Probiotics-Mediated Bioconversion and Periodontitis

Yewon Lee, Yohan Yoon, Kyoung-Hee Choi, Yewon Lee, Yohan Yoon, Kyoung-Hee Choi

Abstract

Novel bioactive metabolites have been developed through a bioconversion of dairy products or other foods using probiotics isolated from dairy products or other fermented foods. These probiotics-mediated bioconversion (PMB) metabolites show antioxidant, anti-inflammatory, antimicrobial, epithelial barrier, and anticancer activities. In addition, the effect of PMB metabolites in periodontitis is recently reported in several studies. Periodontitis is a chronic inflammatory disease caused by infections, and the tooth support tissue is destroyed. Common treatments for periodontitis include scaling and root planning with systemic antibiotics. However, the overuse of antibiotics has led to the emergence of drug-resistant microorganisms and disturbs the beneficial bacteria, including lactobacilli in the oral cavity. For this reason, PMB metabolites, such as fermented milk, have been suggested as substitutes for antibiotics to reduce periodontitis. This paper reviews the recent studies on the correlation between periodontitis and PMB metabolites and classifies the efficacy of major PMB metabolites for periodontitis. The review suggests that PMB is effective for periodontitis, and further studies are needed to confirm the therapeutic effect of PMB metabolites on periodontitis.

Keywords: bioconversion; periodontitis; probiotics; probiotics-mediated bioconversion.

Conflict of interest statement

The authors declare no potential conflicts of interest.

© Korean Society for Food Science of Animal Resources.

Figures

Fig. 1.. Mechanism and function of probiotics-mediated…
Fig. 1.. Mechanism and function of probiotics-mediated bioconversion.

References

    1. Aarnikunnas J, Von Weymarn N, Rönnholm K, Leisola M, Palva A. Metabolic engineering of Lactobacillus fermentum for production of mannitol and pure L-lactic acid or pyruvate. Biotechnol Bioeng. 2003;82:653–663. doi: 10.1002/bit.10615.
    1. Aas JA, Paster BJ, Stokes LN, Olsen I, Dewhirst FE. Defining the normal bacterial flora of the oral cavity. J Clin Microbiol. 2005;43:5721–5732. doi: 10.1128/JCM.43.11.5721-5732.2005.
    1. Ahn J, Chen CY, Hayes RB. Oral microbiome and oral and gastrointestinal cancer risk. Cancer Causes Control. 2012;23:399–404. doi: 10.1007/s10552-011-9892-7.
    1. Armitage GC. Clinical evaluation of periodontal diseases. Periodontol 2000. 1995;7:39–53. doi: 10.1111/j.1600-0757.1995.tb00035.x.
    1. Aura AM. Microbial metabolism of dietary phenolic compounds in the colon. Phytochem Rev. 2008;7:407–429. doi: 10.1007/s11101-008-9095-3.
    1. Baca-Castañón ML, De la Garza-Ramos MA, Alcázar-Pizaña AG, Grondin Y, Coronado-Mendoza A, Sánchez-Najera RI, Cárdenas-Estrada E, Medina-De la Garza CE, Escamilla-García E. Antimicrobial effect of Lactobacillus reuteri on cariogenic bacteria Streptococcus gordonii, Streptococcus mutans, and periodontal diseases Actinomyces naeslundii and Tannerella forsythia. Probiotics Antimicrob. 2015;7:1–8. doi: 10.1007/s12602-014-9178-y.
    1. Bae EA, Kim NY, Han MJ, Choo MK, Kim DH. Transformation of ginsenosides to compound K (IH-901) by lactic acid bacteria of human intestine. J Microbiol Biotechnol. 2003;13:9–14.
    1. Berezina OV, Zakharova NV, Brandt A, Yarotsky SV, Schwarz WH, Zverlov VV. Reconstructing the clostridial n-butanol metabolic pathway in Lactobacillus brevis. Appl Microbiol Biotechnol. 2010;87:635–646. doi: 10.1007/s00253-010-2480-z.
    1. Berg G, Rybakova D, Fischer D, Cernava T, Vergès MCC, Charles T, Chen X, Cocolin L, Eversole K, Corral GH, Kazou M, Kinkel L, Lange L, Lima N, Loy A, Macklin JA, Maguin E, Mauchline T, McClure R, Mitter B, Ryan M, Sarand I, Smidt H, Schelkle B, Roume H, Kiran GS, Selvin J, de Souza RSC, van Overbeek L, Singh BK, Wagner M, Walsh A, Sessitsch A, Schloter M. Microbiome definition re-visited: Old concepts and new challenges. Microbiome. 2020;8:103. doi: 10.1186/s40168-020-00875-0.
    1. Borgnakke WS, Ylöstalo PV, Taylor GW, Genco RJ. Effect of periodontal disease on diabetes: Systematic review of epidemiologic observational evidence. J Periodontol. 2013;84:S135–S152. doi: 10.1902/jop.2013.1340013.
    1. Brooke MA, Nitoiu D, Kelsell DP. Cell-cell connectivity: Desmosomes and disease. J Pathol. 2012;226:158–171. doi: 10.1002/path.3027.
