PROBIOTICS AND THEIR RELATIONSHIP WITH CARIES CONTROL. A TOPIC REVIEW

Angarita-Díaz, María Del Pilar; Angarita-Díaz, María Del Pilar

doi:10.17533/udea.rfo.v28n1a10

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Revista Facultad de Odontología Universidad de Antioquia

Print version ISSN 0121-246X

Rev Fac Odontol Univ Antioq vol.28 no.1 Medellín July/Dec. 2016

https://doi.org/10.17533/udea.rfo.v28n1a10

Original article

PROBIOTICS AND THEIR RELATIONSHIP WITH CARIES CONTROL. A TOPIC REVIEW^*

María Del Pilar Angarita-Díaz¹

^¹ PhD in Biotechnology. Professor of Oral Microbiology. GIOMET Researcher. School of Dentistry, Universidad Cooperativa de Colombia, Villavicencio. E-mail: maria.angaritad@campusucc.edu.co

ABSTRACT

The development of studies related to the human oral microbiome, as well as the applied sciences and techniques to investigate it, have helped reconsidering our understanding of tooth decay as an endogenous infection caused by a conglomerate of microorganisms. In addition to identifying the great diversity of microorganisms involved in carious processes, similar studies in healthy oral cavity have also been conducted, as well as analysis of the interactions between microorganisms and the host. The results are paving the way to implementing biotechnology strategies to interrupt the onset and progression of the disease, and in this sense probiotics are a promising tool. Probiotics are beneficial microorganisms that once in contact with the oral cavity modify the microbial interaction favoring homeostasis. A literature review was conducted using various databases (PubMed, ScienceDirect, and Google Scholar), focusing on probiotics as a strategy for caries control, based on their function in the oral cavity; this includes some of the studies conducted so far as well as the description of features of the bacterial strains most commonly studied and the ones recently isolated. The article concludes by explaining the ideal features that bacterial strains should have to be efficient as probiotics in the oral cavity.

Key words: probiotics; dental caries; microbiota; homeostasis

RESUMEN.

El desarrollo de estudios relacionados con el microbioma oral humano, así como las ciencias y técnicas aplicadas para investigarlo, han permitido replantear el entendimiento de la caries como una infección endógena causada por un consorcio de microorganismos. Además de identificar la gran diversidad de microorganismos implicados en los procesos cariosos, también se han realizado estudios similares en cavidad oral sana, y análisis de las interacciones entre los microorganismos y el hospedador. Los resultados están abriendo paso a la viabilidad de implementar estrategias biotecnológicas que buscan interrumpir el inicio y la progresión de la enfermedad, y en este sentido los probióticos son una herramienta prometedora. Los probióticos son microorganismos benéficos que al entrar en contacto con la cavidad oral modifican la interacción microbiana a favor de una homeostasis. Utilizando diferentes bases de datos (PubMed, ScienceDirect y Google Académico) se realizó la revisión de literatura sobre los probióticos como una estrategia para el control de la caries, mediante el fundamento de su función en cavidad oral, así como algunos de los estudios realizados hasta el momento y la descripción de las características de las cepas bacterianas más estudiadas y las aisladas recientemente. El artículo concluye con la sustentación de las características ideales que deberían tener las cepas bacterianas para que sean eficientes como probióticos de cavidad oral.

Palabras clave: probióticos; caries dental; microbiota; homeostasis.

INTRODUCTION

It has been 36 years since the World Health Organization (WHO) first set forth global goals for oral health and there is still much work to be done. In 1989, the same organization recommended promoting oral health as a public health issue.¹⁾ Consequently, many countries set up strategies to reduce oral diseases. Although according to global reports²⁾ public health efforts have been effective in controlling oral diseases, dental caries remains one of the most prevalent chronic diseases.³⁾ Dental caries may affect basic functions like food intake and nutrition, and can influence the psycho-social life of patients.⁴⁾ It can also produce tooth loss and serious diseases such as bacterial endocarditis.⁵

In Colombia, the most recent Estudio Nacional de Salud Bucal ENSAB IV (2014) showed a decrease in caries prevalence compared to the previous report, especially in the population aged 12 years (going from 57% to 37%) and in the population aged 20 to 34 years (from 75% to 53%). Despite these results, caries remains the most frequent disease in the earlier years, since 33.3% of children aged 1, 3 and 5 years already have experience of this disease, with a prevalence of 5.9%, 43.7% and 52.2% respectively. This shows the need for strategies to complement the existing ones, to achieve the eradication or a greater control of this disease.⁶

Dental caries is a disease caused by a shift in pH balance, resulting in the formation of a biofilm composed mainly of cariogenic microflora. The interaction between this microflora and host factors conditions the deceleration or acceleration of the disease.⁷⁾⁽⁸⁾⁽⁹

Imbalance or dysbiosis of the oral microflora make this disease an endogenous infection, which is not transmissible, as previously believed.¹⁰⁾⁽¹¹⁾ In recent years, several research groups have focused their efforts on the study of oral microbiota,¹²⁾⁽¹³⁾⁽¹⁴⁾ identifying microorganisms involved in cariogenic processes, microorganisms of the healthy oral cavity, their metabolic processes, and the interactions between microorganisms and host. Some biotechnology tools have been tried based on all this research, including probiotics,¹⁵⁾⁽¹⁶⁾ intended for a selective control of the etiological agents of caries and the maintenance of oral homeostasis. The WHO/FAO have accepted the definition of probiotics as “live microorganisms, mainly bacteria, that are safe for human consumption, and when administered in adequate amounts confer a health benefit on the host”.¹⁷

The objective of this topic review is to present probiotics as a strategy for caries control within the context of microbiology and the maintenance of oral homeostasis, as supported by studies conducted on different bacterial strains that comply with this characteristic.

