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Probiotics as an Adjunct Therapy for the Treatment of Halitosis, Dental Caries and Periodontitis

  • Mariela BustamanteEmail author
  • B. Dave Oomah
  • Yohanna Mosi-Roa
  • Mónica Rubilar
  • César Burgos-Díaz
Article

Abstract

Probiotics and prebiotics are popular among consumers worldwide as natural approaches to prevent gastrointestinal diseases. The effects of their consumption on the gastrointestinal system have been extensively investigated. Recently, the efficacy of probiotics and prebiotics has been evaluated against naturally developing microbiome imbalance in the human body, such as in the oral cavity, skin, female urogenital tract, and respiratory tract. This review examines the scientific data related to the effects of probiotics on the treatment of diseases occurring in the oral cavity. Probiotics can effectively prevent and treat some infectious diseases in the oral cavity, such as halitosis and periodontitis, and can reduce the development of dental caries and the concentration of harmful bacteria, according to clinical studies. The results of this meta-analysis also suggest the use of probiotics to treat halitosis and periodontitis. However, the evidence may be inconclusive due in part to the use of a wide range of probiotics, non-standardized study design, small population size, poor quality reports, and inconsistent data. Therefore, future studies should homogenize terms and definitions for primary and secondary outcomes, increase the number of volunteers/patients in in vitro tests and clinical studies, and include an evaluation of the combined use of pre- and probiotics.