    1. Choi Y, Park E, Kim S, Ha J, Oh H, Kim Y, Lee Y, Seo Y, Kang J, Lee S, Lee H, Yoon Y, Choi KH. Fermented milk with Lactobacillus curvatus SMFM2016-NK alleviates periodontal and gut inflammation, and alters oral and gut microbiota. J Dairy Sci. 2021;104:5197–5207. doi: 10.3168/jds.2020-19625.
    1. Claffey N, Polyzois I, Ziaka P. An overview of nonsurgical and surgical therapy. Periodontol 2000. 2004;36:35–44. doi: 10.1111/j.1600-0757.2004.00073.x.
    1. Córdova-Dávalos LE, Jiménez M, Salinas E. Glycomacropeptide bioactivity and health: A review highlighting action mechanisms and signaling pathways. Nutrients. 2019;11:598. doi: 10.3390/nu11030598.
    1. Curiel JA, Rodríguez H, Acebrón I, Mancheño JM, De Las Rivas B, Muñoz R. Production and physicochemical properties of recombinant Lactobacillus plantarum tannase. J Agric Food Chem. 2009;57:6224–6230. doi: 10.1021/jf901045s.
    1. D’Aiuto F, Gkranias N, Bhowruth D, Khan T, Orlandi M, Suvan J, Masi S, Tsakos G, Hurel S, Hingorani AD, Donos N, Deanfield JE. For the TASTE Group. 2018. Systemic effects of periodontitis treatment in patients with type 2 diabetes: A 12 month, single-centre, investigator-masked, randomised trial. Lancet Diabetes Endocrinol. 6:954–965. doi: 10.1016/S2213-8587(18)30038-X.
    1. Danser MM, Gómez SM, Van der Weijden GA. Tongue coating and tongue brushing: A literature review. Int J Dent Hyg. 2003;1:151–158. doi: 10.1034/j.1601-5037.2003.00034.x.
    1. Dewhirst FE, Chen T, Izard J, Paster BJ, Tanner ACR, Yu WH, Lakshmanan A, Wade WG. The human oral microbiome. J Bacteriol. 2010;192:5002–5017. doi: 10.1128/JB.00542-10.
    1. Di Cagno R, Mazzacane F, Rizzello CG, Vincentini O, Silano M, Giuliani G, De Angelis M, Gobbetti M. Synthesis of isoflavone aglycones and equol in soy milks fermented by food-related lactic acid bacteria and their effect on human intestinal Caco-2 cells. J Agric Food Chem. 2010;58:10338–10346. doi: 10.1021/jf101513r.
    1. Diamond G, Beckloff N, Weinberg A, Kisich KO. The roles of antimicrobial peptides in innate host defense. Curr Pharm Des. 2009;15:2377–2392. doi: 10.2174/138161209788682325.
    1. Di Rienzo JM. Breaking the gingival epithelial barrier: Role of the Aggregatibacter actinomycetemcomitans cytolethal distending toxin in oral infectious disease. Cells. 2014;3:476–499. doi: 10.3390/cells3020476.
    1. Doh ES, Chang JP, Lee KH, Seong NS. Ginsenoside change and antioxidation activity of fermented ginseng. Korean J Med Crop Sci. 2010;18:255–265.
    1. Ebringer L, Ferenčík M, Krajčovič J. Beneficial health effects of milk and fermented dairy products: Review. Folia Microbiol. 2008;53:378–394. doi: 10.1007/s12223-008-0059-1.
    1. Elfahri K. Release of bioactive peptides from milk proteins by Lactobacillus species. Victoria Univ.; Melbourne, Australia: 2012. M.S. thesis.
    1. Ewe JA, Wan-Abdullah WN, Alias AK, Liong MT. Effects of ultrasound on growth, bioconversion of isoflavones and probiotic properties of parent and subsequent passages of Lactobacillus fermentum BT 8633 in biotin-supplemented soymilk. Ultrason Sonochem. 2012;19:890–900. doi: 10.1016/j.ultsonch.2012.01.003.
    1. Fernandez MA, Picard-Deland É, Le Barz M, Daniel N, Marette A. In: In Fermented foods in health and disease prevention. 1st ed. Frias J, Martinez-Villaluenga C, Peñas E, editors. Elsevier Science & Technology Books; Québec, QU, Canada: 2017. Yogurt and health; pp. 305–338. (ed)
    1. Gibson GR, Hutkins R, Sanders ME, Prescott SL, Reimer RA, Salminen SJ, Scott K, Stanton C, Swanson KS, Cani PD, Verbeke K, Reid G. 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. doi: 10.1038/nrgastro.2017.75.
    1. Gobbetti M, Minervini F, Rizzello CG. Angiotensin I-converting-enzyme-inhibitory and antimicrobial bioactive peptides. Int J Dairy Technol. 2004;57:173–188. doi: 10.1111/j.1471-0307.2004.00139.x.