MICROBIOLOGY OF THE ORAL CAVITY

It has been estimated that there are over a thousand different species of bacteria in the oral cavity as potential colonizers.¹⁸⁾⁽¹⁹⁾⁽²⁰⁾⁽²¹⁾⁽²²⁾ Only 280 species have been isolated and identified, but using molecular techniques based on the cloning of gene 16S RNA, about 600 species or phylotypes have been identified.¹⁹⁾ Most of these bacteria are commensals, maintaining the homeostasis of the ecosystem, while others are involved in the development of pathologies.²³⁾⁽²⁴⁾⁽²⁵

The types and proportions of bacteria vary according to the conditions of the oral cavity.¹²⁾⁽¹³⁾⁽¹⁴⁾⁽²⁶⁾ These differences are evident between a healthy oral cavity and one with some kind of pathology, such as caries,²⁷⁾⁽²⁸⁾⁽²⁹, periodontitis, ⁽³⁰⁾ or cancer.³¹⁾⁽³²

The healthy oral cavity is characterized by a microflora dominated by phylum Firmicutes (genus Streptococcus, family Veillonellaceae, genus Granulicatella), Proteobacteria (genus Neisseria, Haemophilus), Actinobacteria (genus Corynebacterium, Rothia, Actinomyces), Bacteroidetes (genus Prevotella, Capnocytophaga, Porphyromona) and Fusobacteria (genus Fusobacterium).³³⁾ In a study based on dental plaque from caries-free children, the authors identified an overabundance of _{^{Streptococcus parasanguinis, Abiotrophia defectiva, Streptococcus mitis, Streptococcus oralis, and Streptococcus sanguinis.(}}³⁴⁾ Other bacterial communities associated with caries-free conditions are Cordiobacterium, Rothia, Kingella Aggregatibacter or Mannheimia, some of which, despite being abundant, are not fully known as they belong to groups that cannot be grown in laboratory.³⁵⁾ The findings of a microbial community related with non-cariogenic status support the idea of using bacteria associated to the healthy status as probiotics to prevent oral diseases.²⁸

Regarding microorganisms in oral cavity with caries, some bacteria found in high proportions in carious lesions were identified during the 1960’s and 1970’s.³⁶⁾ During this period, the importance of Streptococcus mutans and related organisms (S. sobrinus, S. cricetus, S. rattus, S. downii, and S. macacae) was established in the etiology of dental caries.²⁷⁾ Another group of bacteria found in high proportions in carious lesions are the acidogenic and acid tolerant lactobacilli which, like S. mutans, transform fermentable carbohydrates into lactic acid, producing tooth demineralization.³⁷

Today, with the advances in molecular techniques, such as PCR, pyrosequencing and the sequencing of 16S rRNA, as well as with the establishment of genomic databases like the Human Oral Microbiome Database (HOMD)³⁸⁾ and OSU CORE Database,³⁹⁾ more microorganisms are known to be involved in the development of dental caries.¹⁰⁾ The identified bacteria include Selenomonas, Neisseria, a variety of species of Streptococcus, Bifidobacterium, Propionibacterium, Scardoviawiggsiae, Veillonella parvula, Veillonella atypica, Megasphaera micronuciformis, Fusobacterium periodontium, Achromobacterxylosoxidans, and _{^{Actinomycesgerensceriae.(}}²⁷⁾⁽²⁸⁾⁽²⁹

The great progress achieved in characterizing microorganisms in the oral cavity has not been sufficient to develop strategies to control the main pathologies. This is due to the complexity of the ecosystem and because understanding the interactions between these microorganisms and the host is critical.³³⁾ The development of “omics” sciences (metatranscriptomics, proteomics, or metabolomics) has enabled a better understanding of these interactions. In fact, it has been concluded that the detection of metabolic profiles associated with the disease provides more information than the composition of microorganisms.¹⁰⁾ As Simon-Soro et al put it, research must focus on intercepting the functions related with the onset and progression of the disease, such as the strategies to regulate pH, the disruption of molecules of adhesion among microorganisms or between microorganisms and the host, or the use of antimicrobial strategies like probiotics, which modify the microbial interaction and therefore the cariogenic effects.¹⁰

STUDIES WITH PROBIOTICS IN THE ORAL CAVITY

Probiotics are widely studied and used for gastrointestinal problems, such as diarrhea by consumption of antibiotics, infection by Helicobacter pylori, management of intolerance to lactose, irritable colon syndrome, and colitis, as well as for urogenital and allergic diseases, to name just a few.⁴⁰⁾⁽⁴¹⁾⁽⁴²⁾ Their use is also common in daily products in order to improve the functioning of the digestive tract and to boost the immune system.⁴³⁾ Regarding probiotics for oral health, they are less frequently used despite the findings of several studies¹⁹⁾⁽⁴⁴⁾⁽⁴⁶⁾⁽⁴⁷⁾ and the development of commercial products with this component.⁴⁸⁾ Also, probiotics have several mechanisms of action to control oral pathogens (Figure 1)

Figure 1 Possible mechanisms of action of probiotics to pathogens in the oral cavity

Source: by the author based on the literature ⁴⁹⁾⁽⁵⁰⁾⁾

Several bacterial strains have been studied as probiotics, either isolated or in combination, as well as the doses used in studies, intervention periods, populations, experimental designs (Table 1), and routes of administration (Figure 2). The results often include a decrease in S. mutans count in saliva or plaque, but few studies conduct dental clinical examinations to assess treatment (Table 1). This is confirmed by a meta-analysis conducted by Laleman et al in 2013, claiming that the scientific evidence demonstrating caries control is insufficient.¹⁵⁾ However, the results of studies describing the effect of probiotics in the index of carious lesions⁴⁴⁾⁽⁴⁷⁾ or dental plaque⁵¹⁾⁽⁵²⁾ are promising (Table 1).

