Effects of probiotics on preventing caries in preschool children: a systematic review and meta-analysis
1North China University of Science and Technology, 063000 Tangshan, Hebei, China
2Department of stomatology, HeBei General Hospital, 050000 Shijiazhuang, Hebei, China
3Department of stomatology, Tangshan Workers Hospital, 063000 Tangshan, Hebei, China
DOI: 10.22514/jocpd.2023.014 Vol.47,Issue 2,March 2023 pp.85-100
Submitted: 31 July 2022 Accepted: 21 September 2022
Published: 03 March 2023
This paper systematically evaluate the effects of probiotics on preventing caries in preschool children. The present systematic review was conducted following the Transparent Reporting of Systematic Reviews and Meta-Analyses (PRISMA) guidelines and recorded in the International prospective register of systematic reviews (PROSPERO) database (registration no: CRD42022325286). Literature were screened from PubMed, Embase, Web of Sciences, China National Knowledge Infrastructure (CNKI), Wanfang and other databases from inception to April 2022 to identify randomized controlled trials on the clinical efficacies of probiotics in preventing dental caries in preschool children and extract relevant data. The meta-analysis was performed using the RevMan5.4 software and the Stata16. Cochrane handbook was used to assess the risk of bias. The Grading of Recommendations Assessment, Development and Evaluation (GRADEprofiler 3.6) was used to determine the evidence quality. A total of 17 randomized controlled trials were eligible, of which two trials had certain levels of bias and 15 had a low risk of bias. Evidence quality assessment showed that the included trials were of medium quality. The meta-analysis results showed that Lactobacillus rhamnosus was associated with a reduced incidence (p = 0.005) and progression (p < 0.001) of caries in preschool children. Probiotics could reduce the number of high-level Streptococcus mutans in saliva (p < 0.00001) but could not reduce the number of Streptococcus mutans in dental plaque nor the amount of Lactobacillus in the saliva and dental plaque. Current evidence shows that probiotics could prevent caries in preschool children, but Lactobacillus rhamnosus was more effective in preventing caries than others. Although probiotics could reduce high levels of Streptococcus mutans in saliva, they could not reduce the amount of Lactobacillus in saliva and dental plaque.
Caries; Probiotics; Preschool child; Microorganism; Systematic review; Meta-analysis
Nan Meng,Qi Liu,Qing Dong,Jianqi Gu,Yuanbo Yang. Effects of probiotics on preventing caries in preschool children: a systematic review and meta-analysis. Journal of Clinical Pediatric Dentistry. 2023. 47(2);85-100.
 Global Burden of Disease Study 2013 Collaborators. Global, regional, and national incidence, prevalence, and years lived with disability for 301 acute and chronic diseases and injuries in 188 countries, 1990–2013: a systematic analysis for the Global Burden of Disease Study 2013. The Lancet. 2015; 386: 743–800.
 Vos T, Flaxman AD, Naghavi M, Lozano R, Michaud C, Ezzati M, et al. Years lived with disability (YLDs) for 1160 sequelae of 289 diseases and injuries 1990–2010: a systematic analysis for the Global Burden of Disease Study 2010. The Lancet. 2012; 380: 2163–2196.
 Xi PF. Oral health status of chinese residents: report of the fourth china oral health epidemiological survey. The 18th Annual Oral Preventive Medicine Academic Conference of Chinese Stomatological Association. 2018.
 Yang ZL, Liu BY. Research progress on the microecology of dental plaque in caries. International Journal of Stomatology. 2020; 47: 506–514.
 Sanders M. Probiotics: definition, sources, selection, and uses. Clinical Infectious Diseases. 2008; 46: S58–S61.
 Sudhakara P, Gupta A, Bhardwaj A, Wilson A. Oral dysbiotic communi-ties and their implications in systemic diseases. Dentistry Journal. 2018; 6: 10.
 Zhan L. Rebalancing the caries microbiome dysbiosis: targeted treatment and sugar alcohols. Advances in Dental Research. 2018; 29: 110–116.