Keywords

Probiotics Oral cavity Oral diseases Oral health 

Notes

Funding information

This research was supported by CONICYT through FONDECYT project 11160249.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    FAO/WHO (2001) Health and nutritional properties of Probiotics in food including powder milk with live lactic acid bacteria. Report of a Joint FAO/WHO Expert Consultation on Evaluation of Health and Nutritional Properties of Probiotics in Food including Powder Milk with Live lactic acid bacteria, Córdoba, ArgentinaGoogle Scholar
  2. 2.
    Gibson GR, Roberfroid MB (1995) Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr 125:1401–1412CrossRefGoogle Scholar
  3. 3.
    Gibson GR, Hutkins R, Sanders ME, Prescott SL, Reimer RA, Salminen SJ, Scott K, Stanton C, Swanson KS, Cani PD, Verbeke K, Reid G (2017) 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 14:491–502PubMedGoogle Scholar
  4. 4.
    Pineiro M, Asp NG, Reid G, Macfarlane S, Morelli L, Brunser O, Touhy K (2008) FAO technical meeting on prebiotics. J Clin Gastroenterol 42:S156–S159CrossRefGoogle Scholar
  5. 5.
    MarketsandMarkets (2017) Probiotics market by application (functional food & beverages (dairy, non-dairy beverages, baked goods, meat, cereal), dietary supplements, animal feed), source (bacteria, yeast), form (dry, liquid), end user (human, animal), and Region - Forecast to 2022. https://www.marketsandmarkets.com/Market-Reports/probiotic-market-advanced-technologies-and-global-market-69. Accessed 01.06.18
  6. 6.
    MarketsandMarkets (2018) Prebiotic ingredients market by type (oligosaccharides, inulin, and polydextrose), application (food & beverages, dietary supplements, and animal feed), source (roots, grains, and vegetables), and Region - Global Forecast to 2023. https://www.marketsandmarkets.com/Market-Reports/prebiotics-ingredients-market-219677001. Accessed 01.06.18
  7. 7.
    Grand View Research (2018) Prebiotics market size, share & trend analysis report by ingredients (FOS, inulin, GOS, MOS), by application (Food and beverages, dietary supplements, animal feed), and segment forecasts, 2018–2024. Available at https://www.grandviewresearch.com/industry-analysis/prebiotics-market. Accessed 09.05.18
  8. 8.
    Grand View Research (2018) Probiotics market size, share & trends analysis report by application (Food & beverages, dietary supplements, animal feed), by end-use, by region, and segment forecast, 2018–2024. Available at https://www.grandviewresearch.com/industry-analysis/probiotics-market. Accessed 09.05.18
  9. 9.
    Likotrafiti E, Rhoades J (2016) Chapter 32. Probiotics, prebiotics, synbiotics, and foodborne illness. In: Watson RR, Preedy VR (eds) Bioactive foods in health promotion: probiotics, prebiotics, and synbiotics. p 469–476.  https://doi.org/10.1016/B978-0-12-802189-7.00032-0
  10. 10.
    Köhler GA, Assefa S, Reid G (2012) Probiotic interference of Lactobacillus rhamnosus GR-1 and Lactobacillus reuteri RC-14 with the opportunistic fungal pathogen Candida albicans. Infect Dis Obstet Gynecol 2012:1–14Google Scholar
  11. 11.
    Morales A, Carvajal P, Silva N, Hernandez M, Godoy C, Rodriguez G, Caballero R, Garcia-Sesnich J, Hoare A, Diaz PI, Gamonal J (2016) Clinical effects of Lactobacillus rhamnosus in non-surgical treatment of chronic periodontitis: a randomized placebo controlled trial with 1-year follow-up. J Periodontol 87:944–952CrossRefGoogle Scholar
  12. 12.
    Wu KG, Li TH, Peng HJ (2012) Lactobacillus salivarius plus fructo-oligosaccharide is superior to fructo-oligosaccharide alone for treating children with moderate to severe atopic dermatitis: a double-blind, randomized, clinical trial of efficacy and safety. Br J Dermatol 166:129–136CrossRefGoogle Scholar
  13. 13.
    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 2010:1–10Google Scholar
  14. 14.
    Yang L, Chen T, Izard J, Tanner AC, Wade WG, Paster BJ, Dewhirst FE (2014) The human oral microbiome database: updates and new features. 43rd Annual Meeting & Exhibition of the American Association for Dental Research. Charlotte, N.C., USAGoogle Scholar
  15. 15.
    Aas JA, Paster BJ, Stokes LN, Olsen I, Dewhirst FE (2005) Defining the normal bacterial flora of the oral cavity. J Clin Microbiol 43:5721–5732CrossRefGoogle Scholar
  16. 16.
    Asakawa M, Takeshita T, Futura M, Kagemaya S, Takeuchi K, Hata J, Ninomiya T, Yamashita Y (2018) Tongue microbiota and oral health status in community-dwelling elderly adults. mSphere.  https://doi.org/10.1128/mSphere.00332-18