    1. Gonzalez-Gonzalez CR, Tuohy KM, Jauregi P. Production of angiotensin-I-converting enzyme (ACE) inhibitory activity in milk fermented with probiotic strains: Effects of calcium, pH and peptides on the ACE-inhibitory activity. Int Dairy J. 2011;21:615–622. doi: 10.1016/j.idairyj.2011.04.001.
    1. Goodson JM, Haffajee AD, Socransky SS, Kent R, Teles R, Hasturk H, Bogren A, Van Dyke T, Wennstrom J, Lindhe J. Control of periodontal infections: A randomized controlled trial I. The primary outcome attachment gain and pocket depth reduction at treated sites. J Clin Periodontol. 2012;39:526–536. doi: 10.1111/j.1600-051X.2012.01870.x.
    1. Grandits M, Michlmayr H, Sygmund C, Oostenbrink C. Calculation of substrate binding affinities for a bacterial GH78 rhamnosidase through molecular dynamics simulations. J Mol Catal B Enzym. 2013;92:34–43. doi: 10.1016/j.molcatb.2013.03.012.
    1. Grudianov AI, Dmitrieva NA, Fomenko EV. Use of probiotics bifidumbacterin and acilact in tablets in therapy of periodontal inflammations. Stomatologiia. 2002;81:39–43.
    1. Grusovin MG, Bossini S, Calza S, Cappa V, Garzetti G, Scotti E, Gherlone EF, Mensi M. 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. Clin Oral Invest. 2020;24:2015–2024. doi: 10.1007/s00784-019-03065-x.
    1. Gupta G. Probiotics and periodontal health. J Med Life. 2011;4:387–394. doi: 10.5005/johcd-4-Spl-35.
    1. Haiwen Z, Rui H, Bingxi Z, Qingfeng G, Jifeng Z, Xuemei W, Beibei W. Oral administration of bovine lactoferrin-derived lactoferricin (Lfcin) B could attenuate enterohemorrhagic Escherichia coli O157:H7 induced intestinal disease through improving intestinal barrier function and microbiota. J Agric Food Chem. 2019;67:3932–3945. doi: 10.1021/acs.jafc.9b00861.
    1. Han HS, Park WS, Lee YJ. Studies on the immunomodulating acitivity of fermented Artemisiae argyi folium extract. Korean J Herbol. 2008;23:103–112.
    1. Heeney DD, Zhai Z, Bendiks Z, Barouei J, Martinic A, Slupsky C, Marco ML. Lactobacillus plantarum bacteriocin is associated with intestinal and systemic improvements in diet-induced obese mice and maintains epithelial barrier integrity in vitro. Gut Microbes. 2019;10:382–397. doi: 10.1080/19490976.2018.1534513.
    1. Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, Morelli L, Berni Canani R, Flint HJ, Salminen S, Calder PC, Sanders ME. Expert consensus document: The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol. 2014;11:506–514. doi: 10.1038/nrgastro.2014.66.
    1. Houle MA, Grenier D. Periodontal diseases: Current knowledge: Current concepts in periodontal diseases. Med Mal Infect. 2003;33:331–340.
    1. How YH, Ewe JA, Song KP, Kuan CH, Kuan CS, Yeo SK. Soy fermentation by indigenous oral probiotic Streptococcus spp. and its antimicrobial activity against oral pathogens. Int Food Res J. 2020;27:357–365.
    1. Hyun DH, Lee M, Hattori N, Kubo SI, Mizuno Y, Halliwell B, Jenner P. Effect of wild-type or mutant Parkin on oxidative damage, nitric oxide, antioxidant defenses, and the proteasome. J Biol Chem. 2002;277:28572–28577. doi: 10.1074/jbc.M200666200.
    1. İnce G, Gürsoy H, İpçi SD, 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;86:746–754. doi: 10.1902/jop.2015.140612.
    1. Invernici MM, Salvador SL, Silva PHF, Soares MSM, Casarin R, Palioto DB, Souza SLS, Taba M, Jr, Novaes AB, Furlaneto FAC, Messora MR. Effects of Bifidobacterium probiotic on the treatment of chronic periodontitis: A randomized clinical trial. J Clin Periodontol. 2018;45:1198–1210. doi: 10.1111/jcpe.12995.
    1. Ishikawa H, Aiba Y, Nakanishi M, Oh-hashi Y, Koga Y. Suppression of periodontal pathogenic bacteria in the saliva of humans by the administration of Lactobacillus salivarius TI 2711. J Jpn Soc Periodontol. 2003;45:105–112. doi: 10.2329/perio.45.105.
    1. Jakesevic M, Aaby K, Borge GIA, Jeppsson B, Ahrné S, Molin G. Antioxidative protection of dietary bilberry, chokeberry and Lactobacillus plantarum HEAL19 in mice subjected to intestinal oxidative stress by ischemia-reperfusion. BMC Complement Altern Med. 2011;11:8. doi: 10.1186/1472-6882-11-8.
    1. John RP, Nampoothiri KM, Pandey A. Fermentative production of lactic acid from biomass: An overview on process developments and future perspectives. Appl Microbiol Biotechnol. 2007;74:524–534. doi: 10.1007/s00253-006-0779-6.
