Advertisement

Clinical Oral Investigations

, Volume 18, Issue 6, pp 1539–1552 | Cite as

Probiotics reduce mutans streptococci counts in humans: a systematic review and meta-analysis

  • Isabelle Laleman
  • Valentine Detailleur
  • Dagmar Else Slot
  • Vera Slomka
  • Marc Quirynen
  • Wim Teughels
Review

Abstract

Objectives

Systematically review the available literature regarding the caries-preventive effect of probiotics.

Data, sources and study selection

An electronic search was conducted in three databases (PubMed MEDLINE, ISI Web of Science and Cochrane Library) to identify all suitable studies. The outcomes had to be presented as the effect of probiotics on the incidence of caries or on the levels of mutans streptococci and/or Lactobacillus species. Human studies, written in English, with at least 15 participants, comparing a probiotic product with a placebo/no probiotic were included. Where possible, a meta-analysis was performed to obtain quantitative data.

Results

Since only two articles presented useful data on the caries incidence, we focused on the surrogate endpoints: mutans streptococci and/or Lactobacillus counts. The meta-analysis showed that when the probiotic and control group are compared after treatment, significantly more patients in the probiotic group had low mutans streptococci (<105 CFU/ml) counts and significantly less patients had high (>106 CFU/ml) counts. Regarding the Lactobacillus counts, comparing the probiotic and control group at the end of the probiotic use, no significant differences could be observed, neither in low (<104 CFU/ml) nor in high Lactobacillus (>106 CFU/ml) counts.

Conclusions

Within the limitations of the available data, it may be concluded that probiotics decrease the mutans streptococci counts. This suggests that probiotics could have a positive effect in the prevention of caries.

Clinical relevance

There is insufficient evidence that probiotics can prevent caries, but they can reduce the mutans streptococci counts.

Keywords

Probiotics Caries Tooth decay Cariogenic bacteria Mutans streptococci Lactobacilli Streptococcus mutans 

Notes

Acknowledgments

Funding source

The study was funded by grants of the Katholieke Universiteit Leuven and the Fund for Scientific Research Flanders.

Conflict of interest

The authors declare that they have no conflict of interest. However, Wim Teughels has received grants from the Katholieke Universiteit Leuven, the Fund for Scientific Research Flanders, BioGaia and Pierre Fabre Médicament for studies in the field of oral probiotics and periodontitis.

Supplementary material

784_2014_1228_MOESM1_ESM.docx (109 kb)
ESM 1 (DOCX 108 kb)

