Lactobacilli for the Treatment of Oral Diseases
Received Date: Aug 30, 2017 / Accepted Date: Sep 07, 2017 / Published Date: Sep 14, 2017
Probiotics are defined as live microorganisms that beneficially affect the host. Probiotic bacteria have been used therapeutically for years to target gastrointestinal disease by rebalancing the complex microflora. Besides the gastrointestinal tract also the oral cavity is highly colonized by bacteria and many different bacterial species are part of the microbiota in the mouth, as it offers ideal conditions for bacteria with a stable temperature, moist surface with a relatively stable pH and regular supply of nutrients. By disturbing the balance of microorganisms in the oral cavity or by extensive accumulation of plaque, the ratio of pathogenic organisms can increase and lead to oral health problems. Probiotic bacteria, like lactobacilli, are a promising treatment strategy for oral diseases with a microbiological aetiology. Those include plaqueÃ¢Â€Âassociated diseases like dental caries, which is an infectious disease with microbial processes eroding and destroying the hard dental tissue or inflammation of periodontal tissue, namely gingivitis and the more severe periodontitis. Moreover, endodontic infections, and even fungal, viral and acute bacterial infections could be treated by a probiotic therapy. The interest of probiotics in the field of oral health is growing, although it is still in its infancy. The present review adresses criteria for the selection of probiotic lactobacilli strains. It encompasses existing evidence on the use of lactobacilli for caries, halitosis and candidiasis, as well as for periodontal disease like Gingivitis and periodontitis.
Keywords: Probiotics; Oral health; Caries; Periodontitis; Gingivitis
The word probiotics comes from the Greek words “pro” and “bios”, meaning ‘for life’. The term probiotics was first mentioned by Lilley and Stillwell in 1965 and was defined as the opposite of antibiotics . “Organisms and substances which contribute to intestinal microbial balance” was a later definition from Parker . Although this definition is still used today, this interpretation included also antibiotics, which is not commonly used today. An advancement was the interpretation from Fuller in 1989, because the importance of living cells was emphasised and the word “substances” was eliminated to avoid confusion. “A live microbial feed supplement which beneficially affects the host animal by improving its intestinal microbial balance”. Ever since, the definition has been reworked several times and it was for instance broadened by Vrese and Schrezenmeir, who included other target location than the gut . An often cited definition is the one in the WHO/FAO report from 2006, wherein probiotics were defined as: “Live microorganisms which when administered in adequate amounts confer a health benefit on the host” .
Probiotics are mainly used in dairy products, but they are increasingly becoming available as dietary supplements and pharmaceutical preparations. A large variety of microorganisms are classified as probiotics at present. Holzapfel  listed strains used as probiotics. Lactic acid bacteria are of most importance in food and nutrition, especially lactobacilli and the genus Bifidobacterium, whereas non-lactic acid bacteria are mainly used in pharmaceutical preparations. Different Lactobacillus species are also found in the oral cavity and in the saliva, the most common of which are: L. fermentum, L. rhamnosus, L. salivarius, L. casei, L. acidophilus and L. plantarum [7-9]. Three of these species are used in dairy products, but yet it is not clear, if they are detected due to frequent consumption of dairy products leading to temporary colonisation, or if the oral environment is the natural habitat .
If probiotics are taken orally, they are considered to be safe. A theoretical concern is that these viable bacteria move into the bloodstream and cause systemic infections. Lactobacillus rhamnosus GG (LGG) became available in Finland in 1990. Salimen et al. analysed blood samples in the period between 1990-2000 and did not find an increase related to the increasing probiotic use of LGG-containing commercial dairy products . One case has been published that was caused by probiotic lactobacilli. A L. rhamnosus GG strain was isolated from a liver abscess in 19994. Some cases of Endocarditis  or L. rhamnosus GG leading to bacteraemia  are described, but it is estimated, that only 0.05%-0.4% of these cases are due to lactobacilli and bifidobacterial . These lactobacilli and bifidobacteria are thought to be part of the commensal microbiota, instead of administered probiotics. Most cases of probiotic bacteraemia responded well to appropriate antibiotic therapy. Common risk factors to Lactobacillus bacteraemia are immunosuppression, prior hospitalisation and previous antibiotic treatment . Even in HIV-infected patients, the use of the probiotic L. rhamnosus GG was well tolerated and no adverse effects, like bacteraemic outbreaks, were observed10. The consumption of 1 × 1010 CFU/day was safe and well tolerated in a HIV-positive population . Antibiotic resistance of lactobacilli can be another safety issue. Probiotics should not carry transmissible antibiotic resistance genes . Lactobacilli are naturally resistant to some antibiotics, as shown by Charteris , but this resistance is usually not of a transmissible type. Non-transmissible antibiotic resistance is usually of no safety concern. Lactobacillus plantarum CCUG 43738 displayed atypical phenotypic resistance to tetracycline and minocycline, from a plasmid-located tet(S) gene. This acquired antibiotic resistance is undesirable for potential probiotics . There are additional reports of acquired antibiotic resistance [20-21]. The transferal of antimicrobial resistance genes between probiotics and closely related opportunistic bacteria may take place . More studies are needed, because the development of resistance to antibiotic drugs is a global issue. The US Food and Drug Administration (FDA) designation ‘Generally Recognized as Safe’ (GRAS) has been applied to several Lactobacillus strains  being a strong indication for safety in human consumption.