    1. Jung J, Jang HJ, Eom SJ, Choi NS, Lee NK, Paik HD. Fermentation of red ginseng extract by the probiotic Lactobacillus plantarum KCCM 11613P: Ginsenoside conversion and antioxidant effects. J Ginseng Res. 2019;43:20–26. doi: 10.1016/j.jgr.2017.07.004.
    1. Kamer AR, Dasanayake AP, Craig RG, Glodzik-Sobanska L, de Bry M, Leon MJ. Alzheimer’s disease and peripheral infections: The possible contribution from periodontal infections, model and hypothesis. J Alzheimers Dis. 2008;13:437–449. doi: 10.3233/JAD-2008-13408.
    1. Kapoor A, Malhotra R, Grover V, Grover D. Systemic antibiotic therapy in periodontics. Dent Res J. 2012;9:505–515. doi: 10.4103/1735-3327.104866.
    1. Kaur S, White S, Bartold PM. Periodontal disease and rheumatoid arthritis: A systematic review. J Dent Res. 2013;92:399–408. doi: 10.1177/0022034513483142.
    1. Kaźmierczyk-Winciorek M, Nędzi-Góra M, Słotwińska SM. The immunomodulating role of probiotics in the prevention and treatment of oral diseases. Cent Eur J Immunol. 2021;46:99–104. doi: 10.5114/ceji.2021.104412.
    1. Ketudat Cairns JR, Esen A. β-Glucosidases. Cell Mol Life Sci. 2010;67:3389–3405. doi: 10.1007/s00018-010-0399-2.
    1. Kishino S, Takeuchi M, Park SB, Hirata A, Kitamura N, Kunisawa J, Kiyono H, Iwamoto R, Isobe Y, Arita M, Arai H, Ueda K, Shima J, Takahashi S, Yokozeki K, Shimizu S, Ogawa J. Polyunsaturated fatty acid saturation by gut lactic acid bacteria affecting host lipid composition. Proc Natl Acad Sci USA. 2013;110:17808–17813. doi: 10.1073/pnas.1312937110.
    1. Kolenbrander PE, Andersen RN, Blehert DS, Egland PG, Foster JS, Palmer RJ., Jr Communication among oral bacteria. Microbiol Mol Biol Rev. 2002;66:486–505. doi: 10.1128/MMBR.66.3.486-505.2002.
    1. Kõll-Klais P, Mändar R, Leibur E, Marcotte H, Hammarström L, Mikelsaar M. Oral lactobacilli in chronic periodontitis and periodontal health: Species composition and antimicrobial activity. Oral Microbiol Immunol. 2005;20:354–361. doi: 10.1111/j.1399-302X.2005.00239.x.
    1. Kumar PS, Griffen AL, Barton JA, Paster BJ, Moeschberger ML, Leys EJ. New bacterial species associated with chronic periodontitis. J Dent Res. 2003;82:338–344. doi: 10.1177/154405910308200503.
    1. Laleman I, Pauwels M, Quirynen M, Teughels W. A dual-strain Lactobacilli reuteri probiotic improves the treatment of residual pockets: A randomized controlled clinical trial. J Clin Periodontol. 2020;47:43–53. doi: 10.1111/jcpe.13198.
    1. Lee G, Kim HJ, Kim HM. RhoA-JNK regulates the E-cadherin junctions of human gingival epithelial cells. J Dent Res. 2016a;95:284–291. doi: 10.1177/0022034515619375.
    1. Lee J, Kim M, Kim D, Yu C, Kim BS, Lee JS, Kang SS. Anti-biofilm effect of bioconversion of whey by lactic acid bacteria against foodborne pathogenic bacteria. Curr Top Lactic Acid Bacteria Probiotics. 2020;6:25–31. doi: 10.35732/ctlabp.2020.6.1.25.
    1. Lee M, Hong GE, Zhang H, Yang CY, Han KH, Mandal PK, Lee CH. Production of the isoflavone aglycone and antioxidant activities in black soymilk using fermentation with Streptococcus thermophilus S10. Food Sci Biotechnol. 2015;24:537–544. doi: 10.1007/s10068-015-0070-7.
    1. Lee NK, Jeewanthi RKC, Park EH, Paik HD. Short communication: Physicochemical and antioxidant properties of Cheddar-type cheese fortified with Inula britannica extract. J Dairy Sci. 2016b;99:83–88. doi: 10.3168/jds.2015-9935.
    1. Lee NK, Paik HD. Bioconversion using lactic acid bacteria: Ginsenosides, GABA, and phenolic compounds. J Microbiol Biotechnol. 2017;27:869–877. doi: 10.4014/jmb.1612.12005.
    1. Li S, Chen L, Yang T, Wu Q, Lv Z, Xie B, Sun Z. Increasing antioxidant activity of procyanidin extracts from the pericarp of Litchi chinensis processing waste by two probiotic bacteria bioconversions. J Agric Food Chem. 2013;61:2506–2512. doi: 10.1021/jf305213e.