References

  1. 1.
    Selwitz RH, Ismail AI, Pitts NB (2007) Dental caries. Lancet 369:51–59. doi: 10.1016/S0140-6736(07)60031-2 PubMedCrossRefGoogle Scholar
  2. 2.
    Michalek SM, Katz J, Childers NK (2001) A vaccine against dental caries: an overview. BioDrugs Clin Immunother Biopharm Gene Ther 15:501–508Google Scholar
  3. 3.
    Fejerskov O (2004) Changing paradigms in concepts on dental caries: consequences for oral health care. Caries Res 38:182–191. doi: 10.1159/000077753 PubMedCrossRefGoogle Scholar
  4. 4.
    Caufield PW, Li Y, Dasanayake A (2005) Dental caries: an infectious and transmissible disease. Compend Contin Educ Dent Jamesburg NJ 26:10–16Google Scholar
  5. 5.
    Loesche WJ (1986) Role of Streptococcus mutans in human dental decay. Microbiol Rev 50:353–380PubMedCentralPubMedGoogle Scholar
  6. 6.
    Hajishengallis G, Michalek SM (1999) Current status of a mucosal vaccine against dental caries. Oral Microbiol Immunol 14:1–20PubMedCrossRefGoogle Scholar
  7. 7.
    Tanzer JM, Livingston J, Thompson AM (2001) The microbiology of primary dental caries in humans. J Dent Educ 65:1028–1037PubMedGoogle Scholar
  8. 8.
    Featherstone JD (2000) The science and practice of caries prevention. J Am Dent Assoc 1939 131:887–899CrossRefGoogle Scholar
  9. 9.
    Featherstone JDB (2004) The continuum of dental caries—evidence for a dynamic disease process. J Dent Res 83:C39–C42, Spec No CPubMedCrossRefGoogle Scholar
  10. 10.
    Marsh P, Martin MV, Lewis MAO (2009) Oral microbiology. Churchill-LivingstonGoogle Scholar
  11. 11.
    Anderson MH, Shi W (2006) A probiotic approach to caries management. Pediatr Dent 28:151–153, discussion 192–198PubMedGoogle Scholar
  12. 12.
    Teughels W, Van Essche M, Sliepen I, Quirynen M (2008) Probiotics and oral healthcare. Periodontol 2000 48:111–147. doi: 10.1111/j.1600-0757.2008.00254.x PubMedCrossRefGoogle Scholar
  13. 13.
    Meurman JH (2005) Probiotics: do they have a role in oral medicine and dentistry? Eur J Oral Sci 113:188–196. doi: 10.1111/j.1600-0722.2005.00191.x PubMedCrossRefGoogle Scholar
  14. 14.
    Meurman JH, Stamatova I (2007) Probiotics: contributions to oral health. Oral Dis 13:443–451. doi: 10.1111/j.1601-0825.2007.01386.x PubMedCrossRefGoogle Scholar
  15. 15.
    Teughels W, Loozen G, Quirynen M (2011) Do probiotics offer opportunities to manipulate the periodontal oral microbiota? J Clin Periodontol 38(Suppl 11):159–177. doi: 10.1111/j.1600-051X.2010.01665.x PubMedCrossRefGoogle Scholar
  16. 16.
    Choudhari S, Mopagar V (2011) Probiotic way of dental caries prevention. Int. J. Contemp. Dent. 2:Google Scholar
  17. 17.
    Broekaert IJ, Walker WA (2006) Probiotics and chronic disease. J Clin Gastroenterol 40:270–274PubMedCrossRefGoogle Scholar
  18. 18.
    Henker J, Schuster F, Nissler K (2001) Successful treatment of gut-caused halitosis with a suspension of living non-pathogenic Escherichia coli bacteria—a case report. Eur J Pediatr 160:592–594PubMedCrossRefGoogle Scholar
  19. 19.
    Burton JP, Wescombe PA, Cadieux PA, Tagg JR (2011) Beneficial microbes for the oral cavity: Time to harness the oral streptococci? Benefic Microbes 2:93–101CrossRefGoogle Scholar
  20. 20.
    Kang M-S, Kim B-G, Chung J et al (2006) Inhibitory effect of Weissella cibariaisolates on the production of volatile sulphur compounds. J Clin Periodontol 33:226–232PubMedCrossRefGoogle Scholar
  21. 21.
    Ahola AJ, Yli-Knuuttila H, Suomalainen T et al (2002) Short-term consumption of probiotic-containing cheese and its effect on dental caries risk factors. Arch Oral Biol 47:799–804PubMedCrossRefGoogle Scholar
  22. 22.