Lactobacilli for Oral Health
The selection of appropriate probiotic strains is a key issue. In contrast to the often used dietary lactobacilli, indigenous bacteria offer an advantage, because they are well adjusted to the human oral ecology. Consequently, the use of orally derived probiotics is recommended. Furthermore, the binding of LAB to mucus might be necessary to show positive effects, if administered to the oral cavity. Carbohydrate-protein interactions probably play a key role in the adhesion of these proteins to mucin-bound oligosaccharides . Presently, most reports on mucus binding of probiotics are in the gastrointestinal field, because this is the main field of application. Several adhesion promoting proteins in Lactobacillus spp. are described and summarised by Van Tassell et al.  and by Vélez et al. . The most studied mucus-targeting bacterial adhesin is mucus-binding protein (MUB), which is produced by L. reuteri . An adhesion-promoting protein that mediated L. fermentum 104R binding to both small intestinal porcine mucus and porcine gastric mucin is described by Royas et al. . Moreover, some Lactobacillus strains adhere to Caco-2 cell cultures, which was observed by Tuomola and Salimen . A mucus adhesion promoting protein, MapA, mediates the adhesion of L. reuteri to human intestinal epithelial cells . In L. plantarum WCFS1 a lectin-like mannose-specific adhesin that interacts with the host intestinal tract has also been described . It is expected, that bacteria, intended as oral probiotics, should adhere to and colonise surfaces of the oral cavity . Yli-Knuuttila et al. investigated whether L. rhamnosus GG could be detected in the oral cavity after discontinuation of administration of a probiotic product. This strain could only temporally be detected, but did not colonise the oral cavity. The authors concluded, that colonisation with this strain is improbable, but possible in some cases30. In a clinical study, the application of a chewable tablet of L. reuteri ATCC 55730 (108 CFU/tablet) for 2 weeks did not lead to permanent colonisation of the oral cavity . The consumption of probiotic yoghurt-containing lactobacilli did also not lead to their installation in the oral cavity . In contrast, salivary Lactobacillus counts increased after consumption of a product containing seven different Lactobacillus strains . L. plantarum 299v (Lp299v) and L. paracasei showed survival in saliva for 24 h. The L. paracasei strain bound well to a surface mimicking human dental enamel, because over 20% of the added bacteria were bound but, for Lp299v the binding was poor with below 5% . Lactobacillus GG, incorporated into yoghurt, was consumed twice a day for 7 d. After discontinuation of consumption, the bacterium was recovered in saliva samples, and after 2 weeks the strain was still present in 8 out of 9 subjects .
A final aspect to consider is lactic acid production by lactobacilli, because this process has been implicated in enamel demineralisation and dental caries in the mouth. The ability to produce acid varies significantly between strains and if they belong to the homofermentative or heterofermentative group . Some strains, such as L. plantarum 299v can not only ferment carbohydrates (e.g. glucose and fructose) but also sugar alcohols (e.g. mannitol or sorbitol) leading to a decrease in pH in-vitro. In contrast Keller and Twetman found no evidence for an increased plaque acidity for L. plantarum 299v with fructose or xylitol . Strains with low metabolic activity are favourable, for example L. paracasei .
Three main factors considered for plaque-related periodontal inflammation are: a susceptible host, which is hard to address; second the presence of pathogenic species and the reduction or even absence of ‘beneficial bacteria’. Today, periodontal therapies aim to reduce the bacterial threat and are based on mechanical subgingival debridement plus improvement of oral hygiene . The subgingivalmicrobiota then shifts towards a less pathogenic composition, meaning a higher proportion of Gram-positive aerobic species and fewer periodontopathogens . Unfortunately, this shift is only temporary. The use of antibiotics or antiseptics for a certain time does not improve the long-term effect of periodontal therapy . The use of probiotics in this field offers the possibility to restore the reduced numbers of beneficial bacteria to prevent and treat plaque-related periodontal disease. On the one hand the inhibition of specific pathogens is a possible mechanism and on the other hand the host response could be affected by probiotics.