 Yu FY, Wang QQ, Li M, Cheng Y, Cheng YL, Zhou Y, et al. Dysbiosis of saliva microbiome in patients with oral lichen planus. BMC Microbiology. 2020; 20: 75.
 Marsh PD. Are dental diseases examples of ecological catastrophes?Microbiology. 2003; 149: 279–294.
 Cortés-Dorantes N, Ruiz-Rodríguez MS, Karakowsky-Kleiman L, Garrocho-Rangel JA, Sánchez-Vargas LO, Pozos-Guillén AJ. Probiotics and their effect on oral bacteria count in children: a pilot study. European Journal of Paediatric Dentistry, 2015, 16: 56–60.
 Villavicencio J, Villegas LM, Arango MC, Arias S, Triana F. Effects of a food enriched with probiotics on Streptococcus mutans and Lactobacillus spp. salivary counts in preschool children: a cluster randomized trial. Journal of Applied Oral Science. 2018; 26: e20170318.
 Pahumunto N, Piwat S, Chankanka O, Akkarachaneeyakorn N, Rangsit-sathian K, Teanpaisan R. Reducing mutans streptococci and caries development by Lactobacillus paracasei SD1 in preschool children: a randomized placebo-controlled trial. Acta Odontologica Scandinavica. 2018; 76: 331–337.
 Hasslöf P, West CE, Videhult FK, Brandelius C, Stecksén-Blicks C. Early intervention with probiotic Lactobacillus paracasei F19 has no long-term effect on caries experience. Caries Research. 2013; 47: 559–565.
 Moher D, Liberati A, Tetzlaff J, Altman DG, PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Medicine. 2009; 6: e1000097.
 Cumpston MS, McKenzie JE, Welch VA, Brennan SE. Strengthening systematic reviews in public health: guidance in the Cochrane Handbook for Systematic Reviews of Interventions, 2nd edition. Journal of Public Health. 2022. [Preprint].
 Zhu YB, Li W. How do clinicians understand meta-analysis. Medical Journal of Peking Union Medical College Hospital. 2020; 11: 314–319.
 Tehrani MH, Akhlaghi N, Talebian L, Emami J, Keyhani SE. Effects of probiotic drop containing Lactobacillus rhamnosus, Bifidobacterium infantis, and Lactobacillus reuteri on salivary Streptococcus mutans and Lactobacillus levels. Contemporary Clinical Dentistry. 2016; 7: 469–474.
 Alamoudi NM, Almabadi ES, El Ashiry EA, El Derwi DA. Effect of probiotic lactobacillus reuteri on salivary cariogenic bacterial counts among groups of preschool children in jeddah, saudi arabia: a randomized clinical trial. The Journal of Clinical Pediatric Dentistry. 2018; 42: 331–338.
 Almabadi ES, El Ashiry EA, Alamoudi NM, AI Tuwirqi AA, Zeiton RM. Evaluation of Lactobacillus reuteri probiotic lozenge intake on salivary cariogenic bacterial counts in preschool children: a randomized clinical trial. Medical Science. 2020; 24: 259–269.
 Manmontri C, Nirunsittirat A, Piwat S, Wattanarat O, Pahumunto N, Makeudom A, et al. Reduction of Streptococcus mutans by probiotic milk: a multicenter randomized controlled trial. Clinical Oral Investigations. 2020; 24: 2363–2374.
 Wattanarat O, Nirunsittirat A, Piwat S, Manmontri C, Teanpaisan R, Pahumunto N, et al. Significant elevation of salivary human neutrophil peptides 1–3 levels by probiotic milk in preschool children with severe early childhood caries: a randomized controlled trial. Clinical Oral Investigations. 2021; 25: 2891–2903.
 Piwat S, Teanpaisan R, Manmontri C, Wattanarat O, Pahumunto N, Makeudom A, et al. Efficacy of probiotic milk for caries regression in preschool children: a multicenter randomized controlled trial. Caries Research. 2020; 54: 491–501.