    1. Listgarten MA. Nature of periodontal diseases: Pathogenic mechanisms. J Periodontal Res. 1987;22:172–178. doi: 10.1111/j.1600-0765.1987.tb01560.x.
    1. Liu TH, Tsai TY, Pan TM. Effects of an ethanol extract from Lactobacillus paracasei subsp. paracasei NTU 101 fermented skimmed milk on lipopolysaccharide-induced periodontal inflammation in rats. Food Funct. 2018b;9:4916–4925. doi: 10.1039/C8FO01303A.
    1. Liu Y, Hui X, Ibrahim SA, Huang W. Increasing antiradical activity of polyphenols from lotus seed epicarp by probiotic bacteria bioconversion. Molecules. 2018a;23:2667. doi: 10.3390/molecules23102667.
    1. Malkoski M, Dashper SG, O’Brien-Simpson NM, Talbo GH, Macris M, Cross KJ, Reynolds EC. Kappacin, a novel antibacterial peptide from bovine milk. Antimicrob Agents Chemother. 2001;45:2309–2315. doi: 10.1128/AAC.45.8.2309-2315.2001.
    1. Masdea L, Kulik EM, Hauser-Gerspach I, Ramseier AM, Filippi A, Waltimo T. Antimicrobial activity of Streptococcus salivarius K12 on bacteria involved in oral malodour. Arch Oral Biol. 2012;57:1041–1047. doi: 10.1016/j.archoralbio.2012.02.011.
    1. Miyamoto J, Mizukure T, Park SB, Kishino S, Kimura I, Hirano K, Bergamo P, Rossi M, Suzuki T, Arita M, Ogawa J, Tanabe S. A gut microbial metabolite of linoleic acid, 10-hydroxy-cis-12-octadecenoic acid, ameliorates intestinal epithelial barrier impairment partially via GPR40-MEK-ERK pathway. J Biol Chem. 2015;290:2902–2918. doi: 10.1074/jbc.M114.610733.
    1. Moreno-Fernandez J, Diaz-Castro J, Alférez MJM, Boesch C, Nestares T, López-Aliaga I. Fermented goat milk improves antioxidant status and protects from oxidative damage to biomolecules during anemia recovery. J Sci Food Agric. 2017;97:1433–1442. doi: 10.1002/jsfa.7882.
    1. Nejati F, Rizzello CG, Di Cagno R, Sheikh-Zeinoddin M, Diviccaro A, Minervini F, Gobbetti M. Manufacture of a functional fermented milk enriched of angiotensin-I converting enzyme (ACE)-inhibitory peptides and γ-amino butyric acid (GABA) LWT-Food Sci Technol. 2013;51:183–189. doi: 10.1016/j.lwt.2012.09.017.
    1. Novakovic N, Todorovic T, Rakic M, Milinkovic I, Dozic I, Jankovic S, Aleksic Z, Cakic S. Salivary antioxidants as periodontal biomarkers in evaluation of tissue status and treatment outcome. J Periodont Res. 2014;49:129–136. doi: 10.1111/jre.12088.
    1. Oda Y, Furutani C, Mizota Y, Wakita A, Mimura S, Kihara T, Ohara M, Okada A, Okada M, Nikawa H. Effect of bovine milk fermented with Lactobacillus rhamnosus L8020 on periodontal disease in individuals with intellectual disability: A randomized clinical trial. J Appl Oral Sci. 2019;27:e20180564. doi: 10.1590/1678-7757-2018-0564.
    1. Omar SH. Oleuropein in olive and its pharmacological effects. Sci Pharm. 2010;78:133–154. doi: 10.3797/scipharm.0912-18.
    1. Ostaff MJ, Stange EF, Wehkamp J. Antimicrobial peptides and gut microbiota in homeostasis and pathology. EMBO Mol Med. 2013;5:1465–1483. doi: 10.1002/emmm.201201773.
    1. Page RC. Gingivitis. J Clin Periodontol. 1986;13:345–355. doi: 10.1111/j.1600-051X.1986.tb01471.x.
    1. Park H, Kim HS, Eom SJ, Kim KT, Paik HD. Antioxidative and anticanceric activities of Magnolia (Magnolia denudata) flower petal extract fermented by Pediococcus acidilactici KCCM 11614. Molecules. 2015;20:12154–12165. doi: 10.3390/molecules200712154.
    1. Pelekos G, Acharya A, Eiji N, Hong G, Leung WK, McGrath C. Effects of adjunctive probiotic L. reuteri lozenges on S/RSD outcomes at molar sites with deep pockets. J Clin Periodontol. 2020;47:1098–1107. doi: 10.1111/jcpe.13329.
    1. Perkins C, Siddiqui S, Puri M, Demain AL. Biotechnological applications of microbial bioconversions. Crit Rev Biotechnol. 2016;36:1050–1065. doi: 10.3109/07388551.2015.1083943.
    1. Pervaiz I, Ahmad S, Madni MA, Ahmad H, Khaliq FH. Microbial biotransformation: A tool for drug designing. Appl Biochem Microbiol. 2013;49:435–449. doi: 10.1134/S0003683813050098.