To date, the following effects have been shown for probiotics in the field of periodontal disease. L. salivarius tablets reduced 5 periodontopathic bacteria in subgingival plaque after 4 weeks and the levels tended to be lower up to 8 weeks compared with placebo . In a clinical trial with L. reuteri containing tablets the number of periodontal pathogens in the subgingivalmicrobiota was reduced, but no significant clinical impact could be shown . A Lactobacillusmicrobiota inhibited growth of S. mutans, P. gingivalis and P. intermedia . Furthermore, antimicrobial effects against P. gingivalis have been described [45-46]. Co-aggregation activity of probiotic strains with oral pathogens (Porphyromonasendodontalis, T. forsythia, Eubacteriumsaphenum, Filifactoralocis or P. gingivalis) can be another mode of action [44,45,47]. Competition with peridontopathogens for the uptake of nutrients could also improve oral health . Some strains produce biosurfactants, which are able to prevent the adhesion of pathogens . L. salivarius TI 2711 administered as tablets did not significantly change the total number of bacteria in the saliva, or the number of mutans-streptococci and lactobacilli. Only for black-pigmented anaerobic rods, which include most periodontopathic bacteria, a significant decrease was found . A promising strain is also L. reuteriProdentis, because not only antimicrobial, but also inflammatory, effects were found along with inhibition of plaque formation . The reduction of pro-inflammatory cytokines (TNF-α, IL-8) in gingival crevicular fluid can be regarded proof of concept for the application of Lactobacillus reuteri in a chewing gum. The modulating effect of short-term intake of probiotics on the oral immune response is dose dependent . An anti-inflammatory effect of Lactobacillus brevis, administered as lozenge to patients with chronic periodontitis, was shown by a significant decrease in the amount of nitrite/nitrate, prostaglandin E2 and matrix metalloproteinase in saliva . Different microbial species show anti-inflammatory activity . Although an anti-inflammatory effect of probiotic milk drink containing L. caseiShirota was shown in a clinical trial, increased plaque accumulation occurred, which is probably linked to the high sugar content . The same product increased the plaque index and papilla bleeding index compared to baseline, whereas the amount of matrix metalloproteinase-3 was reduced . By using a probiotic treatment (L. reuteri) also clinical effects were found, like a significant reduction in the gingival index and plaque scores . Smokers showed a significantly greater improvement in plaque scores in a clinical trial using freeze-dried probiotic tablets of L. salivarius . Even heat-killed L. plantarum decreased the depth of periodontal pockets in a randomised, double-blind, placebo-controlled clinical trial .
Dental caries is on the one hand associated with S. mutans, but also with lactobacilli. Indeed, L. plantarum and L. paracasei are among the species found in adult and childhood caries . Various Lactobacillus spp. have numerical importance in carious dentine  and are often found in caries lesions . L. salivarius LS 1952R induced dental caries in rats . In an in-vitro model the combination of LGG and S. mutans was more cariogenic than monospeciesbiofilms of S. mutans. Therefore, LGG did not reduce the caries activity, but contributed to the caries process . Another finding in this direction is that after restoration of caries, S. mutans and lactobacilli are reduced in saliva . By now the role of lactobacilli in caries is not absolutely sure. It has been observed, that lactobacilli from caries-free people exert more effective inhibition of mutans-streptococci than lactobacilli isolated from caries-active subjects in-vitro . L. plantarum 299v and other Lactobacillus strains coaggregate in-vitro with selected oral streptococci. Coaggregation is an important factor in the development of biofilms and dental plaque .