 Näse L, Hatakka K, Savilahti E, Saxelin M, Pönkä A, Poussa T, et al. Effect of long-term consumption of a probiotic bacterium, lactobacillus rhamnosus gg, in milk on dental caries and caries risk in children. Caries Research. 2001; 35: 412–420.
 Pohjavuori S, Ahola AJ, Yli-Knuuttila H, Piirainen L, Poussa T, Meurman JH. Effect of consumption of Lactobacillus rhamnosus GG and calcium, in carrot-pineapple juice on dental caries risk in children. International Journal of Probiotics and Prebiotics. 2010; 5: 221–228.
 Rodríguez G, Ruiz B, Faleiros S, Vistoso A, Marró ML, Sánchez J, et al. Probiotic compared with standard milk for high-caries children: a cluster randomized trial. Journal of Dental Research. 2016; 95: 402–407.
 Sandoval F, Faleiros S, Cabello R, Díaz-Dosque M, Rodríguez G, Escobar A. The consumption of milk supplemented with probiotics decreases the occurrence of caries and the salivary concentration of hβD-3 in children. Clinical Oral Investigations. 2021; 25: 3823–3830.
 Hedayati-Hajikand T, Lundberg U, Eldh C, Twetman S. Effect of probiotic chewing tablets on early childhood caries-a randomized controlled trial. BMC Oral Health. 2015; 15: 112.
 Stecksén-Blicks C, Sjöström I, Twetman S. Effect of long-term consumption of milk supplemented with probiotic lactobacilli and fluoride on dental caries and general health in preschool children: a cluster-randomized study. Caries Research. 2009; 43: 374–381.
 Taipale T, Pienihäkkinen K, Salminen S, Jokela J, Söderling E. Bifidobacterium animalis subsp. lactis BB-12 administration in early childhood: a randomized clinical trial of effects on oral colonization by mutans streptococci and the probiotic. Caries Research. 2012; 46: 69–77.
 Taipale T, Pienihäkkinen K, Alanen P, Jokela J, Söderling E. Administration of Bifidobacterium animalis subsp. lactis BB-12 in early childhood: a post-trial effect on caries occurrence at four years of age. Caries research. 2013; 47: 364–372.
 Bowen WH, Burne RA, Wu H, Koo H. Oral Biofilms: pathogens, matrix, and polymicrobial interactions in microenvironments. Trends in Microbiology. 2018; 26: 229–242.
 Twetman S. Prevention of dental caries as a non-communicable disease. European Journal of Oral Sciences. 2018; 126: 19–25.
 Pande R, Bagad M, Dubey V, Ghosh AR. Prospectus of probiotics in modern age diseases. Asian Pacific Journal of Tropical Biomedicine. 2012; 2: S1963–S1974.
 Campana R, van Hemert S, Baffone W. Strain-specific probiotic properties of lactic acid bacteria and their interference with human intestinal pathogens invasion. Gut Pathogens. 2017; 9: 12.
 Reid G. Probiotics: definition, scope and mechanisms of action. Best Practice & Research Clinical Gastroenterology. 2016; 30: 17–25.
 Collado MC, Meriluoto J, Salminen S. Measurement of aggregation properties between probiotics and pathogens: in vitro evaluation of different methods. Journal of Microbiological Methods. 2007; 71: 71–74.
 Stamatova I, Meurman J H. Probiotics: health benefits in the mouth. American Journal of Dentistry. 2009; 22: 329–338.
 Toiviainen A. Probiotics and oral health: in vitro and clinical studies. Annales Universitatis Turkuensis, Sarja–Ser. D, Medica-Odontologica, 2015.
 Schwendicke F, Korte F, Dörfer CE, Kneist S, Fawzy El-Sayed K, Paris S. Inhibition of streptococcus mutans growth and biofilm formation by probiotics in vitro. Caries Research. 2017;
 Chandrasekhar SN, Mallikarjun SB, Salim HP. Comparative evaluation of antibacterial activity of probiotics SK12 and SM18: An in vitro study. International Journal of Clinical Pediatric Dentistry. 2021; 13: 611–616.
