Abstract
The current oral health crisis, whose causes are varied and complex, necessitates timely oral evaluation and early detection and treatment of oral health problems. Dramatic changes in eating habits and lifestyles are associated with the recent decline in oral health. Probiotics are “good” bacteria that support digestion and a healthy immune system and offer various health benefits to the host. Traditionally, probiotics have been used to improve gut health; the most common uses have historically been as a treatment or prevention of gastrointestinal infections and disease. During the last decade, studies have additionally suggested the intake of probiotics for oral health purposes. Probiotic use provides an effective strategy to combat oral disease, including the development of dental caries and periodontal infection. The aim of this review is to describe the beneficial roles of probiotic bacteria in the oral cavity and the potential mechanisms by which these bacteria exert their effects on oral health.
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References
Aas JA, Paster BJ, Stokes LN, Olsen I, Dewhirst FE (2005) Defining the normal bacterial flora of the oral cavity. J Clin Microbiol 43(11):5721–5732. https://doi.org/10.1128/JCM.43.11.5721-5732.2005
Ajdić D, McShan WM, McLaughlin RE, Savić G, Chang J, Carson MB, Primeaux C, Tian R, Kenton S, Jia H, Lin S, Qian Y, Li S, Zhu H, Najar F, Lai H, White J, Roe BA, Ferretti JJ (2002) Genome sequence of Streptococcus mutans UA159, a cariogenic dental pathogen. Proc Natl Acad Sci U S A 99(22):14434–14439. https://doi.org/10.1073/pnas.172501299
Banas JA, Vickerman MM (2003) Glucan-binding proteins of the oral streptococci. Crit Rev Oral Biol Med 14(2):89–99. https://doi.org/10.1177/154411130301400203
Bartold PM, Van Dyke TE (2013) Periodontitis: a host-mediated disruption of microbial homeostasis. Periodontol 62(1):203–217. https://doi.org/10.1111/j.1600-0757.2012.00450.x
Burt BA, Pai S (2001) Sugar consumption and caries risk: a systematic review. J Dent Educ 65(10):1017–1023
Busscher HJ, van Hoogmoed CG, Geertsema-Doornbusch GI, van der Kuijl-Booij M, van der Mei HC (1997) Streptococcus thermophilus and its biosurfactants inhibit adhesion by Candida spp. on silicone rubber. Appl Environ Microbiol 63(10):3810–3817
Caufield PW, Dasanayake AP, Li Y, Pan Y, Hsu J, Hardin JM (2000) Natural history of Streptococcus sanguinis in the oral cavity of infants: evidence for a discrete window of infectivity. Infect Immun 68(7):4018–4023. https://doi.org/10.1128/IAI.68.7.4018-4023.2000
Chen F, Wang D (2010) Novel technologies for the prevention and treatment of dental caries: a patent survey. Expert Opin Ther Pat 20(5):681–694. https://doi.org/10.1517/13543771003720491
Chen T, Yu WH, Izard J, Baranova OV, Lakshmanan A, Dewhirst FE (2010) The human oral microbiome database: a web accessible resource for investigating oral microbe taxonomic and genomic information. Database (Oxford) 2010(0):baq013. https://doi.org/10.1093/database/baq013
Cheng MC, Tsai TY, Pan TM (2015) Anti-obesity activity of the water extract of Lactobacillus paracasei subsp. paracasei NTU 101 fermented soy milk products. Food Funct 6(11):3522–3530. https://doi.org/10.1039/C5FO00531K
Chiang SS, Liao JW, Pan TM (2012) Effect of bioactive compounds in lactobacilli-fermented soy skim milk on femoral bone microstructure of aging mice. J Sci Food Agric 92(2):328–335. https://doi.org/10.1002/jsfa.4579