Several studies have been published that hint towards an anti-caries effect of lactobacilli. L. casei ATCC 11578 is able to prevent and even decolonise the adhesion of S. mutans to saliva-coated hydroxyapatite by modifying the protein composition of the salivary pellicle . In a clinical study using L. paracasei GMNL-33 a significant reduction of salivary S. mutans was detected after 4 weeks . L. paracasei showed maximum interference activity against S. mutans in-vitro, as reported by Simark-Mattsson et al. . Lozenges containing L. brevis CD2 taken by school children with a high caries risk, resulted in a reduction in plaque acidogenicity, salivary mutans-streptococci and bleeding on probing . L. reuteri significantly inhibited thegrowth of S. mutans, if applied as yoghurt , via straws and tablets [71,72] or as chewing gum . A combination of L. sporogens, L. bifidum, L. bulgaricus, L. thermophilus, L. acidophilus, L. casei and L. rhamnosus either as capsule or as liquid form was tested. The counts of lactobacilli in the saliva increased significantly, but S. mutans was not significantly influenced. Unfortunately, no follow-up was performed after the trial . Lactobacilli (including L. plantarum 299v, L. paracasei, L. reuteri, L. acidophilus and L. rhamnosus) showed co-aggregation with mutans-streptococci in-vitro and inhibited the clinical mutans-streptococci . In a randomised, double-blind, placebo-controlled intervention study in 594 children, milk containing LGG reduced dental caries and the counts of mutans-streptococci after 7 months. Consequently, the risk of caries was significantly reduced . In another double-blind, placebo-controlled trial of milk supplemented with fluoride and/or L. rhamnosus the effect on primary root caries lesions was investigated. The use of milk only supplemented with lactobacilli showed a positive effect, as well as the fluoride, but the beneficial effect was strongest by combining both .
There is currently limited evidence to support the use of lactobacilli in halitosis. After taking L. salivarius WB21 and xylitol in tablet form daily, the scores of an organoleptic test and bleeding on probing significantly decreased after 4 weeks . In a randomised double-blind, placebo-controlled cross-over trail with 25 adults a probiotic chewing gum with L. reuteri DSM 17938 and L. reuteri ATCC PTA 5289 or placebo was used. After a treatment duration of 14 days the organoleptic scores were significantly lower in the group with probiotic chewing gum .
For candidiasis there is also little evidence available. In a randomised, double-blind, placebo-controlled study the consumption of probiotic cheese (L. rhamnosus GG plus Propionibacteriumfreudenreichiisusp.Shermanii JS) led to reduced C. albicans counts . However, in a 3 week intervention for which subjects ate 5 × 15 g cheese per day containing LGG and L. rhamnosus LC 705, no significant difference in the effect between the probiotic and control cheese on salivary Candida counts was found . The administration of L. casei and Bifidobacteriumbreve for 20 d significantly reduced Candida prevalence and the level of anti-Candida immunoglobulin A . Lozenges with L. reuteriProdentis are available on the market and reduce the prevalence of oral Candida in fragile elderly people . Finally, L. plantarum and L. paracasei showed some co-aggregation with C. albicans .
The cited studies are often limited due to small sample size, lack of appropriate randomisation, blinding, duration of intervention plus follow-up and study set-up. Even fewer studies make inter-group comparison with true placebo or a negative control. The tested population is very heterogeneous and the probiotic doses applied differ up to 2 log scales. Furthermore, the vehicles used to administer the probiotics also clearly differ and might influence the outcome of the study. Typical means of probiotic administration are yoghurt, cheese , lozenges and tablets , capsules or liquids33. Besides, it is expected to be difficult to induce a microbiological shift or a clinical probiotic effect in a matured oral microbiological environment. The probiotics will have difficulties in colonising the mouth. A pre-treatment, to reduce the levels of indigenous microbiota, might be useful and necessary. The authors of a meta-analysis concluded, that the evidence supporting the use of probiotics to prevent or treat caries and periodontal disease is insufficient at present. In spite of the lack of evidence, they also state, that no adverse effects were reported, so there is no strong argument against using such a treatment .
Probiotic effects are strain-specific and cannot be transferred to other subspecies, or even other strains without any tests. Therefore, clear nomenclature of the evaluated strains is crucial for allociation of effects and for the judgement of efficiency. Overall, lactobacilli seem to be a promising way forward regarding restoration of periodontal health, especially in gingivitis, but better designed clinical trials in larger populations are needed. Moreover, combining different probiotic strains could lead to synergistic effects. This research field is in a very early state and enormous efforts are necessary to advance this promising strategy. An application in caries is questionable, as long as the impact of lactobacilli on the cause and progression of the disease is not clarified.
Conflict of Interest Statement
Anja Hoffmann reports Personal fees from Symrise AG and Rolf Daniels reports Grants from Symrise AG, both outside the submitted work. In addition, Rolf Daniels and Anja Hoffmann have a patent EP 15 184849.6 pending.
- Lilly DM, Stillwell RH (1965) Probiotics: Growth-Promoting Factors Produced by Microorganisms. Science 147: 747-748.
- Parker RB (1974) Probiotics, the other half of the antibiotic story. AnimNutr Health 29: 4-8.
- Fuller R (1989) Probiotics in man and animals. J ApplMicrobiol 66: 365-378.