Table 1 Studies carried out with probiotic bacteria to reduce Streptoccus mutans and control caries

SM: streptococcus of the mutans group Lb: Lactobacillus CFU: Colony-Forming Units: EG: experimental group CG: control group.

_{^{Source: By the author based on the literature (}}¹⁵⁾⁽¹⁶⁾⁽⁶⁴⁾⁽⁶⁵⁾⁽⁶⁶⁾⁽⁶⁷⁾⁽⁶⁸⁾⁽⁶⁹⁾⁽⁷⁰⁾⁽⁷¹

Figure 2 Routes of administration of probiotics for the oral cavity

The probiotics most commonly evaluated so far in the oral cavity are isolated microbial strains, mainly of the digestive tract, like the ones belonging to the genus Lactobacillus (L. rhamnosus, L. reuteri, L. casei, L. brevis, L. paracasei, L. acidophilus, L. plantarum) and Bifidobacterium (B. bifidum, B. longum, B. lactis, B. animalis, B. infantis)³⁷⁾⁽⁴⁹ (Table 1). These bacteria have proven their safety for many years, allowing clinical studies and the development of commercial products, with the added value that some have been identified in healthy individuals (DMF = 0) (L. rhamnosus, L. plantarum, L. acidophilus, L. brevis, L. paracasei),⁷² suggesting their role in micro-ecologic balance. As a drawback to their use, some studies have shown their poor colonization capacity in the oral cavity,⁷³⁾⁽⁷⁴⁾ especially in hard tissues,⁷²⁾ in addition to acidogenic properties of some strains and their presence in carious regions,⁷⁵⁾ suggesting the opposite effect to that expected with probiotics.

One of the most commonly studied probiotic bacteria in the oral cavity was isolated by Gorbach and Godin in 1983 from digestive tract of a healthy adult.⁷⁶⁾ It was named Lactobacillus rhamnosus GG (ATCC53103) and is characterized by inhibiting, by means of bacteriocins, a wide variety of human pathogenic bacteria,⁷⁷⁾ including _{^{S. mutans, S. sobrinus, Aggregatibacter actinomycetemcomitans, Porphyromonas gingivalis and Prevotella intermedia.(}}⁷⁸⁾⁽⁷⁹⁾ In addition, this bacterium colonizes the microcosm of saliva, and has no cariogenic effect.⁷⁹⁾ This bacterium was used to conduct one of the most complete clinical studies in children (aged 1 to 6 years), reducing the incidence of caries in the age of 3 to 4 years.⁴⁴

Lactobacillus reuteri is another bacterium that has been commonly studied, and is usually found in the human gastrointestinal tract. It produces bacteriocins that inhibit Gram-positive bacteria as Bacillus cereus, Staphylococcus aureus and Listeria monocytogenes and Gram-negative bacteria such as E. coli, Yersinia enterocolitica and Pseudomonas fluorescens.⁵⁵⁾ In the oral cavity, it has been shown to inhibit S. mutans in saliva, and Tannerella forsythia and S. gordonii in vitro.⁸⁰⁾ The strains most frequently studied in the oral cavity are l. reuteri ATCC 55730, isolated in 1990 from a Peruvian mother’s breast milk, and l. reuteri ATCC 5289, isolated from the oral cavity of a Japanese woman.⁸¹⁾ These bacteria showed suitable characteristics for colonization and maintenance of pH in the oral cavity. In 2012, Jalasvuori et al showed that in vitro the strains kept a pH over 7 during 4 hours of incubation in presence of glucose and sufficient amount of arginine, showing the arginolytic nature of these bacteria.⁸¹⁾ Strain ATCC 5289 is the most efficient to keep an alkaline pH, and has a greater colonizing potential due to its capacity of adhesion and formation of biofilm.⁸¹⁾⁽⁸²

Species of the genus Streptococcus, such as S. salivarius, S. sanguinis and S. oligofermentans, are specific to the oral cavity and have been studied as possible probiotics. S. salivarius is one of the earliest colonizers of the epithelium surface in the human mouth and nasopharynx, and its primary habitat is the dorsum of the healthy tongue; the K12 strain was isolated from a healthy child’s saliva, and is characterized by producing bacteriocins which inhibit the growth of Gram-negative bacteria associated with periodontitis and halitosis

⁸³⁾ and Gram-positive bacteria like S. mutans. In addition, it has the property of producing ammonium from arginine and urea, through the expression of the gene of urease in conditions of acidic pH and excess carbohydrates.⁸⁴

The role of S. oligofermentans as a probiotic was discovered during a clinical trial noting an inverse relationship in the amount of this bacteria with respect to S. mutans in dental plaque.⁸⁵⁾ An in vitro study confirmed the inhibitory effect of this bacterium, due to the production of hydrogen peroxide from lactic acid, suggesting its inhibitory capacity in the presence of bacteria producers of lactic acid.⁸⁶

S. sanguinis, just like S. mutans, is one of the primary colonizers of dental plaque, but with an inverse relationship in quantity, suggesting an antagonism between these two bacteria.⁸⁷⁾ A subsequent study showed that this antagonism was due to the production of hydrogen peroxide by S. sanguninis on the one hand, and the production of bacteriocins by S. mutans, on the other.⁸⁸⁾ The inhibitory capacity of a bacterium on the another is determined by the ecological factors of the host and by the survival mechanisms of the bacteria in the oral cavity, due to the regulation of inhibitory compounds by the environmental conditions and the juxtaposition of the two species.⁸⁹