Chiu CH, TY L, Tseng YY, Pan TM (2006) The effects of Lactobacillus-fermented milk on lipid metabolism in hamsters fed on high-cholesterol diet. Appl Microbiol Biotechnol 71(2):238–245. https://doi.org/10.1007/s00253-005-0145-0
Chuang LC, Huang CS, Ou-Yang LW, Lin SY (2011) Probiotic Lactobacillus paracasei effect on cariogenic bacterial flora. Clin Oral Investig 15(4):471–476. https://doi.org/10.1007/s00784-010-0423-9
Clarke JK (1924) On the bacterial factor in the etiology of dental caries. Br J Exp Pathol 5:141–147
Comelli EM, Guggenheim B, Stingele F, Neeser JR (2002) Selection of dairy bacterial strains as probiotics for oral health. Eur J Oral Sci 110(3):218–224. https://doi.org/10.1034/j.1600-0447.2002.21216.x
Conrads G, de Soet JJ, Song J, Henne K, Sztajer H, Wagner-Döbler I, Zeng AP (2014) Comparing the cariogenic species Streptococcus sobrinus and S. mutans on whole genome level. J Oral Microbiol 6(1):26189. https://doi.org/10.3402/jom.v6.26189
Dhir S (2013) Biofilm and dental implant: the microbial link. J Indian Soc Periodontol 17(1):5–11. https://doi.org/10.4103/0972-124X.107466
Dubrac S, Msadek T (2004) Identification of genes controlled by the essential YycG/YycF two-component system of Staphylococcus aureus. J Bacteriol 186(4):1175–1181. https://doi.org/10.1128/JB.186.4.1175-1181.2004
Duque C, Stipp RN, Wang B, Smith DJ, Höfling JF, Kuramitsu HK, Duncan MJ, Mattos-Graner RO (2011) Downregulation of GbpB, a component of the VicRK regulon, affects biofilm formation and cell surface characteristics of Streptococcus mutans. Infect Immun 79(2):786–796. https://doi.org/10.1128/IAI.00725-10
FAO/WHO (2002) Guidelines for the evaluation of probiotics in foods. Food and Agriculture Organization of the United Nations and World Health Organization Expert Consultation Report. Food and Agricultural Organization of the United Nations and World Health Organization Working Group Report (http://www.who.int/foodsafety/fs_management/en/probiotic_guidelines.pdf)
Featherstone JD (1999) Prevention and reversal of dental caries: role of low level fluoride. Community Dent Oral Epidemiol 27(1):31–40. https://doi.org/10.1111/j.1600-0528.1999.tb01989.x
Featherstone JD, Adair SM, Anderson MH, Berkowitz RJ, Bird WF, Crall JJ, Den Besten PK, Donly KJ, Glassman P, Milgrom P, Roth JR, Snow R, Stewart RE (2003) Caries management by risk assessment: consensus statement. J Calif Dent 31:257–269
Fukushima T, Szurmant H, Kim EJ, Perego M, Hoch JA (2008) A sensor histidine kinase co-ordinates cell wall architecture with cell division in Bacillus subtilis. Mol Microbiol 69(3):621–632. https://doi.org/10.1111/j.1365-2958.2008.06308.x
Hasslöf P, Hedberg M, Twetman S, Stecksén-Blicks C (2010) Growth inhibition of oral mutans streptococci and candida by commercial probiotic lactobacilli–an in vitro study. BMC Oral Health 10(1):18–23. https://doi.org/10.1186/1472-6831-10-18
Haukioja A (2010) Probiotics and oral health. Eur J Dent 4(3):348–355
Hoceini A, Khelil NK, Ben-Yelles I, Mesli A, Ziouani S, Ghellai L, Aissaoui N, Nas F, Arab M (2016) Caries-related factors and bacterial composition of supragingival plaques in caries free and caries active Algerian adults. Asian Pac J Trop Biomed 6(8):720–726. https://doi.org/10.1016/j.apjtb.2016.06.011
Jørgensen MR, Keller MK, Kragelund C, Hamberg K, Ericson D, Nielsen CH, Twetman S (2016) 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 74(5):399–404. https://doi.org/10.3109/00016357.2016.1169439