    Hatakka K, Ahola AJ, Yli-Knuuttila H et al (2007) Probiotics reduce the prevalence of oral candida in the elderly—a randomized controlled trial. J Dent Res 86:125–130PubMedCrossRefGoogle Scholar
  23. 23.
    Teughels W, Newman MG, Coucke W et al (2007) Guiding periodontal pocket recolonization: a proof of concept. J Dent Res 86:1078–1082PubMedCrossRefGoogle Scholar
  24. 24.
    Nackaerts O, Jacobs R, Quirynen M et al (2008) Replacement therapy for periodontitis: pilot radiographic evaluation in a dog model. J Clin Periodontol 35:1048–1052. doi: 10.1111/j.1600-051X.2008.01333.x PubMedCrossRefGoogle Scholar
  25. 25.
    Krasse P, Carlsson B, Dahl C et al (2006) Decreased gum bleeding and reduced gingivitis by the probiotic Lactobacillus reuteri. Swed Dent J 30:55–60PubMedGoogle Scholar
  26. 26.
    Twetman L, Larsen U, Fiehn N-E et al (2009) Coaggregation between probiotic bacteria and caries-associated strains: an in vitro study. Acta Odontol Scand 67:284–288PubMedCrossRefGoogle Scholar
  27. 27.
    Shimauchi H, Mayanagi G, Nakaya S et al (2008) Improvement of periodontal condition by probiotics with Lactobacillus salivarius WB21: a randomized, double-blind, placebo-controlled study. J Clin Periodontol 35:897–905. doi: 10.1111/j.1600-051X.2008.01306.x PubMedCrossRefGoogle Scholar
  28. 28.
    Mayanagi G, Kimura M, Nakaya S et al (2009) Probiotic effects of orally administered Lactobacillus salivarius WB21-containing tablets on periodontopathic bacteria: a double-blinded, placebo-controlled, randomized clinical trial. J Clin Periodontol 36:506–513. doi: 10.1111/j.1600-051X.2009.01392.x PubMedCrossRefGoogle Scholar
  29. 29.
    Staab B, Eick S, Knöfler G, Jentsch H (2009) The influence of a probiotic milk drink on the development of gingivitis: a pilot study. J Clin Periodontol 36:850–856. doi: 10.1111/j.1600-051X.2009.01459.x PubMedCrossRefGoogle Scholar
  30. 30.
    Zahradnik RT, Magnusson I, Walker C et al (2009) Preliminary assessment of safety and effectiveness in humans of ProBiora3(trademark) a probiotic mouthwash. J Appl Microbiol 107:682–690PubMedCrossRefGoogle Scholar
  31. 31.
    Riccia DND, Bizzini F, Perilli MG et al (2007) Anti-inflammatory effects of Lactobacillus brevis (CD2) on periodontal disease. Oral Dis 13:376–385. doi: 10.1111/j.1601-0825.2006.01291.x PubMedCrossRefGoogle Scholar
  32. 32.
    Moher D, Liberati A, Tetzlaff J, Altman DG (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 6:e1000097. doi: 10.1371/journal.pmed.1000097 PubMedCentralPubMedCrossRefGoogle Scholar
  33. 33.
    Stamatova I, Meurman JH (2009) Probiotics and periodontal disease. Periodontology 2000 51:141–151. doi: 10.1111/j.1600-0757.2009.00305.x PubMedCrossRefGoogle Scholar
  34. 34.
    Bonifait L, Chandad F, Grenier D (2009) Probiotics for oral health: myth or reality? J Can Dent Assoc 75:585–590PubMedGoogle Scholar
  35. 35.
    Twetman S (2012) Are we ready for caries prevention through bacteriotherapy? Braz Oral Res 26(Suppl 1):64–70PubMedCrossRefGoogle Scholar
  36. 36.
    Ahn S-J, Lim B-S, Lee S-J (2007) Prevalence of cariogenic streptococci on incisor brackets detected by polymerase chain reaction. Am J Orthod Dentofac Orthop Off Publ Am Assoc Orthod Const Soc Am Board Orthod 131:736–741. doi: 10.1016/j.ajodo.2005.06.036 CrossRefGoogle Scholar
  37. 37.
    Schulz KF, Altman DG, Moher D (2010) CONSORT 2010 statement: updated guidelines for reporting parallel group randomised trials. J Clin Epidemiol 63:834–840. doi: 10.1016/j.jclinepi.2010.02.005 PubMedCrossRefGoogle Scholar
  38. 38.
    Verhagen AP, de Vet HC, de Bie RA et al (1998) The Delphi list: a criteria list for quality assessment of randomized clinical trials for conducting systematic reviews developed by Delphi consensus. J Clin Epidemiol 51:1235–1241PubMedCrossRefGoogle Scholar
