|Year : 2019 | Volume
| Issue : 2 | Page : 90-96
Role of probiotics in the treatment and prevention of oral malodor/halitosis: A systematic review
Pragati Ishwar Shringeri1, Nusrath Fareed1, Hemant Battur1, Sanjeev Khanagar2
1 Department of Public Health Dentistry, KVG Dental College and Hospital, Sullia, Karnataka, India
2 Lecturer, College of Dentistry, King Saud Bin Abdul Aziz University for Health Sciences, Riyadh, Saudi Arabia
|Date of Submission||27-Aug-2018|
|Date of Acceptance||27-Apr-2019|
|Date of Web Publication||20-Jun-2019|
Dr. Pragati Ishwar Shringeri
Department of Public Health Dentistry, KVG Dental College and Hospital, Kurunjibag, Sullia, Dakshina Kannada - 574 327, Karnataka
Source of Support: None, Conflict of Interest: None
Oral malodor is a condition which impedes people's social life and self-esteem. With more widespread acceptance of the potential for probiotic intervention providing health benefits for nonintestinal body sites, application of it on alternative target tissues has increased, to obtain more specific and enduring benefits. From the periodontal perspective, several studies have revealed the role of probiotic in the reduction of gingival inflammation. However, the studies of stronger evidence pertaining to the role of probiotics in the treatment and prevention of halitosis is limited. The aim of this study was to determine the role of probiotic strains in the treatment and prevention of oral malodor. Records were searched from various databases such as PubMed/Medline, Cochrane, and EMBASE. Articles published over the past 11 years were identified using the key search terms. A total of 178 records were identified by title/abstracts/full-text articles and were retrieved. After thorough assessment, 11 manuscripts were included in qualitative synthesis in this systematic review. Analysis of studies revealed 666 participants, aged 4–76 years, and about 20 probiotic strains were assigned to the test groups and control groups with a varying follow-up period. The effect size for randomized control trials ranged from 0.08 to 0.7 which suggests low-to-moderate practical significance. The results of this systematic review confirm that more studies are necessary to evaluate the efficacy of probiotics with correct methodological design, in broader population samples, and over longer periods.
Keywords: Halitosis, oral malodor, probiotics, volatile sulfur compound
|How to cite this article:|
Shringeri PI, Fareed N, Battur H, Khanagar S. Role of probiotics in the treatment and prevention of oral malodor/halitosis: A systematic review. J Indian Assoc Public Health Dent 2019;17:90-6
|How to cite this URL:|
Shringeri PI, Fareed N, Battur H, Khanagar S. Role of probiotics in the treatment and prevention of oral malodor/halitosis: A systematic review. J Indian Assoc Public Health Dent [serial online] 2019 [cited 2021 Oct 22];17:90-6. Available from: https://www.jiaphd.org/text.asp?2019/17/2/90/260867
| Introduction|| |
Oral malodor is a condition which impedes people's social life and hampers one's self-esteem. Patients with halitosis look up to dentists for professional consultation; therefore, dentists should have an understanding of the local as well as the systemic factors which cause halitosis. The most common oral malodor compounds are by-products of the metabolism of oral bacteria, especially anaerobes, located on the dorsum of the tongue. Volatile sulfur compounds (VSCs), valeric acid, butyric acid, and putrescine are thought to contribute to the odor.