Karpiński TM, Szkaradkiewicz AK (2013) Microbiology of dental caries. J Biol Earth Sci 3:M21–M24
Keyes PH, Jordan HV (1964) Periodontal lesions in the Syrian hamster-III. Findings related to an infectious and transmissible component. Arch Oral Biol 9(4):377–400. https://doi.org/10.1016/0003-9969(64)90024-X
Kidd EA, Fejerskov O (2004) What constitutes dental caries? Histopathology of carious enamel and dentin related to the action of cariogenic biofilms. J Dent Res 83:Spec No C:C35–38
Kleinberg I (2002) A mixed-bacteria ecological approach to understanding the role of the oral bacteria in dental caries causation: an alternative to Streptococcus mutans and the specific-plaque hypothesis. Crit Rev Oral Biol Med 13(2):108–125. https://doi.org/10.1177/154411130201300202
Koo H, Xiao J, Klein MI, Jeon JG (2010) Exopolysaccharides produced by Streptococcus mutans glucosyltransferases modulate the establishment of microcolonies within multispecies biofilms. J Bacteriol 192(12):3024–3032. https://doi.org/10.1128/JB.01649-09
Kraft-Bodi E, Jørgensen MR, Keller MK, Kragelund C, Twetman S (2015) Effect of probiotic bacteria on oral Candida in frail elderly. J Dent Res 94(9_suppl):181S–186S. https://doi.org/10.1177/0022034515595950
Krasse P, Carlsson B, Dahl C, Paulsson A, Nilsson A, Sinkiewicz G (2006) Decreased gum bleeding and reduced gingivitis by the probiotic Lactobacillus reuteri. Swed Dent J 30(2):55–60
Kristofersson K, Grondahl JG, Bratthall D (1985) The more Streptococcus mutans, the more caries on approximal surfaces. J Dent Res 64(1):58–61. https://doi.org/10.1177/00220345850640011101
Lin TH, Pan TM (2014) Inhibitory effect of Lactobacillus paracasei subsp. paracasei NTU 101 on rat dental caries. J Funct Foods 10:223–231. https://doi.org/10.1016/j.jff.2014.06.015
Lin FM, Chiu CH, Pan TM (2004) Fermentation of a milk–soymilk and Lycium chinense Miller mixture using a new isolate of Lactobacillus paracasei subsp. paracasei NTU 101 and Bifidobacterium longum. J Ind Microbiol 31(12):559–564. https://doi.org/10.1007/s10295-004-0184-z
Lin YT, Chou CC, Hsu CY (2017) Effects of Lactobacillus casei Shirota intake on caries risk in children. J Dent Sci 12(2):179–184. https://doi.org/10.1016/j.jds.2016.09.005
Liong MT (2008) Roles of probiotics and prebiotics in colon cancer prevention: postulated mechanisms and in-vivo evidence. Int J Mol Sci 9(5):854–863. https://doi.org/10.3390/ijms9050854
Liu CF, CL H, Chiang SS, Tseng KC, RC Y, Pan TM (2009) Beneficial preventive effects of gastric mucosal lesion for soy-skim milk fermented by lactic acid bacteria. J Agric Food Chem 57(10):4433–4438. https://doi.org/10.1021/jf900465c
Liu CF, Tung YT, CL W, Lee BH, Hsu WH, Pan TM (2011) Antihypertensive effects of Lactobacillus-fermented milk orally administered to spontaneously hypertensive rats. J Agric Food Chem 59(9):4537–4543. https://doi.org/10.1021/jf104985v
Lodi CS, Manarelli MM, Sassaki KT, Fraiz FC, Delbem ACB, Martinhon CCR (2010) Evaluation of fermented milk containing probiotic on dental enamel and biofilm: in situ study. Arch Oral Biol 55(1):29–33. https://doi.org/10.1016/j.archoralbio.2009.10.009
Lynch DJ, Fountain TL, Mazurkiewicz JE, Banas JA (2007) Glucan-binding proteins are essential for shaping Streptococcus mutans biofilm architecture. FEMS Microbiol Lett 268(2):158–165. https://doi.org/10.1111/j.1574-6968.2006.00576.x
Marsh PD (2004) Dental plaque as a microbial biofilm. Caries Res 38(3):204–211. https://doi.org/10.1159/000077756