IN SEARCH OF THE IDEAL BACTERIA AS PROBIOTICS

Various research groups⁹⁰⁾⁽⁹¹⁾⁽⁹²⁾⁽⁹³⁾⁽⁹⁴ have conducted studies aiming to isolate, identify, and assess bacterial strains complying with the characteristics of probiotics in the oral cavity (Table 2). One of such studies is that by Strahinic et al, who searched for strains of Lactobacillus sp. with probiotic characteristics in human oral cavity, identifying l. salivarius BGH01 and l. gasseri BGH089.⁹⁰⁾ These strains showed antagonism against human pathogenic bacteria (Staphylococcus auereus, Enterococcus faecalis, Micrococcus flavus, Salmonella enteritidis), including S. mutans. A subsequent study showed that L. salivarius BGH01 produces more than one bacteriocin; of these, LS1 and LS2 have already been isolated and evaluated.⁹⁵

Table 2 Characteristics of probiotics for the oral cavity

Another study, focused on finding lactic acid bacteria in saliva from healthy children, identified 11 bacteria strains that met the criteria defined by the researchers, such as ability of adherence to oral tissues and aggregation to form biofilm, antagonism against pathogens, bacterial genetic identification, absence of acids and malodorous volatile compounds, and absence of resistance to antibiotics.⁹¹

Camelo-Castillo et al identified two strains of bacteria that they named Streptococcus dentisani in the dental plaque of individuals who have never had dental caries. This bacterium belongs to the mitis group, but was grouped with a new phylogenetic branch. Through the analysis of genomic and metabolic characteristics, they confirmed it belongs to a new species of the genus Streptococcus. As probiotic characteristics, S. dentisani has antimicrobial activity against S. mutans in in vitro conditions, and produces ammonium by arginine metabolism, controlling the pH of the oral cavity and thus preventing the colonization of strains related to the development of caries.⁹²

To identify bacteria with probiotic characteristics, Wu et al analyzed bacterial strains of Lactobacillus salivarius with antagonistic activity against S. mutans. They studied 64 strains and found two, K35 and K43, which significantly inhibited the formation of biofilm of S. mutans. Subsequent in vitro studies confirmed that they had strong bactericidal activity against S. mutans.⁹³

In 2015, Terai et al selected, from dental plaque and tongue of healthy individuals, bacteria of the genus Lactobacillus and Streptococcus which did not produce volatile sulfur compounds (VSCs) or water-insoluble glucans, with high antibacterial activity against caries and periodontitis-causing bacteria as well as high activity of adherence to oral epithelial cells and hydroxyapatite in vitro. The authors selected L. crispatus YIT 12319, L. fermentum YIT12320, L. gasseri YIT 12321 and S. mitis YIT 12322 for complying with the abovementioned characteristics, and for not having cariogenic risk or causing infective endocarditis.⁹⁴

In addition to presenting findings related to the evaluation for probiotic characteristics, some of the studies ⁹¹⁾⁽⁹⁴ show the safety tests that selected bacteria are subjected to. These tests (Figure 3) are necessary to use these bacteria without any risk for humans, they begin as in vitro studies in laboratories and continue in animals and clinical trials in humans.

Figure 3 Safety tests for the use of probiotic strains

CONCLUSIONS

Understanding caries as an oral microbiota dysbiosis has raised again the issue of the development of strategies for the control of this disease. One of the biotechnological strategies is the use of probiotics, with the main objective of establishing beneficial microorganisms to contribute to homeostasis in the oral cavity. In oral health, the findings in a variety of studies on probiotics are promising, although few include clear results. Understanding the characteristics that probiotics should have for the oral cavity will allow selecting the most suitable strains for this purpose. This article discussed some of the most important features, prioritizing safety in their use and location in the oral cavity.

RECOMMENDATIONS

Probiotics could be used as a preventive treatment for tooth decay; however, in some countries like Colombia no products have been developed specifically for the control of this disease. This creates an invitation to conduct studies on bacteria that satisfy the ideal characteristics for the oral cavity and prove being effective.

Such studies could start by isolating and identifying native bacterial strains that are safe, in order to create a greater availability of options and select the most appropriate for clinical studies. If a strain with clear results is found, new products will be available in the market and probably public health measures as well.

CONFLICTS OF INTEREST

The authors declare not having any conflict of interest.

REFERENCES

1. World Health Organization. Oral health: priority action areas [Internet]. [Consultado el 20 de octubre de 2015] Disponible en: http://www.who.int/oral_health/action/information/surveillance/en/ [ Links ]

2. Petersen PE, Bourgeois D, Ogawa H, Estupinan-Day S, Ndiaye C. The global burden of oral diseases and risks to oral health. Bull World Health Organ 2005; 83(9): 661-669. [ Links ]

3. Selwitz RH, Ismail AI, Pitts NB. Dental caries. Lancet 2007; 369(9555): 51-59. [ Links ]

4. Olmos P, Piovesán S, Musto M, Lorenzo S, Álvarez R, Massa F. Caries dental. La enfermedad oral más prevalente. Primer estudio poblacional en jóvenes y adultos uruguayos del interior del país. Odontoestomatol 2013; 15: 26-34. [ Links ]

5. Casabe JH. Endocarditis infecciosa. Una enfermedad cambiante. Medicina (B Aires) 2008; 68(2): 164-174. [ Links ]

6. Colombia. Ministerio de Salud. IV Estudio Nacional de Salud Bucal: ENSAB IV: situación en salud bucal: para saber cómo estamos y saber qué hacemos. [Internet]. Bogotá: Minsalud; 2014 [Consultado el 10 de noviembre de 2015]. Disponible en: https: //www.minsalud.gov.co/sites/rid/Lists/BibliotecaDigital/RIDE/VS/PP/ENSAB-IV-Situacion-Bucal-Actual.pdf [ Links ]

7. Wongkamhaeng K, Poachanukoon O, Koontongkaew S. Dental caries, cariogenic microorganisms and salivary properties of allergic rhinitis children. Int J Pediatr Otorhinolaryngol 2014; 78(5): 860-865. [ Links ]