  39. 39.
    Van der Weijden F, Dell’Acqua F, Slot DE (2009) Alveolar bone dimensional changes of post-extraction sockets in humans: a systematic review. J Clin Periodontol 36:1048–1058. doi: 10.1111/j.1600-051X.2009.01482.x PubMedCrossRefGoogle Scholar
  40. 40.
    Simark-Mattsson C, Emilson C-G, Håkansson EG et al (2007) Lactobacillus-mediated interference of mutans streptococci in caries-free vs. caries-active subjects. Eur J Oral Sci 115:308–314. doi: 10.1111/j.1600-0722.2007.00458.x PubMedCrossRefGoogle Scholar
  41. 41.
    Khanafari A, Porgham SH, Ebrahimi MT (2012) Investigation of probiotic chocolate effect on Streptococcus mutans growth inhibition. Jundishapur J Microbiol 5:590–597CrossRefGoogle Scholar
  42. 42.
    Hillman JD, Dzuback AL, Andrews SW (1987) Colonization of the human oral cavity by a Streptococcus mutans mutant producing increased bacteriocin. J Dent Res 66:1092–1094PubMedCrossRefGoogle Scholar
  43. 43.
    Glavina D, Gorseta K, Skrinjarić I et al (2012) Effect of LGG yoghurt on Streptococcus mutans and Lactobacillus spp. salivary counts in children. Coll Antropol 36:129–132PubMedGoogle Scholar
  44. 44.
    Chuang L-C, Huang C-S, Ou-Yang L-W, Lin S-Y (2011) Probiotic Lactobacillus paracasei effect on cariogenic bacterial flora. Clin Oral Investig 15:471–476. doi: 10.1007/s00784-010-0423-9 PubMedCentralPubMedCrossRefGoogle Scholar
  45. 45.
    Stecksen-Blicks C, Sjostrom I, Twetman S (2009) 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 Res 43:374–381PubMedCrossRefGoogle Scholar
  46. 46.
    Taipale T, Pienihäkkinen K, Salminen S et al (2012) 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 Res 46:69–77. doi: 10.1159/000335567 PubMedCrossRefGoogle Scholar
  47. 47.
    Taipale T, Pienihäkkinen K, Alanen P et al (2013) Administration of Bifidobacterium animalis subsp. lactis BB-12 in early childhood: a post-trial effect on caries occurrence at four years of age. Caries Res 47:364–372. doi: 10.1159/000348424 PubMedCrossRefGoogle Scholar
  48. 48.
    Cildir SK, Germec D, Sandalli N et al (2009) Reduction of salivary mutans streptococci in orthodontic patients during daily consumption of yoghurt containing probiotic bacteria. Eur J Orthod 31:407–411PubMedCrossRefGoogle Scholar
  49. 49.
    Marttinen A, Haukioja A, Karjalainen S et al (2011) Short-term consumption of probiotic lactobacilli has no effect on acid production of supragingival plaque. Clin Oral Investig. doi: 10.1007/s00784-011-0584-1 PubMedGoogle Scholar
  50. 50.
    Montalto M, Vastola M, Marigo L et al (2004) Probiotic treatment increases salivary counts of lactobacilli: a double-blind, randomized, controlled study. Digestion 69:53–56. doi: 10.1159/000076559 PubMedCrossRefGoogle Scholar
  51. 51.
    Caglar E, Kuscu OO, Cildir SK et al (2008) A probiotic lozenge administered medical device and its effect on salivary mutans streptococci and lactobacilli. Int J Paediatr Dent Br Paedodontic Soc Int Assoc Dent Child 18:35–39. doi: 10.1111/j.1365-263X.2007.00866.x Google Scholar
  52. 52.
    Lexner MO, Blomqvist S, Dahlén G, Twetman S (2010) Microbiological profiles in saliva and supragingival plaque from caries-active adolescents before and after a short-term daily intake of milk supplemented with probiotic bacteria—a pilot study. Oral Health Prev Dent 8:383–388PubMedGoogle Scholar
  53. 53.
    Sinkiewicz G, Cronholm S, Ljunggren L et al (2010) Influence of dietary supplementation with Lactobacillus reuteri on the oral flora of healthy subjects. Swed Dent J 34:197–206PubMedGoogle Scholar
  54. 54.