Marsh PD, Martin MV (1999) Oral Microbiology, 4th edn. Wright, Oxford
Marsh PD, Martin MV, Lewis MA, Williams DW, Marsh PD, Martin MV (2012) Oral microbiology, 5th edn. Elsevier, Edinburgh
Mattila-Sandholm T, Saarela M (2003) Functional dairy products. Woodhead Publishing, UK. https://doi.org/10.1533/9781855736917
Meurman JH, Stamatova I (2007) Probiotics: contributions to oral health. Oral Dis 13(5):443–451. https://doi.org/10.1111/j.1601-0825.2007.01386.x
Näse L, Hatakka K, Savilahti E, Saxelin M, Pönkä A, Poussa T, Korpela R, Meurman JH (2001) Effect of long-term consumption of a probiotic bacterium, Lactobacillus rhamnosus GG, in milk on dental caries and caries risk in children. Caries Res 35(6):412–420. https://doi.org/10.1159/000047484
Ortet P, Whitworth DE, Santaella C, Achouak W, Barakat M (2015) P2CS: updates of the prokaryotic two-component systems database. Nucleic Acids Res 43(D1):D536–D541. https://doi.org/10.1093/nar/gku968
Pozharitskaia MM, Morozova LV, Mel'nichuk GM, Mel'nichuk SS (1994) The use of the new bacterial biopreparation Acilact in the combined treatment of periodontitis. Stomatologiia (Mosk) 73(2):17–20
Rastogi P, Saini H, Dixit J, Singhal R (2011) Probiotics and oral health. Natl J Maxillofac Surg 2(1):6–9. https://doi.org/10.4103/0975-5950.85845
Robertson PB, Mackler BF, Wright TE, Levy BM (1980) Periodontal status of patients with abnormalities of the immune system. II. Observations over a 2-year period. J Periodontol 51(2):70–73. https://doi.org/10.1902/jop.1980.51.2.70
Rodrigues L, van der Mei H, Teixeira JA, Oliveira R (2004) Biosurfactant from Lactococcus lactis 53 inhibits microbial adhesion on silicone rubber. Appl Microbiol Biotechnol 66(3):306–311. https://doi.org/10.1007/s00253-004-1674-7
Saarela M, Laĥteenmaki L, Crittenden R, Salminen S, Mattila-Sandholm T (2002) Gut bacteria and health foods—the European perspective. Int J Food Microbiol 78(1-2):99–117. https://doi.org/10.1016/S0168-1605(02)00235-0
Sato Y, Yamamoto Y, Kizaki H (2000) Construction of region-specific partial duplication mutants (merodiploid mutants) to identify the regulatory gene for the glucan-binding protein C gene in vivo in Streptococcus mutans. FEMS Microbiol Lett 186(2):187–191. https://doi.org/10.1111/j.1574-6968.2000.tb09102.x
Saxelin M, Tynkkynen S, Mattila-Sandholm T, de Vos WM (2005) Probiotic and other functional microbes: from markets to mechanisms. Curr Opin Biotechnol 16(2):204–211. https://doi.org/10.1016/j.copbio.2005.02.003
Schwandt LQ, van Weissenbruch R, van der Mei HC, Busscher HJ, Albers FW (2005) Effect of dairy products on the lifetime of Provox2 voice prostheses in vitro and in vivo. Head Neck 27(6):471–477. https://doi.org/10.1002/hed.20180
Selwitz RH, Ismail A, Pitts NB (2007) Dental caries. Lancet 369(9555):51–59. https://doi.org/10.1016/S0140-6736(07)60031-2
Senadheera MD, Guggenheim B, Spatafora GA, Huang YC, Choi J, Hung DC, Treglown JS, Goodman SD, Ellen RP, Cvitkovitch DG (2005) A VicRK signal transduction system in Streptococcus mutans affects gtfBCD, gbpB, and ftf expression, biofilm formation, and genetic competence development. J Bacteriol 187(12):4064–4076. https://doi.org/10.1128/JB.187.12.4064-4076.2005
Senadheera DB, Cordova M, Ayala EA, Chávez de Paz LE, Singh K, Downey JS, Svensäter G, Goodman SD, Cvitkovitch DG (2012) Regulation of bacteriocin production and cell death by the VicRK signaling system in Streptococcus mutans. J Bacteriol 194(6):1307–1316. https://doi.org/10.1128/JB.06071-11