8. Castellanos JE, Marín LM, Úsuga MV, Castiblanco GA, Martingnon S. La remineralización del esmalte bajo el entendimiento actual de la caries dental. Univ Odontol 2013; 32(69): 49-59. [ Links ]

9. Kutsch VK. Dental caries: an updated medical model of risk assessment. J Prosthet Dent 2014; 111(4): 280-285. [ Links ]

10. Simón-Soro A, Mira A. Solving the etiology of dental caries. Trends Microbiol 2015; 23(2): 76-82. [ Links ]

11. Rojas S, Echeverría S. Caries temprana de infancia: ¿enfermedad infecciosa? Rev Med Clin Condes 2014; 25(3): 581-587. [ Links ]

12. Gross EL, Leys EJ, Gasparovich SR, Firestone ND, Schwartzbaum JA, Janies DA et al. Bacterial 16S sequence analysis of severe caries in young permanent teeth. J Clin Microbiol 2010; 48(11): 4121-4128. [ Links ]

13. Tanner AC, Kent RL Jr, Holgerson PL, Hughes CV, Loo CY, Kanasi E et al. Microbiota of severe early childhood caries before and after therapy. J Dent Res 2011; 90(11): 1298-1305. [ Links ]

14. Burne RA, Zeng L, Ahn SJ, Palmer SR, Liu Y, Lefebure T et al. Progress dissecting the oral microbiome in caries and health. Adv Dent Res 2012; 24(2): 77-80. [ Links ]

15. 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. Clin Oral Investig 2014; 18(6): 1539-1552. [ Links ]

16. Cagetti MG, Mastroberardino S, Milia E, Cocco F, Lingström P, Campus G. The use of probiotic strains in caries prevention: a systematic review. Nutrients 2013; 5(7): 2530-2550. [ Links ]

17. Joint FAO/WHO. Guidelines for the Evaluation of Probiotics in Food [Internet]. London: FAO/WHO; 2002. [ Links ]

18. Wade WG. Has the use of molecular methods for the characterization of the human oral microbiome changed our understanding of the role of bacteria in the pathogenesis of periodontal disease? J Clin Periodontol 2011; 38(Suppl 11): 7-16. [ Links ]

19. Dewhirst FE, Chen T, Izard J, Paster BJ, Tanner ACR, Yu WH et al. The human oral microbiome. J Bacteriol 2010; 192(19): 5002-5017. [ Links ]

20. Lazarevic V, Whiteson K, Hernandez D, François P, Schrenzel J. Study of inter- and intra-individual variations in the salivary microbiota. BMC Genom 2010; 11: 523. DOI: 10.1186/1471-2164-11-523 [ Links ]

21. Ten-Cate JM. Biofilms, a new approach to the microbiology of dental plaque. Odontology 2006; 94(1): 1-9. [ Links ]

22. Mark Welch J, Rossetti B, Rieken C, Dewhirst F, Borisy G. Biogeography of a human oral microbiome at the micron scale. PNAS 2016; 113(6): 791-800. DOI: 10.1073/pnas.1522149113 [ Links ]

23. Rouabhia M. Interactions between host and oral commensal microorganisms are key events in health and disease status. Can J Infect Dis 2002; 13(1): 47-51. [ Links ]

24. Bowden GHW. The microbial ecology of dental caries. Microb Ecol Health Dis 2000; 12(3): 138-148. [ Links ]

25. Marsh PD. Microbiology of dental plaque biofilms and their role in oral health and caries. Dent Clin North Am 2010; 54(3): 441-454. [ Links ]

26. Zarco MF, Vess TJ, Ginsburg GS. The oral microbiome in health and disease and the potential impact on personalized dental medicine. Oral Dis 2012; 18(2): 109-120. [ Links ]

27. Scannapieco FA. The oral microbiome: Its role in health and in oral and systemic infections. Clin Microbiol Newsl 2013; 35(20): 163-169. [ Links ]

28. Duran-Pinedo AE, Frias-Lopez J. Beyond microbial community composition: functional activities of the oral microbiome in health and disease. Microbes Infect 2015; 17(7): 505-516. [ Links ]

29. Belstrøm D, Fiehn NE, Nielsen CH, Holmstrup P, Kirkby N, Klepac-Ceraj V et al. Altered bacterial profiles in saliva from adults with caries lesions: a case-cohort study. Caries Res 2014; 48(5): 368-375. [ Links ]

30. Vieira-Colombo AP, Magalhães CB, Hartenbach FA, Martins-do-Souto R, Macielda-Silva-Boghossian C. Periodontal-disease-associated biofilm: A reservoir for pathogens of medical importance. Microb Pathog 2016; 94: 27-34. [ Links ]

31. Chocolatewala N, Chaturvedi P, Desale R. The role of bacteria in oral cancer. Indian J Med Paediatr Oncol 2010; 31(4): 126-131. [ Links ]

32. Whitmore SE, Lamont RJ. Oral bacteria and cancer. PLoS Pathog 2014; 10(3): e1003933. DOI: 10.1371/journal.ppat.1003933 [ Links ]

33. Zaura E, Keijser BJ, Huse SM, Crielaard W. Defining the healthy “core microbiome” of oral microbial communities. BMC Microbiol 2009; 9(259): 1-12. DOI: 10.1186/1471-2180-9-259 [ Links ]

34. Kianoush N, Adler CJ, Nguyen KA, Browne GV, Simonian M, Hunter N. Bacterial profile of dentine caries and the impact of pH on bacterial population diversity. PLoS One 2014; 9(3): e92940. DOI: 10.1371/journal.pone.0092940 [ Links ]

35. Corby PM, Lyons-Weiler J, Bretz WA, Hart TC, Aas JA et al. Microbial Risk Indicators of Early Childhood Caries. J Clin Microbiol 2005; 43(11): 5753-5759. [ Links ]