As defined by the WHO, “Probiotics are live microorganisms which when administered inadequate amounts confer a health benefit on the host.” The term probiotic, which is an antonym of the term antibiotic, was first introduced by Lilly and Stillwell (1965) as substances produced by microorganisms, which promotes the growth of other microorganisms. The usage of probiotics by humans has almost exclusively focused on the derivation of benefits through the ingestion of microbes originally obtained from intestinal sources. However, with the more widespread acceptance of the potential for probiotic intervention to also effect health benefits for nonintestinal body sites, there has come the increased application of effector strains of species that are indigenous to alternative target tissues, to obtain more specific and enduring benefits. From the periodontal perspective, several studies have revealed the role of probiotic strains in the reduction of gingival inflammation., However, the studies of stronger evidence pertaining to the role of probiotics in the treatment and prevention of halitosis is limited. The aim was to review the literature about the role of probiotics in the treatment and prevention of oral malodor.
| Material and Methods|| |
Literature search strategy
To identify studies included in or considered for this review, search strategies were developed for each database that we searched. An online search of the MEDLINE-PubMed, EMBASE, and Cochrane Library was conducted from January 2000 to January 2017. The strategy used was a combination of MeSH terms and free text words including probiotics (MeSH), halitosis (MeSH), oral malodor (text word), VSC (MeSH), and beneficial bacteria (text word) with bullion words; AND, OR, and NOT.
Inclusion and exclusion criteria
Randomized controlled trials andin vitro studies about the use of probiotics in the treatment and prevention of halitosis or oral malodor and the effect of beneficial bacteria on VSCs were included in the study.
The primary outcome we have considered were reduction in the organoleptic scores and in the production of VSCs in bothin vitro andin vivo studies.
Potentially relevant reports identified from the reference lists of relevant studies, review articles, and chapters were searched. Those records selected for retrieval were assessed by the first three authors (selectors and extractors) for methodological validity before the inclusion in the review. Details of the search steps and the reasons for exclusion from the review were documented and are presented in [Flow Chart 1].
Full-length articles of all included studies were obtained. The aim, study design, characteristics of the participants, and VSC-producing bacteria of each eligible study were collected. The type of probiotic bacteria and its concentration and the vehicle of its administration were recorded in conjunction with the outcome of data.
The studies were assessed in terms of a series of methodological factors. The selected articles were critically appraised by all the authors, based on Joanna Briggs Institute (JBI) critical appraisal checklist for systematic reviews. The studies were scored by assigning “✓” if the study appropriately met the quality item, a “×” was assigned if the study did not meet the quality item. A “?” was assigned if there was no sufficient information regarding the quality item, and “NA” was assigned in case if the criteria did not apply to the particular study being rated. If the authors disagreed on the classification of a study, a discussion was held to reach a consensus.
The process and results of the electronic and hand searches are as shown in Flow Chart 1. The authors took part in all phases of the study selection. A total of 178 records were identified by title/abstracts/full-text articles and were retrieved. Potentially relevant reports identified from the reference lists of relevant studies, review articles, and chapters were hand searched, which yielded an additional ten articles. Sixty-two articles were identified as duplicates and were excluded from the study. At the next level, 92 records were eliminated as the outcome in those studies was the role of probiotics in the treatment and prevention of periodontal diseases. Further, 68 records were excluded as they were studies which included the combination of probiotics with chlorhexidine. At this level, a total of 24 records were considered potentially eligible and sought for further assessment. Eventually, 11 manuscripts were included in qualitative synthesis in this systematic review.
| Results|| |
Included studies were published between 2006 and 2016. Two studies were conducted in 2006–2010,,, nine studies in 2011–2016.,,,,,,, Four studies were conducted in Japan,,,, three in South Korea,,, one in New Zealand, one in Denmark, one in Switzerland, and one in the United Kingdom. Quality assessment was based on JBI level of evidence (2014) as described in [Table 1]. The main characteristics and results of the studies analyzed in this review are summarized in [Table 2]. Risk of bias assessments in this review is discussed in [Table 3].