    1. Quan LH, Piao JY, Min JW, Yang DU, Lee HN, Yang DC. Bioconversion of ginsenoside rb1 into compound k by Leuconostoc citreum LH1 isolated from kimchi. Braz J Microbiol. 2011;42:1227–1237. doi: 10.1590/S1517-83822011000300049.
    1. Rice-Evans C, Miller N, Paganga G. Antioxidant properties of phenolic compounds. Trends Plant Sci. 1997;2:152–159. doi: 10.1016/S1360-1385(97)01018-2.
    1. Riep B, Edesi-Neuss L, Claessen F, Skarabis H, Ehmke B, Flemmig TF, Bernimoulin JP, Göbel UB, Moter A. Are putative periodontal pathogens reliable diagnostic markers? J Clin Microbiol. 2009;47:1705–1711. doi: 10.1128/JCM.01387-08.
    1. Rodríguez H, Curiel JA, Landete JM, de las Rivas B, de Felipe FL, Gómez-Cordovés C, Mancheño JM, Muñoz R. Food phenolics and lactic acid bacteria. Int J Food Microbiol. 2009;132:79–90. doi: 10.1016/j.ijfoodmicro.2009.03.025.
    1. Rodríguez H, Landete JM, de las Rivas B, Muñoz R. Metabolism of food phenolic acids by Lactobacillus plantarum CECT 748T. Food Chem. 2008;107:1393–1398. doi: 10.1016/j.foodchem.2007.09.067.
    1. Rupasinghe HPV, Parmar I, Neir SV. Biotransformation of cranberry proanthocyanidins to probiotic metabolites by Lactobacillus rhamnosus enhances their anticancer activity in HepG2 cells in vitro. Oxid Med Cell Longev. 2019;2019:4750795. doi: 10.1155/2019/4750795.
    1. Sanz M, Beighton D, Curtis MA, Cury JA, Dige I, Dommisch H, Ellwood R, Giacaman RA, Herrera D, Herzberg MC, Könönen E, Marsh PD, Meyle J, Mira A, Molina A, Mombelli A, Quirynen M, Reynolds MC, Shapira L, Zaura E. Role of microbial biofilms in the maintenance of oral health and in the development of dental caries and periodontal diseases. Consensus report of group 1 of the joint EFP/ORCA workshop on the boundaries between caries and periodontal disease. J Clin Periodontol. 2017;44:S5–S11. doi: 10.1111/jcpe.12682.
    1. Sanz M, Ceriello A, Buysschaert M, Chapple I, Demmer RT, Graziani F, Herrera D, Jepsen S, Lione L, Madianos P, Mathur M, Montanya E, Shapira L, Tonetti M, Vegh D. Scientific evidence on the links between periodontal diseases and diabetes: Consensus report and guidelines of the joint workshop on periodontal diseases and diabetes by the International Diabetes Federation and the European Federation of Periodontology. J Clin Periodontol. 2018;45:138–149. doi: 10.1111/jcpe.12808.
    1. Scannapieco FA. The oral microbiome: Its role in health and in oral and systemic infections. Clin Microbiol Newsl. 2013;35:163–169. doi: 10.1016/j.clinmicnews.2013.09.003.
    1. Schlagenhauf U, Rehder J, Gelbrich G, Jockel-Schneider Y. Consumption of Lactobacillus reuteri-containing lozenges improves periodontal health in navy sailors at sea: A randomized controlled trial. J Periodontol. 2020;91:1328–1338. doi: 10.1002/JPER.19-0393.
    1. Selma MV, Espín JC, Tomás-Barberán FA. Interaction between phenolics and gut microbiota: Role in human health. J Agric Food Chem. 2009;57:6485–6501. doi: 10.1021/jf902107d.
    1. Shin YW, Bae EA, Lee BM, Min SW, Baek NI, Ryu SN, Chung HG, Kim DH. Effect of fermented lactic acid bacteria on antiallergic effect of Artemisia princeps pampanini. J Microbiol Biotechnol. 2006;16:1464–1467.
    1. Sibel Akalın A. Dairy-derived antimicrobial peptides: Action mechanisms, pharmaceutical uses and production proposals. Trends Food Sci Technol. 2014;36:79–95. doi: 10.1016/j.tifs.2014.01.002.
    1. Socransky SS, Haffajee AD, Cugini MA, Smith C, Kent RL., Jr Microbial complexes in subgingival plaque. J Clin Periodontol. 1998;25:134–144. doi: 10.1111/j.1600-051X.1998.tb02419.x.
    1. Solieri L, Rutella GS, Tagliazucchi D. Impact of non-starter lactobacilli on release of peptides with angiotensin-converting enzyme inhibitory and antioxidant activities during bovine milk fermentation. Food Microbiol. 2015;51:108–116. doi: 10.1016/j.fm.2015.05.012.
    1. Son HU, Lee S, Heo JC, Lee SH. The solid-state fermentation of Artemisia capillaris leaves with Ganoderma lucidum enhances the anti-inflammatory effects in a model of atopic dermatitis. Int J Mol Med. 2017;39:1233–1241. doi: 10.3892/ijmm.2017.2945.