36. Tanzer JM, Livingston J, Thompson AM. The microbiology of primary dental caries in humans. J Dent Educ 2001; 65(10): 1028-1037. [ Links ]

37. Badet C, Thebaud NB. Ecology of lactobacilli in the oral cavity: a review of literature. Open Microbiol J 2008; 2: 38-48. [ Links ]

38. Chen T, Yu W-H, Izard J, Baranova OV, Lakshmanan A, Dewhirst FE. The Human Oral Microbiome Database: a web accessible resource for investigating oral microbe taxonomic and genomic information. Database 2010; Article ID baq013, DOI: 10.1093/database/baq013 [ Links ]

39. Griffen AL, Beall CJ, Firestone ND, Gross EL, Difranco JM, Hardman JH et al. CORE: A Phylogenetically-Curated 16S rDNA Database of the Core Oral Microbiome. PLoS One 2011; 6(4): e19051. DOI: 10.1371/journal.pone.0019051. [ Links ]

40. Iniesta M, Zurbriggen M, Montero E, Herrera D. Los probióticos y sus beneficios terapéuticos. Periodoncia y Osteintegración 2011; 21(3): 171-179. [ Links ]

41. Organización Mundial de Gastroenterología. Guía práctica de la Organización Mundial de Gastroenterología: Probióticos y prebióticos [Internet]. Milwaukee: WGO; 2011 [Consultado el 24 de octubre de 2015]. Disponible en: http://www.worldgastroenterology.org/UserFiles/file/guidelines/probiotics-spanish-2011.pdf [ Links ]

42. Singh VP, Sharma J, Babu S, Rizwanulla T, Singla A. Role of probiotics in health and disease: a review. J Pak Med Assoc 2013; 63(2): 253-57. [ Links ]

43. Cáceres RP, Gotteland RM. Alimentos probióticos en Chile: ¿Qué cepas y qué propiedades saludables? Rev Chil Nutr 2010; 37(1): 97-109. [ Links ]

44. 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 risk in children. Caries Res 2001; 35(6): 412-420. [ Links ]

45. Petersson LG, Magnusson K, Hakestam U, Baigi A, Twetman S. Reversal of primary root caries lesions after daily intake of milk supplemented with fluoride and probiotic lactobacilli in older adults. Acta Odontol Scand 2011; 69(6): 321-327. [ Links ]

46. Vistoso-Monreal AP. Efecto del consumo de leche enriquecida con probióticos lactobacilos, en la incidencia de lesiones de caries en niños preescolares [Trabajo de grado Cirujano-Dentista]. Santiago de Chile: Universidad de Chile; 2013 [Consultado el 2 de noviembre de 2015]. Disponible en: http://repositorio.uchile.cl/handle/2250/130016 [ Links ]

47. 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(1): 112. [ Links ]

48. Breath MD. Oral probiotics [Internet]. BreathMD; 2015 [Consultado el 2 de octubre de 2015]. Disponible en: http://www.breathmd.com/oral-probiotics.php. [ Links ]

49. Agrawal V, Kapoor S, Shah N. Role of “Live Microorganisms” (Probiotics) in Prevention of Caries: Going on the Natural Way Towards Oral Health. Indian J Multidiscip Dent 2012; 2(3): 491-496. [ Links ]

50. Haukioja A. Probiotics and oral health. Eur J Dent 2010; 4(3): 348-355. [ Links ]

51. Burton JP, Drummond BK, Chilcott CN, Tagg JR, Thomson WM, Hale JD et al. Influence of the probiotic Streptococcus salivarius strain M18 on indices of dental health in children: A randomized double-blind, placebo-controlled trial. J Med Microbiol 2013; 62(Part 6): 875-884. [ Links ]

52. Toiviainen A, Jalasvuori H, Lahti E, Gursoy U, Salminen S, Fontana M et al. Impact of orally administered lozenges with Lactobacillus rhamnosus GG and Bifidobacterium animalis subsp. lactis BB-12 on the number of salivary mutans streptococci, amount of plaque, gingival inflammation and the oral microbiome in healthy adults. Clin Oral Investig 2015; 19(1): 77-83. [ Links ]

53. Ahola AJ, Yli-Knuuttila H, Suomalainen T, Poussa T, Ahlström A, Meurman JH et al. Short-term consumption of probiotic-containing cheese and its effect on dental caries risk factors. Arch Oral Biol 2002; 47(11): 799-804. [ Links ]

54. Montalto M, Vastola M, Marigo L, Covino M, Graziosetto R, Curigliano V et al. Probiotic treatment increases salivary counts of lactobacilli: a double-blind, randomized, controlled study. Digestion 2004; 69(1): 53-56. [ Links ]

55. Nikawa H, Makihira S, Fukushima H, Nishimura H, Ozaki Y, Ishida K et al. Lactobacillus reuteri in bovine milk fermented decreases the oral carriage of mutans streptococci. Int J Food Microbiol 2004; 95(2): 219-223. [ Links ]

56. Caglar E, Sandalli N, Twetman S, Kavaloglu S, Ergeneli S, Selvi S. Effect of yogurt with Bifidobacterium DN-173 010 on salivary mutans streptococci and lactobacilli in young adults. Acta Odontol Scand 2005; 63(6): 317-320. [ Links ]

57. Caglar E, Cildir SK, Ergenelli S, Sandalli N, Tweetman S. Salivary mutans streptococci and lactobacilli levels after ingestion of the probiotic bacterium Lactobacillus reuteri ATCC 55730 by straws or tablets. Acta Odontol Scand 2006; 65(5): 314-318. [ Links ]

58. Caglar E, Kavaloglu SC, Kuscu OO, Sandalli N, Holgerson PL, Twetman S. Effect of chewing gums containing xylitol or probiotic bacteria on salivary mutans streptococci and lactobacilli. Clin Oral Investig 2007; 11(4): 425-429. [ Links ]