Simon L (2007) The role of Streptococcus mutans and oral ecology in the formation of dental caries. Lethbridge Undergraduate Res J 2:1–6
Slavkin HC (1999) Streptococcus mutans, early childhood caries and new opportunities. J Am Dent Assoc 130(12):1787–1792. 10.14219/jada.archive.1999.0138
Sliepen I, Van Damme J, Van Essche M, Loozen G, Quirynen M, Teughels W (2009) Microbial interactions influence inflammatory host cell responses. J Dent Res 88(11):1026–1030. https://doi.org/10.1177/0022034509347296
Stipp RN, Boisvert H, Smith DJ, Höfling JF, Duncan MJ, Mattos-Graner RO (2013) CovR and VicRK regulate cell surface biogenesis genes required for biofilm formation in Streptococcus mutans. PLoS One 8(3):e58271. https://doi.org/10.1371/journal.pone.0058271
Struzycka I (2014) The oral microbiome in dental caries. Pol J Microbiol 63(2):127–135
Takahashi N, Nyvad B (2011) The role of bacteria in the caries process: ecological perspectives. J Dent Res 90(3):294–303. https://doi.org/10.1177/0022034510379602
Tambekar D, Bhutada S (2009) Studies on antimicrobial activity and characteristics of bacteriocins produced by Lactobacillus strains isolated from milk of domestic animals. Int J Microbiol 8:1–5
Tokunaga T, Oku T, Hosoya N (1989) Utilization and excretion of a new sweetener, fructooligosaccharide (Neosugar), in rats. J Nutr 119(4):553–559
Tsai YT, Cheng PC, Fan CK, Pan TM (2008) Time-dependent persistence of enhanced immune response by a potential probiotic strain Lactobacillus paracasei subsp. paracasei NTU 101. Int J Food Microbiol 10(128):219–225
Tsai TY, Chu LH, Lee CH, Pan TM (2009) Atherosclerosis-preventing activity of lactic acid bacteria-fermented milk-soymilk supplemented with Momordica charantia. J Agric Food Chem 57(5):2065–2071. https://doi.org/10.1021/jf802936c
Tsai YT, Cheng PC, Pan TM (2010) Immunomodulating activity of Lactobacillus paracasei subsp. paracasei NTU 101 in enterohemorrhagic Escherichia coli O157:H7-infected mice. J Agric Food Chem 58(21):11265–11272. https://doi.org/10.1021/jf103011z
Twetman L, Larsen U, Fiehn NE, Stecksén-Blicks C, Twetman S (2009) Coaggregation between probiotic bacteria and caries-associated strains: an in vitro study. Acta Odontol Scand 67(5):284–288. https://doi.org/10.1080/00016350902984237
Vargas CM, Crall JJ, Schneider DA (1998) Sociodemographic distribution of pediatric dental caries: NHANES III, 1988–1994. J Am Dent Assoc 129(9):1229–1238. 10.14219/jada.archive.1998.0420
Venkatesan G, Ashita Uppoor A, Dilip G, Naik DG (2013) Redefining the role of dendritic cells in periodontics. J Indian Soc Periodontol 17(6):700–705. https://doi.org/10.4103/0972-124X.124467
Volozhin AI, Il’in VK, Maksimovskiĭ IM, Sidorenko AB, Istranov LP, Tsarev VN, Istranova EV, Aboiants RK (2004) Development and use of periodontal dressing of collagen and Lactobacillus casei 37 cell suspension in combined treatment of periodontal disease of inflammatory origin. Stomatologiia (Mosk) 83(6):6–8
WHO (2003) The world oral health report. Continuous improvement of oral health in the 21st century—the approach of the WHO Global Oral Health Programme. (http://www.who.int/oral_health)
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Lin, TH., Lin, CH. & Pan, TM. The implication of probiotics in the prevention of dental caries. Appl Microbiol Biotechnol 102, 577–586 (2018). https://doi.org/10.1007/s00253-017-8664-z
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DOI: https://doi.org/10.1007/s00253-017-8664-z