduction in number of subjects with P. gingivalis compared with baseline. However, there were no significant differences between groups The adjunctive use of L. rhamnosus SP1 sachets and azithromycin during initial therapy resulted in similar clinical and microbiological improvements compared with the placebo group. * Sample size |
Kobayashi et al. (2017) [70] | Experimental study in mice (n = 108; 36 tréhalose + Pg, 36 LG2055 + Pg, 36 placebo group) | L. gasseri SBT2055 | Assessment of the potential of oral administration of Lactobacillus gasseri SBT2055 (LG2055) for Porphyromonas gingivalis infection | Oral intubation with a LG2055 suspension (1 × 109 CFU/200 µL/mouse) through a syringe fitted with a ball-type feeding needle once per day for 5 weeks. | LG2055 treatment significantly reduced alveolar bone loss, detachment and disorganization of the periodontal ligament, and bacterial colonization by subsequent P. gingivalis challenge. The expression and secretion of TNF-α and IL-6 in gingival tissue was significantly decreased in LG2055-administered mice after bacterial infection. * Experimental design |
Maekawa et al. (2014) [71] | Experimental study in mice (n = 6; 3 probiotic, 3 placebo group) | L. brevis CD2 | Determination of the Lactobacillus brevis CD2 potential on inhibit periodontal inflammation and bone loss in experimental periodontitis. | Lyopatch with L. brevis CD2 (8 × 105 CFU in 1-mm2) | L. brevis CD2-treated mice exhibited significantly decreased expression of all proinflammatory cytokines tested (TNF, IL-1β, IL-6, and IL-17A). L. brevis CD2 treatment resulted in significantly higher counts of aerobic bacteria and, conversely, significantly lower numbers of anaerobic bacteria, as compared to the placebo-treated control group. * Sample size |
Keller et al. (2018) [72] | Randomized placebo-controlled study (n = 47, 23 probiotic, 24 placebo group) | L. rhamnosus PB01, L. curvatus EB10 | Investigation of the clinical and the microbial effects of probiotic candidate strains in patients with moderate gingivitis. | One tablet in the morning and one in the evening 30 min after tooth brushing containing a mix of L. rhamnosus and L. curvatus (108 CFU/tablet) | The concentration of selected cytokines (interleukin (IL 1β, IL6, IL8, IL10, tumour necrosis factor alpha (TNF-α)) in gingival crevicular fluid were unaffected by the intervention as well as the salivary microbiome. * Sample size, healthy patient |
Braathen et al. (2017) [73] | randomised, double-blind, placebo-controlled, cross-over trial (n = 47) | L. reuteri DSM 17938, L. reuteri ATCC PTA 5289 | Comparaison of the concentration of salivary immunoglobulin A (IgA) and the selected interleukins (IL)-1β, IL-6, IL-8 and IL-10 in young individuals with presence and non-presence of Lactobacillus reuteri in saliva after a three-week intervention with probiotic lozenges. | Two lozenges per day containing the probiotic bacterium L. reuteri for three weeks (L. reuteri DSM 17938 1 × 109 CFU/lozenge, ATCC PTA5289 2 × 109 CFU/lozenge) | No differences in the cytokine levels (IL1β, IL-6, IL-8 and IL-10) were observed. Individuals with presence of L. reuteri in saliva had significantly higher concentrations of salivary IgA * Sample size, healthy patient |
Jørgensen et al. (2016) [74] | randomised, double-blind, placebo-controlled, cross-over trial (n = 47) | L. reuteri DSM 17938, L. reuteri ATCC PTA 5289 | Evaluation of the effect of daily ingestion of probiotic lactobacilli on the levels of secretory IgA (sIgA) and selected cytokines in whole saliva of healthy young adults. | Two lozenges per day containing L. reuteri DSM 17938, L. reuteri ATCC PTA 5289 L. reuteri DSM 17938, L. reuteri ATCC PTA 5289 | No significant differences in the concentrations of salivary sIgA or cytokines were recorded between the L. reuteri and placebo interventions or between baseline and 3 weeks post-intervention levels. * Sample size, healthy patient |
Hallström et al. (2016) [75] | Randomized placebo-controlled study. (n = 46; 22 probiotic, 24 placebo group) | L. reuteri DSM 17938, L. reuteri ATCC PTA 5289 | Evaluation of the effects of probiotic supplements in adjunct to conventional management of peri-implant mucositis | Topical oil application (2 × 107 CFU of each strain) followed by twice-daily intake of lozenges for 3 months (1 × 108 CFU of each strain) | Topical treatment and daily intake of probiotic lozenges as an adjunct to mechanical debridement and oral hygiene instructions did not improve clinical, microbial or inflammatory variables of peri implant mucositis as compared to the use of placebo. * Sample size |
Lactobacilli | Bifidobacterium | Streptococci | Others * |
---|---|---|---|
L. rhamnosus | B. animalis | S. thermophilus | L. lactis |
L. reuteri | B. longum | S. uberis | P. acidilactici |
L. salivarius | B. pseudolongum | S. rattus | |
L. caseï | S. oralis | ||
L. paracaseï | |||
L. delbruekii | |||
L. acidophilus | |||
L. plantarum | |||
L. fermentum | |||
L. gasseri | |||
L. crispatus | |||
L. brevis | |||
L. curvatus |
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Maitre, Y.; Mahalli, R.; Micheneau, P.; Delpierre, A.; Guerin, M.; Amador, G.; Denis, F. Pre and Probiotics Involved in the Modulation of Oral Bacterial Species: New Therapeutic Leads in Mental Disorders? Microorganisms 2021, 9, 1450. https://doi.org/10.3390/microorganisms9071450
Maitre Y, Mahalli R, Micheneau P, Delpierre A, Guerin M, Amador G, Denis F. Pre and Probiotics Involved in the Modulation of Oral Bacterial Species: New Therapeutic Leads in Mental Disorders? Microorganisms. 2021; 9(7):1450. https://doi.org/10.3390/microorganisms9071450
Chicago/Turabian StyleMaitre, Yoann, Rachid Mahalli, Pierre Micheneau, Alexis Delpierre, Marie Guerin, Gilles Amador, and Frédéric Denis. 2021. "Pre and Probiotics Involved in the Modulation of Oral Bacterial Species: New Therapeutic Leads in Mental Disorders?" Microorganisms 9, no. 7: 1450. https://doi.org/10.3390/microorganisms9071450