 Hao SY, Wang JH, Zhang XQ, Zou J, Wang Y. Efficacy and safety of Bifidobacteria in preventing caries: a systematic review and meta⁃analysis. Journal of Dental Prevention & Treatment. 2021; 29: 241–248.
 Twetman S, Jørgensen MR. Can probiotic supplements prevent early childhood caries? A systematic review and meta-analysis. Beneficial Microbes. 2021; 12: 231–238.
 Hotel ACP, Cordoba A. Health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria. Prevention. 2001; 5: 1–10.
 Haukioja A, Yli-Knuuttila H, Loimaranta V, Kari K, Ouwehand AC, Meurman JH, et al. Oral adhesion and survival of probiotic and other lactobacilli and bifidobacteria in vitro. Oral Microbiology and Immunology. 2006; 21: 326–332.
 Caglar E, Kargul B, Tanboga I. Bacteriotherapy and probiotics’ role on oral health. Oral Diseases. 2005; 11: 131–137.
 Chapman CMC, Gibson GR, Rowland I. In vitro evaluation of single- and multi-strain probiotics: inter-species inhibition between probiotic strains, and inhibition of pathogens. Anaerobe. 2012; 18: 405–413.
 Grudianov A, Dmitrieva N, Fomenko E. Use of probiotics Bifidum-bacterin and Acilact in tablets in therapy of periodontal inflammations. Stomatologiia. 2002; 81: 39–43.
 Fang F, Xu J, Li Q, Xia X, Du G. Characterization of a Lactobacillus brevis strain with potential oral probiotic properties. BMC Microbiology. 2018; 18: 221.
 Laleman I, Detailleur V, Slot DE, Slomka V, Quirynen M, Teughels W. Probiotics reduce mutans streptococci counts in humans: a systematic review and meta-analysis. Clinical Oral Investigations. 2014; 18: 1539–1552.
 Nadelman P, Magno MB, Masterson D, da Cruz AG, Maia LC. Are dairy products containing probiotics beneficial for oral health? A systematic review and meta-analysis. Clinical Oral Investigations. 2018; 22: 2763–2785.
 Coqueiro AY, Bonvini A, Raizel R, Tirapegui J, Rogero MM. Probiotic supplementation in dental caries: is it possible to replace conventional treatment? Nutrire. 2018; 43: 6.
 Caufield PW, Li Y, Dasanayake A, Saxena D. Diversity of lactobacilli in the oral cavities of young women with dental caries. Caries Research. 2007; 41: 2–8.
 Piwat S, Teanpaisan R, Dahlén G, Thitasomakul S, Douglas CWI. Acid production and growth by oral Lactobacillus species in vitro. Journal of Investigative and Clinical Dentistry. 2012; 3: 56–61.
 Simón-Soro A, Mira A. Solving the etiology of dental caries. Trends in Microbiology. 2015; 23: 76–82.
 Abiko Y, Saitoh M. Salivary Defensins and their importance in oral health and disease. Current Pharmaceutical Design. 2007; 13: 3065–3072.
 Harder J, Bartels J, Christophers E, Schroder JM. Isolation and characterization of human beta-defensin-3, a novel human inducible peptide antibiotic. The Journal of Biological Chemistry. 2001; 276: 5707–5713.
 Dhople V, Krukemeyer A, Ramamoorthy A. The human beta-defensin-3, an antibacterial peptide with multiple biological functions. Biochimica et Biophysica Acta. 2006; 1758: 1499–1512.
 Twetman S, Stecksen-Blicks C. Probiotics and oral health effects in children. International Journal of Paediatric Dentistry. 2008; 18: 3–10.
 Twetman S. Are we ready for caries prevention through bacteriotherapy?Brazilian Oral Research. 2012; 26: 64–70.
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