- Vrese MD, Schrezenmeir J (2002) Probiotics and non-intestinal infectious conditions. Br J Nutr 88: 59-66.
- Food and Agriculture Organization of the United Nations (2006) Probiotics in food: Health and nutritional properties and guidelines for evaluation. Food and nutrition paper 85.
- Holzapfel WH, Haberer P, Geisen R, Björkroth J, Schillinger U (2001) Taxonomy and important features of probiotic microorganisms in food and nutrition. Am J ClinNutr 73: 365-373.
- Teanpaisan R, Dahlen G (2006) Use of polymerase chain reaction techniques and sodium dodecyl sulfate-polyacrylamide gel electrophoresis for differentiation of oral Lactobacillus species. Oral MicrobiolImmunol 21: 79-83.
- Ahrne S, Nobaek S, Jeppsson B, Adlerberth I, Wold AE, et al. (1998) The normal Lactobacillus flora of healthy human rectal and oral mucosa. J ApplMicrobiol 85: 88-94.
- Maukonen J, Matto J, Suihko ML, Saarela M (2008) Intra-individual diversity and similarity of salivary and faecal microbiota. J Med Microbiol 57:1560-1568.
- Meurman JH, Stamatova I (2007) Probiotics: contributions to oral health. Oral Dis 13: 443-451.
- Salminen MK, Tynkkynen S, Rautelin H (2002) Lactobacillus bacteremia during a rapid increase in probiotic use of Lactobacillus rhamnosus GG in Finland. Clin Infect Dis 35: 1155-1160.
- Mackay AD, Taylor MB, Kibbler CC, Hamilton Miller JM (1999) Lactobacillus endocarditis caused by a probiotic organism. ClinMicrobiol Infect 5: 290-292.
- Boyle RJ, Robins Browne RM, Tang MLK (2006) Probiotic use in clinical practice: what are the risks? Am J ClinNutr 83: 1256-1264.
- Borriello SP, Hammes WP, Holzapfel W (2003) Safety of probiotics that contain lactobacilli or bifidobacteria. Clin Infect Dis 36: 775-780.
- Salminen MK, Rautelin H, Tynkkynen S (2004) Lactobacillus bacteremia, clinical significance, and patient outcome, with special focus on probiotic L. rhamnosus GG. Clin Infect Dis 38: 62-69.
- Wolf BW, Wheeler KB, Ataya DG, Garleb KA (1998) Safety and tolerance of Lactobacillus reuteri supplementation to a population infected with the human immunodeficiency virus. Food ChemToxicol 36: 1085-1094.
- Saarela M, Mogensen G, Fondén R, Mättö J, MattilaSandholm T (2000) Probiotic bacteria: Safety, functional and technological properties. J Biotechnol 84: 197-215.
- Charteris WP, Kelly PM, Morelli L, Collins JK (1998) Antibiotic susceptibility of potentially probiotic Lactobacillus species. J Food Prot 61: 1636-1643.
- Huys G, D'Haene K, Swings J (2006) Genetic basis of tetracycline and minocycline resistance in potentially probiotic Lactobacillus plantarum strain CCUG 43738. Antimicrob Agents Chemother 50: 1550-1551.
- Danielsen M (2002) Characterization of the tetracycline resistance plasmid pMD5057 from Lactobacillus plantarum 5057 reveals a composite structure. Plasmid 48: 98-103.
- Stroman P, Muller CC, Sorensen KI (2003) Heat Shock Treatment Increases the Frequency of Loss of an Erythromycin Resistance-Encoding Transposable Element from the Chromosome of Lactobacillus crispatus CHCC3692. Appl Environ Microbiol 69: 7173-7180.
- Liong MT (2008) Safety of probiotics: translocation and infection. Nutr Rev 66: 192-202.
- Van Tassell ML, Miller MJ (2011) Lactobacillus adhesion to mucus. Nutrients 3: 613-636.
- Vélez MP, Keersmaecker D, Sigrid CJ, Vanderleyden J (2007) Adherence factors of Lactobacillus in the human gastrointestinal tract. FEMS MicrobiolLett 276: 140-148.
- Roos S, Jonsson H (2002) A high-molecular-mass cell-surface protein from Lactobacillus reuteri 1063 adheres to mucus components. Microbiology 148: 433-442.
- Rojas M, Ascencio F, Conway PL (2002) Purification and Characterization of a Surface Protein from Lactobacillus fermentum 104R That Binds to Porcine Small Intestinal Mucus and Gastric Mucin. Appl Environ Microbiol 68: 2330-2336.