    1. Spano G, Rinaldi A, Ugliano M, Moio L, Beneduce L, Massa S. A β-glucosidase producing gene isolated from wine Lactobacillus plantarum is regulated by abiotic stresses. J Appl Microbiol. 2005;98:855–861. doi: 10.1111/j.1365-2672.2004.02521.x.
    1. Stagos D, Amoutzias GD, Matakos A, Spyrou A, Tsatsakis AM, Kouretas D. Chemoprevention of liver cancer by plant polyphenols. Food Chem Toxicol. 2012;50:2155–2170. doi: 10.1016/j.fct.2012.04.002.
    1. Sulijaya B, Masulili SLC, Lessang R, Soeroso Y, Auerkari EI. The human beta-defensin-1 level from smokers with chronic periodontitis. Asian J Pharm Clin Res. 2016;9:174–176.
    1. Sulijaya B, Takahashi N, Yamada M, Yokoji M, Sato K, Aoki-Nonaka Y, Nakajima T, Kishino S, Ogawa J, Yamazaki K. The anti-inflammatory effect of 10-oxo-trans-11-octadecenoic acid (KetoC) on RAW 264.7 cells stimulated with Porphyromonas gingivalis lipopolysaccharide. J Periodontal Res. 2018;53:777–784. doi: 10.1111/jre.12564.
    1. Sulijaya B, Yamada-Hara M, Yokoji-Takeuchi M, Matsuda-Matsukawa Y, Yamazaki K, Matsugishi A, Tsuzuno T, Sato K, Aoki-Nonaka Y, Takahashi N, Kishino S, Ogawa J, Tabeta K, Yamazaki K. Antimicrobial function of the polyunsaturated fatty acid KetoC in an experimental model of periodontitis. J Periodontol. 2019;90:1470–1480. doi: 10.1002/JPER.19-0130.
    1. Suthanthangjai W, Kilmartin PA, Phillips ARJ, Davies K, Ansell J. Bioconversion of Pinot noir anthocyanins into bioactive phenolic compounds by lactic acid bacteria. Nutr Aging. 2014;2:145–149. doi: 10.3233/NUA-130021.
    1. Tabasco R, Sánchez-Patán F, Monagas M, Bartolomé B, Moreno-Arribas MV, Peláez C, Requena T. Effect of grape polyphenols on lactic acid bacteria and bifidobacteria growth: Resistance and metabolism. Food Microbiol. 2011;28:1345–1352. doi: 10.1016/j.fm.2011.06.005.
    1. Takahashi N. Microbial ecosystem in the oral cavity: Metabolic diversity in an ecological niche and its relationship with oral diseases. Int Congr Ser. 2005;1284:103–112. doi: 10.1016/j.ics.2005.06.071.
    1. Takahashi N, Sulijaya B, Yamada-Hara M, Tsuzuno T, Tabeta K, Yamazaki K. Gingival epithelial barrier: Regulation by beneficial and harmful microbes. Tissue Barriers. 2019;7:e1651158. doi: 10.1080/21688370.2019.1651158.
    1. Teeuw WJ, Slot DE, Susanto H, Gerdes VEA, Abbas F, D’Aiuto F, Kastelein JJP, Loos BG. Treatment of periodontitis improves the atherosclerotic profile: A systematic review and meta-analysis. J Clin Periodontol. 2014;41:70–79. doi: 10.1111/jcpe.12171.
    1. Tekce M, Ince G, Gursoy H, Dirikan Ipci S, Cakar G, Kadir T, Yılmaz S. Clinical and microbiological effects of probiotic lozenges in the treatment of chronic periodontitis: A 1-year follow-up study. J Clin Periodontol. 2015;42:363–372. doi: 10.1111/jcpe.12387.
    1. Tellez A, Corredig M, Brovko LY, Griffiths MW. Characterization of immune-active peptides obtained from milk fermented by Lactobacillus helveticus. J Dairy Res. 2010;77:129–136. doi: 10.1017/S002202990999046X.
    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;40:1025–1035. doi: 10.1111/jcpe.12155.
    1. Teughels W, Van Essche M, Sliepen I, Quirynen M. Probiotics and oral healthcare. Periodontol 2000. 2008;48:111–147. doi: 10.1111/j.1600-0757.2008.00254.x.
    1. Thilakarathna WW, Langille MG, Rupasinghe HPV. Polyphenol-based prebiotics and synbiotics: Potential for cancer chemoprevention. Curr Opin Food Sci. 2018;20:51–57. doi: 10.1016/j.cofs.2018.02.011.
    1. Tomasi C, Leyland AH, Wennström JL. Factors influencing the outcome of non-surgical periodontal treatment: A multilevel approach. J Clin Periodontol. 2007;34:682–690. doi: 10.1111/j.1600-051X.2007.01111.x.
    1. Tonetti MS, Van Dyke TE. Working group 1 of the Joint EFP/AAP workshop. 2013. Periodontitis and atherosclerotic cardiovascular disease: Consensus report of the joint EFP/AAP workshop on periodontitis and systemic diseases. J Clin Periodontol. 40:S24–S29. doi: 10.1111/jcpe.12089.