59. Caglar E, Kuscu OO, Cildir SK, Kuvvetli SS, Sandalli N. A probiotic lozenge administered medical device and its effect on salivary mutans streptococci and lactobacilli. Int J Paediatr Dent 2008; 18(1): 35-39. [ Links ]

60. Caglar E, Kuscu OO, Selvi Kuvvetli S, Kavaloglu Cildir S, Sandalli N, Twetman S. Short-term effect of ice-cream containing Bifidobacterium lactis Bb-12 on the number of salivary mutans streptococci and lactobacilli. Acta Odontol Scand 2008; 66(3): 154-158. [ Links ]

61. 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 Res 2009; 43(5): 374-381. [ Links ]

62. Cogulu D, Topaloglu-Ak A, Caglar E, Sandalli N, Karagozlu C, Ersin N et al. Potential effects of a multistrain probiotic-kefir on salivary Streptococcus mutans and Lactobacillus spp. J Dent Sci 2010; 5(3): 144-149. [ Links ]

63. Lexner MO, Blomqvist S, Dahlen G, Twetman S. 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 Heal Prev Dent 2010; 8(4): 383-388. [ Links ]

64. Aminabadi NA, Erfanparast L, Ebrahimi A, Oskouei SG. Effect of chlorhexidine pretreatment on the stability of salivary lactobacilli probiotic in six- to twelve-year-old children: a randomized controlled trial. Caries Res 2011; 45(2): 148-154. [ Links ]

65. Jindal G, Pandey RK, Agarwal J, Singh M. A comparative evaluation of probiotics on salivary mutans streptococci counts in Indian children. Eur Arch Paediatr Dent 2011; 12(4): 211-215. [ Links ]

66. Mortazavi S, Akhlaghi N. Salivary Streptococcus mutans and Lactobacilli levels following probiotic cheese consumption in adults: A double blind randomized clinical trial(*). J Res Med Sci 2012; 17(1): 57-66. [ Links ]

67. 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 Res 2012; 46(1): 69-77. [ Links ]

68. Campus G, Cocco F, Carta G, Cagetti MG, Simark-Mattson C, Strohmenger L et al. Effect of a daily dose of Lactobacillus brevis CD2 lozenges in high caries risk schoolchildren. Clin Oral Investig 2014; 18(2): 555-561. [ Links ]

69. 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 Res 2013; 47(6): 559-565. [ Links ]

70. Nishihara T, Suzuki N, Yoneda M, Hirofuji T. Effects of Lactobacillus salivarius-containing tablets on caries risk factors: a randomized open-label clinical trial. BMC Oral Health 2014; 14(1): 110. [ Links ]

71. 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(1): 112. [ Links ]

72. Colloca ME, Ahumada MC, López ME, Nader-Macías ME. Surface properties of lactobacilli isolated from healthy subjects. Oral Dis 2000; 6(4): 227-233. [ Links ]

73. Yli-Knuuttila H, Snäll J, Kari K, Meurman JH. Colonization of Lactobacillus rhamnosus GG in the oral cavity. Oral Microbiol Immunol 2006; 21(2): 129-131. [ Links ]

74. Busscher HJ, Mulder AF, van der Mei HC. In vitro adhesion to enamel and in vivo colonization of tooth surfaces by Lactobacilli from a bio-yoghurt. Caries Res. 1999; 33(5): 403-404. [ Links ]

75. Matee MI, Mikx FH, Maselle SY, Van Palenstein Helderman WH. Mutans streptococci and lactobacilli in breast-fed children with rampant caries. Caries Res. 1992; 26(3): 183-187. [ Links ]

76. Gorbach SL, Goldin BR, inventors; New England Medical Center Inc, assignee. Lactobacillus strains and methods of selection. United States patent US 4839281(A). 1989 Jun 13. [ Links ]

77. Doron S, Snydman DR, Gorbach SL. Lactobacillus GG: bacteriology and clinical applications. Gastroenterol Clin North Am 2005; 34(3): 483-498. [ Links ]

78. Kõll P, Mändar R, Marcotte H, Leibur E, Mikelsaar M, Hammarström L. Characterization of oral lactobacilli as potential probiotics for oral health. Oral Microbiol Immunol 2008; 23(2): 139-147. [ Links ]

79. Pham LC, Hoogenkamp MA, Exterkate RA, Terefework Z, de Soet JJ, ten Cate JM et al. Effects of Lactobacillus rhamnosus GG on saliva-derived microcosms. Arch Oral Biol 2011; 56(2): 136-147. [ Links ]

80. Baca-Castañón ML, De la Garza-Ramos MA, Alcázar-Pizaña AG, Grondin Y, Coronado-Mendoza A, Sánchez-Najera RI et al. Antimicrobial Effect of Lactobacillus reuteri on Cariogenic Bacteria Streptococcus gordonii, Streptococcus mutans, and Periodontal Diseases Actinomyces naeslundii and Tannerella forsythia. Probiotics Antimicrob Proteins 2015; 7(1): 1-8. [ Links ]

81. Jalasvuori H, Haukioja A, Tenovuo J. Probiotic Lactobacillus reuteri strains ATCC PTA 5289 and ATCC 55730 differ in their cariogenic properties in vitro. Arch Oral Biol 2012; 57(12): 1633-1638. [ Links ]

82. Madhwani T, McBain AJ. Bacteriological effects of a Lactobacillus reuteri probiotic on in vitro oral biofilms. Arch Oral Biol 2011; 56(11): 1264-1273. [ Links ]

83. Burton JP, Chilcott CN, Moore CJ, Speiser G, Tagg JR. A preliminary study of the effect of probiotic Streptococcus salivarius K12 on oral malodour parameters. J Appl Microbiol 2006; 100(4): 754-764. [ Links ]