    Caglar E, Kavaloglu SC, Kuscu OO et al (2007) Effect of chewing gums containing xylitol or probiotic bacteria on salivary mutans streptococci and lactobacilli. Clin Oral Investig 11:425–429. doi: 10.1007/s00784-007-0129-9 PubMedCrossRefGoogle Scholar
  55. 55.
    Petersson LG, Magnusson K, Hakestam U et al (2011) Reversal of primary root caries lesions after daily intake of milk supplemented with fluoride and probiotic lactobacilli in older adults. Acta Odontol Scand 69:321–327. doi: 10.3109/00016357.2011.568962 PubMedCrossRefGoogle Scholar
  56. 56.
    Juneja A, Kakade A (2012) Evaluating the effect of probiotic containing milk on salivary mutans streptococci levels. J Clin Pediatr Dent 37:9–14PubMedGoogle Scholar
  57. 57.
    Aminabadi NA, Erfanparast L, Ebrahimi A, Oskouei SG (2011) Effect of chlorhexidine pretreatment on the stability of salivary lactobacilli probiotic in six- to twelve-year-old children: a randomized controlled trial. Caries Res 45:148–154. doi: 10.1159/000325741 PubMedCrossRefGoogle Scholar
  58. 58.
    Burton JP, Drummond BK, Chilcott CN et al (2013) The influence of the probiotic Streptococcus salivarius M18 on indices of dental health in children: a randomised double-blind placebo-controlled trial. J Med Microbiol. doi: 10.1099/jmm.0.056663-0 PubMedGoogle Scholar
  59. 59.
    Keller MK, Hasslöf P, Dahlén G et al (2012) Probiotic supplements (Lactobacillus reuteri DSM 17938 and ATCC PTA 5289) do not affect regrowth of mutans streptococci after full-mouth disinfection with chlorhexidine: a randomized controlled multicenter trial. Caries Res 46:140–146. doi: 10.1159/000337098 PubMedCrossRefGoogle Scholar
  60. 60.
    Nikawa H, Makihira S, Fukushima H et al (2004) Lactobacillus reuteri in bovine milk fermented decreases the oral carriage of mutans streptococci. Int J Food Microbiol 95:219–223PubMedCrossRefGoogle Scholar
  61. 61.
    Caglar E, Sandalli N, Twetman S et al (2005) Effect of yogurt with Bifidobacterium DN-173 010 on salivary mutans streptococci and lactobacilli in young adults. Acta Odontol Scand 63:317–320PubMedCrossRefGoogle Scholar
  62. 62.
    Caglar E, Cildir SK, Ergeneli S et al (2006) Salivary mutans streptococci and lactobacilli levels after ingestion of the probiotic bacterium Lactobacillus reuteri ATCC 55730 by straws or tablets. Acta Odontol Scand 64:314–318. doi: 10.1080/00016350600801709 PubMedCrossRefGoogle Scholar
  63. 63.
    Cogulu D, Topaloglu-Ak A, Caglar E et al (2010) Potential effects of a multistrain probiotic-kefir on salivary Streptococcus mutans and Lactobacillus spp. J Dent Sci 5:144–149. doi: 10.1016/S1991-7902(10)60021-9 CrossRefGoogle Scholar
  64. 64.
    Cildir S, Sandalli N, Alp F, Caglar E (2011) A novel delivery system of probiotic drop and its effect on dental caries risk factors in cleft lip/palate children. Cleft Palate Craniofac J Off Publ Am Cleft Palate Craniofac Assoc. doi: 10.1597/10-035 Google Scholar
  65. 65.
    Jindal G, Pandey RK, Agarwal J, Singh M (2011) A comparative evaluation of probiotics on salivary mutans streptococci counts in Indian children. Eur Arch Paediatr Dent Off J Eur Acad Paediatr Dent 12:211–215CrossRefGoogle Scholar
  66. 66.
    Singh RP, Damle SG, Chawla A (2011) Salivary mutans streptococci and lactobacilli modulations in young children on consumption of probiotic ice-cream containing Bifidobacterium lactis Bb12 and Lactobacillus acidophilus La5. Acta Odontol Scand 69:389–394PubMedCrossRefGoogle Scholar
  67. 67.
    Mortazavi S, Akhlaghi N (2012) Salivary Streptococcus mutans and Lactobacilli levels following probiotic cheese consumption in adults: a double blind randomized clinical trial. J Res Med Sci 17:57–66PubMedCentralPubMedGoogle Scholar