  17. 17.
    Moynihan PJ, Kelly SAM (2014) Effect on caries of restricting sugars intake: systematic review to inform WHO guidelines. J Den Res 93:8–18CrossRefGoogle Scholar
  18. 18.
    Palmer RJ (2014) Composition and development of oral bacterial communities. Periodontol 2000:20–39.  https://doi.org/10.1111/j.1600-0757.2012.00453.x CrossRefGoogle Scholar
  19. 19.
    Bustamante M, Villarroel M, Rubilar M, Shene C (2015) Lactobacillus acidophilus La-05 encapsulated by spray drying: effect of mucilage and protein from flaxseed (Linum usitatissimum L.). LWT Food Sci Technol 62:1162–1168CrossRefGoogle Scholar
  20. 20.
    Collins MD, Gibson GR (1999) Probiotics, prebiotics, and synbiotics: approaches for modulating the microbial ecology of the gut. Am J Clin Nutr 69:1052S–1057SCrossRefGoogle Scholar
  21. 21.
    Holzapfel WH, Haberer P, Geisen R, Björkroth J, Schillinger U (2001) Taxonomy and important features of probiotic microorganisms in food and nutrition. Am J Clin Nutr 73:365S–373SCrossRefGoogle Scholar
  22. 22.
    Markowiak P, Śliżewska K (2017) Effects of probiotics, prebiotics, and synbiotics on human health. Nutrients.  https://doi.org/10.3390/nu9091021
  23. 23.
    Parčina Amižić IP, Cigić L, Gavić L, Radić M, Biočina Lukenda D, Tonkić M, Goić Barišić I (2017) Antimicrobial efficacy of probiotic-containing toothpastes: an in vitro evaluation. Med Glas (Zenica) 14(1):139–144.  https://doi.org/10.17392/870-16 CrossRefGoogle Scholar
  24. 24.
    Bustamante M, Oomah BD, Rubilar M, Shene C (2017) Effective Lactobacillus plantarum and Bifidobacterium infantis encapsulation with chia seed (Salvia hispanica L.) and flaxseed (Linum usitatissimum L.) mucilage and soluble protein by spray drying. Food Chem 216:97–105CrossRefGoogle Scholar
  25. 25.
    Endres JR, Clewell A, Jade KA, Farber T, Hauswirth J, Schauss AG (2009) Safety assessment of a proprietary preparation of a novel probiotic, Bacillus coagulans, as a food ingredient. Food Chem Toxicol 47:1231–1238CrossRefGoogle Scholar
  26. 26.
    FAO/WHO (2002) Guidelines for the evaluation of probiotics in food, food and agriculture. Organization of the United Nations/World Health Organization, LondonGoogle Scholar
  27. 27.
    Prado FC, Parada JL, Pandey A, Soccol CR (2008) Trends in non-dairy probiotic beverages. Food Res Int 41:111–123CrossRefGoogle Scholar
  28. 28.
    Sanders ME (2008) Probiotics: definitions, sources, selections, and uses. Clin Infect Dis 46:S58–S61CrossRefGoogle Scholar
  29. 29.
    Saarela M (2017) Recent development in the probiotic research and market. Available http://www.global-engage.com/life-science/probiotics-market-trends-and-opportunities-2017/. Accessed 09.05.18
  30. 30.
    Vasiljevic T, Shah N (2008) Probiotics—from Metchnikoff to bioactives. Int Dairy J 18:714–728CrossRefGoogle Scholar
  31. 31.
    Roy D (2005) Technological aspects related to the use of bifidobacteria in dairy products. Lait 85:39–56CrossRefGoogle Scholar
  32. 32.
    Shah NP (2007) Functional cultures and health benefits. Int Dairy J 17:1262–1277CrossRefGoogle Scholar
  33. 33.
    Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, Morelli L, Canani RB, Flint HJ, Salminen S, Calder PC, Sanders ME (2014) 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 11:506–514CrossRefGoogle Scholar
  34. 34.
    Aymerich T, Artigas MG, Monfort JM, Hugas M (2000) Effect of sausage ingredients and additives on the production of enterocins A and B by Enterococcus faecium CTC492. Optimization of in vitro production and anti-listerial effect in dry fermented sausages. J Appl Microbiol 88:686–694CrossRefGoogle Scholar
  35. 35.
    Çaglar E, Cildir SK, Ergeneli S, Sandalli N, Twetman S (2006) Salivarius mutans streptococci and lactobacilli levels after ingestion of the probiotic bacterium Lactobacillus reuteri ATCC 55739 by straws or tables. Acta Odontol Scand 64:314–318CrossRefGoogle Scholar
  36. 36.
    Jyoti BD, Suresh AK, Venkatesh KV (2003) Diacetyl production and growth of Lactobacillus rhamnosus on multiple substrates. World J Microbiol Biotechnol 19:509–514CrossRefGoogle Scholar
  37. 37.
    Mu Q, Tavella VJ, Luo XM (2018) Role of Lactobacillus reuteri in human health and diseases. Front Microbiol 9:1–17CrossRefGoogle Scholar
  38. 38.
    Reid G, Burton J (2002) Use of Lactobacillus to prevent infection by pathogenic bacteria. Microbes Infect 4:319–324CrossRefGoogle Scholar
  39. 39.
    Silva J, Carvalho AS, Teixeira P, Gibbs PA (2002) Bacteriocin productin by spray-dried lactic acid bacteria. Lett Appl Microbiol 34:77–81CrossRefGoogle Scholar