- Tuomola, Elina M, Salminen SJ (1998) Adhesion of some probiotic and dairy Lactobacillus strains to Caco-2 cell cultures. Int J Food Microbiol 41: 45-51.
- Miyoshi Y, Okada S, Uchimura T, Satoh E (2006) A mucus adhesion promoting protein, MapA, mediates the adhesion of Lactobacillus reuteri to Caco-2 human intestinal epithelial cells. BiosciBiotechnolBiochem 70: 1622-1628.
- Pretzer G, Snel J, Molenaar D (2005) Biodiversity-Based Identification and Functional Characterization of the Mannose-Specific Adhesin of Lactobacillus plantarum. J Bacteriol 187: 6128-6136.
- YliKnuuttila H, Snall J, Kari K, Meurman JH (2006) Colonization of Lactobacillus rhamnosus GG in the oral cavity. Oral MicrobiolImmunol 21: 129-131.
- Caglar E, Topcuoglu N, Cildir SK, Sandalli N, Kulekci G (2009) Oral colonization by Lactobacillus reuteri ATCC 55730 after exposure to probiotics. Int J Paediatr Dent 19: 377-381.
- Busscher HJ, Mulder AF, Van Der Mei HC (1999) In vitro Adhesion to Enamel and in vivo Colonization of Tooth Surfaces by Lactobacilli from a Bio-Yoghurt. Caries Res 33: 403-404.
- Montalto M, Vastola M, Marigo L (2004) Probiotic treatment increases salivary counts of lactobacilli: a double-blind, randomized, controlled study. Digestion 69: 53-56.
- Haukioja A, YliKnuuttila H, Loimaranta V (2006) Oral adhesion and survival of probiotic and other lactobacilli and bifidobacteria in vitro. Oral MicrobiolImmunol 21: 326-332.
- Meurman JH, Antila H, Salminen S (1994) Recovery of Lactobacillus strain GG (ATCC 53103) from saliva of healthy volunteers after consumption of yoghurt prepared with the bacterium. MicrobEcol Health Dis 7: 295-298.
- McBain A, Madhwani T, Eatough J, Ledder R (2009) An introduction to probiotics for dental health. Food SciTechnol Bull 6: 5-29.
- Keller MK, Twetman S (2012) Acid production in dental plaque after exposure to probiotic bacteria. BMC Oral Health 12: 44.
- Hedberg M, Hasslof P, Sjostrom I, Twetman S, StecksenBlicks C (2008) Sugar fermentation in probiotic bacteria-an in vitro study. Oral MicrobiolImmunol 23: 482-485.
- Haffajee AD, Arguello EI, XimenezFyvie LA, Socransky SS (2003) Controlling the plaque biofilm. Int Dent J 53: 191-199.
- XiménezFyvie LA, Haffajee AD, Som S, Thompson M, Torresyap G, et al. (2000) The effect of repeated professional supragingival plaque removal on the composition of the supra-and subgingivalmicrobiota. J ClinPeriodontol 27: 637-647.
- Quirynen M, Teughels W, Soete MDE, Van Steenberghe D (2002) Topical antiseptics and antibiotics in the initial therapy of chronic adult periodontitis: microbiological aspects. Periodontol 28: 72-90.
- Mayanagi G, Kimura M, Nakaya S (2009) Probiotic effects of orally administered Lactobacillus salivarius WB21-containing tablets on periodontopathic bacteria: a double-blinded, placebo-controlled, randomized clinical trial. J ClinPeriodontol 36: 506-513.
- Iniesta M, Herrera D, Montero E (2012) Probiotic effects of orally administered Lactobacillus reuteri-containing tablets on the subgingival and salivary microbiota in patients with gingivitis. A randomized clinical trial. J ClinPeriodontol 39: 736-744.
- Koll Klais P, Mandar R, Leibur E, Marcotte H, Hammarstrom L, et al. (2005) Oral lactobacilli in chronic periodontitis and periodontal health: species composition and antimicrobial activity. Oral MicrobiolImmunol 20: 354-361.
- Pangsomboon K, Kaewnopparat S, Pitakpornpreecha T, Srichana T (2006) Antibacterial activity of a bacteriocin from Lactobacillus paracasei HL32 against Porphyromonasgingivalis. Arch Oral Biol 51: 784-793.
- Connelly P (2008) Lactobacillus plantarum-A literature review of therapeutic benefits. J AustTradit-Med So 14: 79-82.
- Hojo K, Nagaoka S, Ohshima T, Maeda N (2009) Bacterial Interactions in Dental Biofilm Development. J Dent Res 88: 982-990.