  68. 68.
    Keller MK, Twetman S (2012) Acid production in dental plaque after exposure to probiotic bacteria. BMC Oral Health. doi: 10.1186/1472-6831-12-44 PubMedCentralPubMedGoogle Scholar
  69. 69.
    Nase L, Hatakka K, Savilahti E et al (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 35:412–420PubMedCrossRefGoogle Scholar
  70. 70.
    Caglar E, Kuscu OO, Selvi Kuvvetli S et al (2008) Short-term effect of ice-cream containing Bifidobacterium lactis Bb-12 on the number of salivary mutans streptococci and lactobacilli. Acta Odontol Scand 66:154–158. doi: 10.1080/00016350802089467 PubMedCrossRefGoogle Scholar
  71. 71.
    Sudhir R, Praveen P, Anantharaj A, Venkataraghavan K (2012) Assessment of the effect of probiotic curd consumption on salivary pH and streptococcus mutans counts. Niger Med J J Niger Med Assoc 53:135–139. doi: 10.4103/0300-1652.104382 CrossRefGoogle Scholar
  72. 72.
    Caufield PW, Dasanayake AP, Li Y (2001) The antimicrobial approach to caries management. J Dent Educ 65:1091–1095PubMedGoogle Scholar
  73. 73.
    Aguilera Galaviz LA, Premoli G, Gonzalez A, Rodriguez RA (2005) Caries risk in children: determined by levels of mutans streptococci and Lactobacillus. J Clin Pediatr Dent 29:329–333PubMedGoogle Scholar
  74. 74.
    Parisotto TM, Steiner-Oliveira C, Silva CM et al (2010) Early childhood caries and mutans streptococci: a systematic review. Oral Health Prev Dent 8:59–70PubMedGoogle Scholar
  75. 75.
    Thenisch NL, Bachmann LM, Imfeld T et al (2006) Are mutans streptococci detected in preschool children a reliable predictive factor for dental caries risk? A systematic review. Caries Res 40:366–374. doi: 10.1159/000094280 PubMedCrossRefGoogle Scholar
  76. 76.
    Gross EL, Beall CJ, Kutsch SR et al (2012) Beyond Streptococcus mutans: dental caries onset linked to multiple species by 16S rRNA community analysis. PloS One 7:e47722. doi: 10.1371/journal.pone.0047722 PubMedCentralPubMedCrossRefGoogle Scholar
  77. 77.
    Tanabe Y, Park JH, Tinanoff N et al (2006) Comparison of chairside microbiological screening systems and conventional selective media in children with and without visible dental caries. Pediatr Dent 28:363–368PubMedGoogle Scholar
  78. 78.
    Davenport ES, Day S, Hardie JM, Smith JM (1992) A comparison between commercial kits and conventional methods for enumeration of salivary mutans streptococci and lactobacilli. Community Dent Health 9:261–271PubMedGoogle Scholar
  79. 79.
    Karjalainen S, Söderling E, Pienihäkkinen K (2004) Validation and inter-examiner agreement of mutans streptococci levels in plaque and saliva of 10-year-old children using simple chair-side tests. Acta Odontol Scand 62:153–157. doi: 10.1080/00016350410001559 PubMedCrossRefGoogle Scholar
  80. 80.
    Pham LC, Hoogenkamp MA, Exterkate RAM et al (2011) Effects of Lactobacillus rhamnosus GG on saliva-derived microcosms. Arch Oral Biol 56:136–147PubMedCrossRefGoogle Scholar
  81. 81.
    Hasslöf P, West CE, Karlsson Videhult F et al (2013) Early intervention with probiotic Lactobacillus paracasei F19 has no long-term effect on caries experience. Caries Res 47:559–565. doi: 10.1159/000350524 PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Isabelle Laleman
    • 1
  • Valentine Detailleur
    • 1
  • Dagmar Else Slot
    • 2
  • Vera Slomka
    • 1
  • Marc Quirynen
    • 1
  • Wim Teughels
    • 1
  1. 1.Department of Oral Health Sciences, KU Leuven & DentistryUniversity Hospitals LeuvenLeuvenBelgium
  2. 2.Department of PeriodontologyAcademic Centre for Dentistry Amsterdam (ACTA)AmsterdamThe Netherlands

Personalised recommendations