84. Huang SC, Burne RA, Chen YY. The pH-dependent expression of the urease operon in Streptococcus salivarius is mediated by CodY. Appl Environ Microbiol 2014; 80(17): 5386-5393. [ Links ]

85. Tong H, Gao X, Dong X. Streptococcus oligofermentans sp. nov., a novel oral isolate from caries-free humans. Int J Syst Evol Microbiol 2003; 53(Pt 4): 1101-1104. [ Links ]

86. Tong H, Chen W, Merritt J, Qi F, Shi W, Dong X. Streptococcus oligofermentans inhibits Streptococcus mutans through conversion of lactic acid into inhibitory H₂O₂: a possible counteroffensive strategy for interspecies competition. Mol Microbiol 2007; 63(3): 872-880. [ Links ]

87. Caufield PW, Dasanayake AP, Li Y, Pan Y, Hsu J, Hardin JM. Natural history of Streptococcus sanguinis in the oral cavity of infants: evidence for a discrete window of infectivity. Infect Immun 2000; 68(7): 4018-4023. [ Links ]

88. Kreth J, Zhang Y, Herzberg MC. Streptococcal antagonism in oral biofilms: Streptococcus sanguinis and Streptococcus gordonii interference with Streptococcus mutans. J Bacteriol 2008; 190(13): 4632-4640. [ Links ]

89. Kreth J, Merritt J, Shi W, Qi F. Competition and coexistence between streptococcus mutans and streptococcus sanguinis in the dental biofilm. J Bacteriol 2005; 187(21): 7193-7203. [ Links ]

90. Strahinic I, Busarcevic M, Pavlica D, Milasin J, Golic N, Topisirovic L. Molecular and biochemical characterizations of human oral lactobacilli as putative probiotic candidates. Oral Microbiol Immunol 2007; 22(2): 111-117. [ Links ]

91. Bosch M, Nart J, Audivert S, Bonachera MA, Alemany AS, Fuentes MC et al. Isolation and characterization of probiotic strains for improving oral health. Arch Oral Biol 2012; 57(5): 539-549. [ Links ]

92. Camelo-Castillo A, Benítez-Páez A, Belda-Ferre P, Cabrera-Rubio R, Mira A. Streptococcus dentisani sp. nov., a novel member of the mitis group. Int J Syst Evol Microbiol 2014; 64(Pt 1): 60-65. [ Links ]

93. Wu CC, Lin CT, Wu CY, Peng WS, Lee MJ, Tsai YC. Inhibitory effect of Lactobacillus salivarius on Streptococcus mutans biofilm formation. Mol Oral Microbiol 2015; 30(1): 16-26. [ Links ]

94. Terai T, Okumura T, Imai S, Nakao M, Yamaji K, Ito M et al. Screening of probiotic candidates in human oral bacteria for the prevention of dental disease. PLoS One 2015; 10(6): e0128657. DOI: 10.1371/journal.pone.0128657 [ Links ]

95. Busarcevic M, Dalgalarrondo M. Purification and genetic characterisation of the novel bacteriocin LS2 produced by the human oral strain Lactobacillus salivarius BGHO1. Int J Antimicrob Agents 2012; 40(2): 127-134. [ Links ]

96. Sanders ME, Akkermans LM, Haller D, Hammerman C, Heimbach J, Hörmannsperger G et al. Safety assessment of probiotics for human use. Gut Microbes 2010; 1(3): 164-185. [ Links ]

97. Burton JP, Wescombe PA, Moore CJ, Chilcott CN, Tagg JR. Safety assessment of the oral cavity probiotic Streptococcus salivarius K12. Appl Environ Microbiol 2006; 72(4): 3050-3053. [ Links ]

98. Senok AC, Ismaeel AY, Botta GA. Probiotics: facts and myths. Clin Microbiol Infect 2005; 11(12): 958-966. [ Links ]

99. Petti S, Tarsitani G, D’Arca AS. A randomized clinical trial of the effect of yoghurt on the human salivary microflora. Arch Oral Biol 2001; 46(8): 705-712. [ Links ]

100. Kilian M, Frandsen EV, Haubek D, Poulsen K. The etiology of periodontal disease revisited by population genetic analysis. Periodontol 2000 2006; 42(1): 158-179. [ Links ]

101. Devine DA, Marsh PD. Prospects for the development of probiotics and prebiotics for oral applications. J Oral Microbiol [Internet] 2009; 1. Disponible en: http://www.journaloforalmicrobiology.net/index.php/jom/article/view/1949 [ Links ]

102. Samot J, Badet C. Antibacterial activity of probiotic candidates for oral health. Anaerobe 2013; 19(1): 34-38. [ Links ]

103. Stamatova I, Meurman JH. Probiotics: Health benefits in the mouth. Am J Dent 2009; 22(6): 329-338. [ Links ]

104. Suárez JE. Microbiota autóctona, probióticos y prebióticos. Nutr Hosp 2013; 28 (1): 38-41. [ Links ]

105. Makinen K, Berger B, Bel-Rhlid R, Ananta E. Science and technology for the mastership of probiotic applications in food products. J Biotechnol 2012; 162(4): 356-365. [ Links ]

¹Angarita-Díaz MP. Probiotics and their relationship with caries control. A topic review. Rev Fac Odontol Univ Antioq 2016; 28 (1): 179-202. DOI: http://dx.doi.org/10.17533/udea.rfo.v28n1a10

Received: November 24, 2015; Accepted: May 10, 2016

CORRESPONDENCIA María del Pilar Angarita Díaz, Universidad Cooperativa de Colombia, sede Villavicencio, (+57) 300 898 3524, maria.angaritad@campusucc.edu.co, Carrera 35 No. 36-99 Barzal. Villavicencio, Colombia

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