- Smith VH, Pippin DJ (1998) Implications of resource-ratio theory for oral microbial ecology. Eur J Oral Sci 106: 605-615.
- Van Hoogmoed CG, Van Der Kuijl BM, Van Der Mei HC, Busscher HJ (2000) Inhibition of Streptococcus mutans NS Adhesion to Glass with and without a Salivary Conditioning Film by Biosurfactant-Releasing Streptococcus mitisStrains. Appl Environ Microbiol 66: 659-663.
- Ishikawa H, Aiba Y, Nakanishi M, Oh-hashi Y, Koga Y () Suppression of Periodontal Pathogenic Bacteria in the Saliva of Humans by the Administration of Lactobacillus salivarius TI2711. J JpnSocPeriodontol 45: 105-112.
- Vivekananda MR, Vandana KL, Bhat KG (2010) Effect of the probiotic Lactobacilli reuteri (Prodentis) in the management of periodontal disease: a preliminary randomized clinical trial. J Oral Microbiol 2:5344.
- Twetman S, Derawi B, Keller M, Ekstrand K, Yucel Lindberg T, et al. (2009) Short-term effect of chewing gums containing probiotic Lactobacillus reuteri on the levels of inflammatory mediators in gingival crevicular fluid. ActaOdontolScand 67: 19-24.
- Della Riccia DN, Bizzini F, Perilli MG (2007) Anti-inflammatory effects of Lactobacillus brevis (CD2) on periodontal disease. Oral Dis 13: 376-385.
- Slawik S, Staufenbiel I, Schilke R (2011) Probiotics affect the clinical inflammatory parameters of experimental gingivitis in humans. Eur J ClinNutr 65: 857-863.
- Staab B, Eick S, Knofler G, Jentsch H (2009) The influence of a probiotic milk drink on the development of gingivitis: a pilot study. J ClinPeriodontol 36: 850-856.
- Krasse P, Carlsson B, Dahl C, Paulsson A, Nilsson A, et al. (2005) Decreased gum bleeding and reduced gingivitis by the probiotic Lactobacillus reuteri. Swed Dent J 30: 55-60.
- Shimauchi H, Mayanagi G, Nakaya S (2008) Improvement of periodontal condition by probiotics with Lactobacillus salivarius WB21: a randomized, double-blind, placebo-controlled study. J ClinPeriodontol 35: 897-905.
- Iwasaki K, Maeda K, Hidaka K, Nemoto K, Hirose Y, et al. (2016) Daily Intake of Heat-killed Lactobacillus plantarum L-137 Decreases the Probing Depth in Patients Undergoing Supportive Periodontal Therapy. Oral Health Prev Dent 14: 207-214.
- Caufield PW, Schön CN, Saraithong P, Li Y, Argimón S (2015) Oral Lactobacilli and Dental Caries. J Dent Res 94: 110-118.
- Byun R, Nadkarni MA, Chhour KL, Martin FE, Jacques NA, et al. (2004) Quantitative analysis of diverse Lactobacillus species present in advanced dental caries. J ClinMicrobiol 42: 3128-3136.
- Chhour KL, Nadkarni MA, Byun R, Martin FE, Jacques NA, et al. (2005) Molecular analysis of microbial diversity in advanced caries. J ClinMicrobiol 43: 843-849.
- Matsumoto M, Tsuji M, Sasaki H (2005) Cariogenicity of the probiotic bacterium Lactobacillus salivarius in rats. Caries Res 39: 479-483.
- Schwendicke F, Dorfer C, Kneist S, Meyer Lueckel H, Paris S (2014) Cariogenic effects of probiotic Lactobacillus rhamnosus GG in a dental biofilm model. Caries Res 48: 186-192.
- Wright JT, Cutter GR, Dasanayake AP, MacStiles H, Caufield PW (1992) Effect of conventional dental restorative treatment on bacteria in saliva. Commun Dent Oral Epidemiol 20: 138-143.
- SimarkMattsson C, Emilson CG, Hakansson EG, Jacobsson C, Roos K, et al. (2007) Lactobacillus-mediated interference of mutans streptococci in caries-free vs. caries-active subjects. Eur J Oral Sci 115: 308-314.
- Twetman L, Larsen U, Fiehn NE, StecksenBlicks C, Twetman S (2009) Coaggregation between probiotic bacteria and caries-associated strains: an in vitro study. ActaOdontolScand 67: 284-288.