  40. 40.
    Tachedjian G, Aldunate M, Bradshaw CS, Cone RA (2017) The role of lactic acid production by probiotic Lactobacillus species in vaginal health. Res Microbiol 168:782–792CrossRefGoogle Scholar
  41. 41.
    Dover SE, Aroutcheva AA, Faro S, Chikindas ML (2008) Natural antimicrobials and their role in vaginal health: a short review. Int J Probiotics Prebiotics 3:219–230PubMedPubMedCentralGoogle Scholar
  42. 42.
    Hertzberger R, Arents J, Dekker HL, Pridmore RD, Gysler C, Kleerebezem M, de Mattos MJ (2014) H2O2 production in species of the Lactobacillus acidophilus group: a central role for a novel NADH-dependent flavin reductase. Appl Environ Microbiol 80:2229–2239CrossRefGoogle Scholar
  43. 43.
    Gillor O, Nigro LM, Riley MA (2005) Genetically engineered bacteriocins and their potential as the next generation of antimicrobials. Curr Pharm Des 11:1067–1075CrossRefGoogle Scholar
  44. 44.
    Barrons R, Tassone D (2008) Use of Lactobacillus probiotics for bacterial genitourinary infections in women: a review. Clin Ther 30:453–468CrossRefGoogle Scholar
  45. 45.
    Velraeds MMC, van der Mei HC, Reid G, Busscher HJ (1996) Inhibition of initial adhesion of uropathogenic Enterococcus faecalis by biosurfactants from Lactobacillus isolates. Appl Environ Microbiol 62:1958–1963PubMedPubMedCentralGoogle Scholar
  46. 46.
    Pandey KR, Naik SR, Vakil BV (2015) Probiotics, prebiotics and synbiotics—a review. J Food Sci Technol 52:7577–7587CrossRefGoogle Scholar
  47. 47.
    Sekhon BS, Jairath S (2010) Prebiotics, probiotics and synbiotics: an overview. J Pharm Educ Res 1:13–36Google Scholar
  48. 48.
    Mahasneh SA, Mahasneh AM (2017) Probiotics: a promising role in dental health. Dentistry Journal 5:1–10CrossRefGoogle Scholar
  49. 49.
    Agarwal G, Ingle NA, Kaur N, Yadav P, Ingle E, Charania Z (2015) Probiotics and oral health: a review. J Int Oral Health 7:133–136Google Scholar
  50. 50.
    Haukioja A (2010) Probiotics and oral health. Eur J Dent 4:348–355PubMedPubMedCentralGoogle Scholar
  51. 51.
    Pandya D (2016) Benefits of probiotics in oral cavity—A detailed review. Ann Int Med Den Res 2(5):DE10–DE17.  https://doi.org/10.21276/aimdr.2016.2.5.DE3 CrossRefGoogle Scholar
  52. 52.
    Mohanty R, Nazareth B, Shrivastava N (2012) The potential role if probiotics in periodontal health. Rev Sul-bras Odontol 9(1):85–88. Available at https://www.redalyc.org/articulo.oa?id=153023690012. Accessed 08 Feb 2018
  53. 53.
    Keller MK, Bardow A, Jensdottir T, Lykkeaa J, Twetman S (2012) Effect of chewing gums containing the probiotic bacterium Lactobacillus reuteri on oral malodour. Acta Odontol Scand 70:246–250CrossRefGoogle Scholar
  54. 54.
    Suzuki N, Yoneda M, Tanake K, Fujimoto A, Iha K, Seno K, Yamada K, Iwamoto T, Masuo Y, Hirofuji T (2014) Lactobacillus salivarius WB21-containing tablets for the treatment of oral malodor: a double-blind, randomized, placebo-controlled. Oral Surg Oral Med Oral Pathol Oral Radiol 117:462–470CrossRefGoogle Scholar
  55. 55.
    Penala S, Kalakonda B, Pathakota KR, Jayakumar A, Koppolu P, Lakshmi BV, Pandey R, Mishra A (2016) Efficacy of local use of probiotics as an adjunct to scaling and root planing in chronic periodontitis and halitosis: a randomized controlled trial. J Res Pharm Pract 5:86–93CrossRefGoogle Scholar
  56. 56.
    Keller MK, Nøhr Larsen I, Karlsson I, Twetman S (2014) Effect of tablets containing probiotic bacteria (Lactobacillus reuteri) on early caries lesions in adolescents: a pilot study. Benefic Microbes 5:403–407CrossRefGoogle Scholar
  57. 57.
    Stensson M, Koch G, Coric S, Abrahamsson TR, Jenmalm MC, Birkhed D, Wendt LK (2014) Oral administration of Lactobacillus reuteri during the first year of life reduces caries prevalence in the primary dentition at 9 years of age. Caries Res 48:111–117CrossRefGoogle Scholar
  58. 58.
    Rodríguez G, Ruiz B, Faleiros S, Vistoso A, Marró ML, Sánchez J, Urzúam I, Cabello R (2016) Probiotic compared with standard milk for high-caries children: a cluster randomized trial. J Dent Res 95:402–407CrossRefGoogle Scholar
  59. 59.
    Iwasaki K, Maeda K, Hidaka K, Nemoto K, Hirose Y, Deguchi S (2016) Daily intake of heat-killed Lactobacillus plantarum L-137 decreases the probing depth in patients undergoing supportive periodontal therapy. Oral Health Preve Dent 14:207–214Google Scholar
  60. 60.