    1. Turnbaugh PJ, Ley RE, Hamady M, Fraser-Liggett CM, Knight R, Gordon JI. The human microbiome project. Nature. 2007;449:804–810. doi: 10.1038/nature06244.
    1. van Winkelhoff AJ, Rams TE, Slots J. Systemic antibiotic therapy in periodontics. Periodontol 2000. 1996;10:45–78. doi: 10.1111/j.1600-0757.1996.tb00068.x.
    1. Varela-López A, Battino M, Bullón P, Quiles JL. Dietary antioxidants for chronic periodontitis prevention and its treatment. A review on current evidences from animal and human studies. ARS Pharm. 2015;56:131–140. doi: 10.4321/S2340-98942015000300001.
    1. Vicario M, Santos A, Violant D, Nart J, Giner L. Clinical changes in periodontal subjects with the probiotic Lactobacillus reuteri Prodentis: A preliminary randomized clinical trial. Acta Odontol Scand. 2013;71:813–819. doi: 10.3109/00016357.2012.734404.
    1. Vieira LV, de Sousa LM, Maia TAC, Gusmão JNFM, Goes P, Pereira KMA, Miyajima F, Gondim DV. Milk kefir therapy reduces inflammation and alveolar bone loss on periodontitis in rats. Biomed Pharmacother. 2021;139:111677. doi: 10.1016/j.biopha.2021.111677.
    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. doi: 10.3402/jom.v2i0.5344.
    1. Wang X, Geng X, Egashira Y, Sanada H. Purification and characterization of a feruloyl esterase from the intestinal bacterium Lactobacillus acidophilus. Appl Environ Microbiol. 2004;70:2367–2372. doi: 10.1128/AEM.70.4.2367-2372.2004.
    1. Wang Y, Andrukhov O, Rausch-Fan X. Oxidative stress and antioxidant system in periodontitis. Front Physiol. 2017;8:910. doi: 10.3389/fphys.2017.00910.
    1. Weydert CJ, Cullen JJ. Measurement of superoxide dismutase, catalase and glutathione peroxidase in cultured cells and tissue. Nat Protoc. 2010;5:51–66. doi: 10.1038/nprot.2009.197.
    1. Xu S, Boylston TD, Glatz BA. Conjugated linoleic acid content and organoleptic attributes of fermented milk products produced with probiotic bacteria. J Agric Food Chem. 2005;53:9064–9072. doi: 10.1021/jf051030u.
    1. Yamada M, Takahashi N, Matsuda Y, Sato K, Yokoji M, Sulijaya B, Maekawa T, Ushiki T, Mikami Y, Hayatsu M, Mizutani Y, Kishino S, Ogawa J, Arita M, Tabeta K, Maeda T, Yamazaki K. A bacterial metabolite ameliorates periodontal pathogen-induced gingival epithelial barrier disruption via GPR40 signaling. Sci Rep. 2018;8:9008. doi: 10.1038/s41598-018-27408-y.
    1. Yang HE, Li Y, Nishimura A, Jheng HF, Yuliana A, Kitano-Ohue R, Nomura W, Takahashi N, Kim CS, Yu R, Kitamura N, Park SB, Kishino S, Ogawa J, Kawada T, Goto T. Synthesized enone fatty acids resembling metabolites from gut microbiota suppress macrophage-mediated inflammation in adipocytes. Mol Nutr Food Res. 2017;61:1700064. doi: 10.1002/mnfr.201700064.
    1. Yang SJ, Choe TB. Antioxidant activity and whitening effect of Forsythiae fructus extracts. Korean J Med Crop Sci. 2011;19:472–477. doi: 10.7783/KJMCS.2011.19.6.472.
    1. Yokoji-Takeuchi M, Takahashi N, Yamada-Hara M, Sulijaya B, Tsuzuno T, Aoki-Nonaka Y, Tabeta K, Kishino S, Ogawa J, Yamazaki K. A bacterial metabolite induces Nrf2-mediated anti-oxidative responses in gingival epithelial cells by activating the MAPK signaling pathway. Arch Oral Biol. 2020;110:104602. doi: 10.1016/j.archoralbio.2019.104602.
    1. Zhang Y, Wang X, Li H, Ni C, Du Z, Yan F. Human oral microbiota and its modulation for oral health. Biomed Pharmacother. 2018;99:883–893. doi: 10.1016/j.biopha.2018.01.146.
    1. Zokaityte E, Cernauskas D, Klupsaite D, Lele V, Starkute V, Zavistanaviciute P, Ruzauskas M, Gruzauskas R, Juodeikiene G, Rocha JM, Bliznikas S, Viskelis P, Ruibys R, Bartkiene E. Bioconversion of milk permeate with selected lactic acid bacteria strains and apple by-products into beverages with antimicrobial properties and enriched with galactooligosaccharides. Microorganisms. 2020;8:1182. doi: 10.3390/microorganisms8081182.

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