- Haukioja A, Loimaranta V, Tenovuo J (2008) Probiotic bacteria affect the composition of salivary pellicle and streptococcal adhesion in vitro. Oral MicrobiolImmunol 23: 336-343.
- Chuang LC, Huang CS, Ou Yang LW, Lin SY (2011) Probiotic Lactobacillus paracasei effect on cariogenic bacterial flora. Clin Oral Invest 15: 471-476.
- Campus G, Cocco F, Carta G (2014) Effect of a daily dose of Lactobacillus brevis CD2 lozenges in high caries risk schoolchildren. Clin Oral Investig 18: 555-561.
- Nikawa H, Makihira S, Fukushima H (2004) Lactobacillus reuteri in bovine milk fermented decreases the oral carriage of mutans streptococci. Int J Food Microbiol 95: 219-223.
- Caglar E, Kuscu OO, Cildir SK, Kuvvetli SS, Sandalli N (2008) A probiotic lozenge administered medical device and its effect on salivary mutans streptococci and lactobacilli. Int J Paediatr Dent 18: 35-39.
- Caglar E, Cildir SK, Ergeneli S, Sandalli N, Twetman S (2006) Salivary mutans streptococci and lactobacilli levels after ingestion of the probiotic bacterium Lactobacillus reuteri ATCC 55730 by straws or tablets. ActaOdontolScand 64: 314-318.
- Caglar E, Kavaloglu SC, Kuscu OO, Sandalli N, Holgerson PL, et al. (2007) Effect of chewing gums containing xylitol or probiotic bacteria on salivary mutans streptococci and lactobacilli. Clin Oral Investig 11: 425-429.
- Keller MK, Hasslof P, StecksenBlicks C, Twetman S (2011) Co-aggregation and growth inhibition of probiotic lactobacilli and clinical isolates of mutans streptococci: an in vitro study. ActaOdontolScand 69: 263-268.
- Näse L, Hatakka K, Savilahti E (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: 412-420.
- Petersson LG, Magnusson K, Hakestam U, Baigi A, Twetman S (2011) Reversal of primary root caries lesions after daily intake of milk supplemented with fluoride and probiotic lactobacilli in older adults. ActaOdontolScand 69: 321-327.
- Iwamoto T, Suzuki N, Tanabe K, Takeshita T, Hirofuji T (2010) Effects of probiotic Lactobacillus salivarius WB21 on halitosis and oral health: an open-label pilot trial. Oral Surg Oral Med Oral Pathol Oral RadiolEndod 110: 201-208.
- Keller MK, Bardow A, Jensdottir T, Lykkeaa J, Twetman S (2012) Effect of chewing gums containing the probiotic bacterium Lactobacillus reuteri on oral malodour. ActaOdontolScand 70: 246-250.
- Hatakka K, Ahola AJ, YliKnuuttila H (2007) Probiotics reduce the prevalence of oral Candida in the elderly-A randomized controlled trial. J Dent Res 86: 125-130.
- Ahola AJ, YliKnuuttila H, Suomalainen T (2002) Short-term consumption of probiotic-containing cheese and its effect on dental caries risk factors. Arch Oral Biol 47: 799-804.
- Santos ALD, Jorge AOC, Santos SSFD, Silva CRGE, Leão MVP (2009) Influence of probiotics on Candida presence and IgA anti-Candida in the oral cavity. Braz J Microbiol 40: 960-964.
- Kraft Bodi E, Jorgensen MR, Keller MK, Kragelund C, Twetman S (2015) Effect of Probiotic Bacteria on Oral Candida in Frail Elderly. J Dent Res 94: 181-186.
- Gomaa EZ (2013) Antimicrobial and anti-adhesive properties of biosurfactant produced by lactobacilli isolates, biofilm formation and aggregation ability. J Gen ApplMicrobiol 59: 425-436.
- Gruner D, Paris S, Schwendicke F (2016) Probiotics for managing caries and periodontitis: Systematic review and meta-analysis. J Dent 48: 16-25.
Citation: Hoffmann A, Daniels R (2017) Lactobacilli for the Treatment of Oral Diseases. J Prob Health 5: 181. Doi: 10.4172/2329-8901.1000181
Copyright: © 2017 Hoffmann A, et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Select your language of interest to view the total content in your interested language
Share This Article
28th World Nutrition Congress
August 9- 10 2018 Manila, Philippines
8th Annual Congress on Probiotics & Functional Foods
September 24-25, 2018 Tokyo, Japan
- Total views: 679
- [From(publication date): 0-2017 - Jul 21, 2018]
- Breakdown by view type
- HTML page views: 605
- PDF downloads: 74