    Alanzi A, Honkala S, Honkala E, Varghese A, Tolvanen M, Söderling E (2018) Effect of Lactobacillus rhamnosus and Bifidobacterium lactis on gingival health, dental plaque, and periodontopathogens in adolescents: a randomised placebo-controlled clinical trial. Benefic Microbes 9:593–602CrossRefGoogle Scholar
  61. 61.
    Persson S, Edlund MB, Claesson R, Carlsson J (1990) The formation of hydrogen sulfide and methyl mercaptan by oral bacteria. Oral Microbiol Immunol 5:195–201CrossRefGoogle Scholar
  62. 62.
    Teughels W, Newman MG, Coucke W, Haffajee AD, Van Der Mei HC, Haake SK, Schepers E, Cassiman JJ, Van Eldere J, van Steenberghe D, Quirynen M (2007) Guiding periodontal pocket recolonization: a proof of concept. J Dent Res 86:1078–1082CrossRefGoogle Scholar
  63. 63.
    Kazor CE, Mitchell PM, Lee AM, Stokes LN, Loesche WJ, Dewhirst FE, Paster BJ (2003) Diversity of bacterial populations on the tongue dorsa of patients with halitosis and healthy patients. J Clil Microbiol 41:558–563CrossRefGoogle Scholar
  64. 64.
    Yoshida Y, Negishi M, Amano A, Oho T, Nakano Y (2003) Differences in the beta C-S lyase activities of viridians group streptococci. Biochem Biophys Res Commun 300:55–60CrossRefGoogle Scholar
  65. 65.
    Featherstone JDB (2004) The continuum of dental caries-evidence for a dynamic disease process. J Dent Res 83 Special Issue C:C39–C42CrossRefGoogle Scholar
  66. 66.
    Cereceda MA, Faleiros S, Ormeño A, Pinto M, Tapia R, Díaz C, Garcia H (2010) Prevalencia de caries en alumnos de educación básica y su asociación con el estado nutricional. Rev Chil Pediatr 8:28–36Google Scholar
  67. 67.
    Petersen PE, Bourgeois D, Ogawa H, Estupinan-Day S, Ndiaye C (2005) The global burden of oral diseases and risks to oral health. Bull World Health Organ 83:661–669PubMedPubMedCentralGoogle Scholar
  68. 68.
    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 35:412–420CrossRefGoogle Scholar
  69. 69.
    Ahola AJ, Yli-Knuuttila H, Suomalainen T, Poussa T, Ahlstrom A, Meurman JH, Korpela R (2002) Short-term consumption of probiotic-containing cheese and its effect on dental caries risk factors. Arch Oral Biol 47:799–804CrossRefGoogle Scholar
  70. 70.
    Yli-Knuuttila H, Snäll J, Kari K, Meurman JH (2006) Colonization of Lactobacillus rhamnosus GG in the oral cavity. Oral Microbiol Immunol 21:129–131CrossRefGoogle Scholar
  71. 71.
    Schwendicke F, Korte F, Dorfer CE, Kneist S, El-Sayed KF, Paris S (2017) Inhibition of Streptococcus mutans growth and biofilm formation by probiotics in vitro. Caries Res 51:87–95CrossRefGoogle Scholar
  72. 72.
    Nunpan S, Suwannachart C, Wayakanon K (2017) The inhibition of dental caries pathogen by using prebiotic and probiotic combination. JDAT DFCT Supplement Issue 67:31–38Google Scholar
  73. 73.
    Mujica Troncoso C, Castillo-Ruiz M, Daille LK, Fuentevilla IA, Bittner M (2010) Co-detection of periodontal pathogens in Chilean patients with chronic periodontitis. Rev Clin Periodoncia, Implantol Rehabil Oral 3:118–122CrossRefGoogle Scholar
  74. 74.
    Alkaya B, Laleman I, Keceli S, Ozcelik O, Cenk Haytac M, Teughels W (2016) Clinical effects of probiotics containing Bacillus species on gingivitis: a pilot randomized controlled trial. J Periodontal Res 52:497–504.  https://doi.org/10.1111/jre.12415 CrossRefPubMedGoogle Scholar
  75. 75.
    Yoo IL, Shin IS, Jeon JG, Yang YM, Kim JG, Lee DW (2017) The effect of probiotcs on halitosis: a systematic review and meta-analysis. Probiotics Antimicrob Proteins.  https://doi.org/10.1007/s12602-017-9351-1
  76. 76.
    Gruner D, Paris S, Schwendicke F (2016) Probiotics for managing caries and periodontitis: systematic review and meta-analysis. J Dent 48:16–25.  https://doi.org/10.1016/j.jdent.2016.03.002 CrossRefPubMedGoogle Scholar
  77. 77.
    Martin-Cabezas R, Davideau J-L, Tenenbaum H, Huck O (2016) Clinical efficacy of probiotics as an adjunctive therapy to non-surgical periodontal treatment of chronic periodontitis: a systematic review and meta-analysis. J Clin Periodontol 43:520–530CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Center of Food Biotechnology and Bioseparations, Scientific and Technological Bioresource Nucleus, BIOREN, and Department of Chemical EngineeringUniversidad de La FronteraTemucoChile
  2. 2.National Bioproducts and Bioprocesses Program, Pacific Agri-Food Research CentreAgriculture and Agri-Food CanadaSummerlandCanada
  3. 3.Scientific and Technological Bioresource Nucleus, BIORENUniversidad de La FronteraTemucoChile
  4. 4.Agriaquaculture Nutritional Genomic Center, CGNATemucoChile

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