|Table 2: Quality assessment, main characteristics and results of the studies analyzed in the review|
Click here to view
Analysis of studies revealed 666 participants, aged 4–76 years, and about 20 VSCs-producing bacteria were assigned to the test groups and control groups with a varying follow-up period. Allin vivo studies had patients <50,,,,,,, except one study which included 460 children  as the study population. Seven types of probiotic strains were used in the studies where three studies each have administered Streptococcus salivarius K12,, and Lactobacillus salivarius.,, Of 11 studies, four were in vitro,,, and six were in vivo,,,,, and one study  was bothin vitro and in vivo. The effect size for randomized control trials ranged from 0.08 to 0.7 which suggests low-to-moderate practical significance. The vehicle of administration of probiotics varied from lozenge, probiotic suspension, tablets (Iwamoto et al., 2010; Suzuki et al., 2012),, chewing gum, oil drops (Suzuki et al., 2014), and fermented drink. The administered probiotics were within the concentration range of 1 × 108–1 × 109 colony-forming unit (CFU), and three studies ,, used concentration of more than 1 × 109 CFU. Allin vivo studies showed randomization and three studies performed double blinding.,,
| Discussion|| |
Several mechanisms have been proposed to explain how probiotics work. For example, these bacteria secrete various antimicrobial substances such as organic acids, hydrogen peroxide, and bacteriocins. In addition, they compete with pathogenic agents for adhesion sites on the mucosa. Probiotics can also modify the surrounding environment by modulating the pH and/or the oxidation-reduction potential, which may compromise the ability of pathogens to become established. Finally, probiotics may provide beneficial effects by stimulating nonspecific immunity and modulating the humoral and cellular immune response. A combination of probiotic strains is often used to increase these beneficial effects.
The usage of probiotics by humans has almost exclusively focused on the derivation of benefits through the ingestion of microbes originally obtained from intestinal sources. The bacteria in yoghurt and fermented milk products constitute the most important source of probiotics for humans. The vast majority of probiotic bacteria belong to the genera Lactobacillus, Bifidobacterium, Propionibacterium, and Streptococcus.,, Several clinical studies have already demonstrated the effectiveness of certain probiotics in the treatment of systemic and infectious diseases. Probiotics have been widely used for “healthy gut,” however, the concept of alternative target sites has emerged. Bernaola Aponte et al. in a review implied that there was limited evidence suggesting that probiotics can be effective in treating persistent diarrhea in children. Goldenberg et al. in a review claimed that probiotic was both safe and effective for preventing clostridium difficile-associated diarrhea. Hao et al. revealed in their review on probiotics for preventing acute upper respiratory tract infection (URTI) that probiotics were found to be better than placebo in reducing the number of participants experiencing episodes of acute URTI by about 47% and the duration of an episode of acute URTI by about 1.89 days and may slightly reduce antibiotic use and cold-related school absence, also side effects of probiotics were minor and gastrointestinal symptoms were the most common.
Along came the concept of application of probiotic therapy in oral health. Aside from the use of probiotics in treatment and prevention of gastrointestinal tract infection, there have been studies conducted to test its efficacy in the treatment and prevention of dental caries and periodontal diseases., Yanine et al. in their review stated that the effectiveness of probiotics on the prevention and treatment of periodontal diseases is questionable.
The oral cavity is home to a wide range of bacterial species that produce several fetid substances as a result of protein degradation. VSC-producing bacteria colonizing the dorsum of the tongue have recently been implicated in halitosis. Detection of VSCs, such as methylmercaptan and hydrogen sulfite, through organoleptic and objective methods, can aid in the identification of their source. Following comprehensive evaluation for possible causes, most halitosis in patients seen in an ear, nose, and throat or dental practice can be localized to the tongue., Bacteriologic analysis of biofilm and scraped specimens obtained from the lingual dorsum and other oral sites, primarily gingival pockets and tonsillar crypts can identify VSC-producing bacteria. Porphyromonas, Prevotella, Actinobacillus, and Fusobacterium species are the most common identified organisms. Halitosis arising from the lingual dorsum secondary to overpopulated VSC-producing bacteria can be successfully managed with a combination of mechanical cleansing using tongue brushes or scrapes and chemical solutions containing essential oils, zinc chloride, and cetylpyridinium chloride.,,
Standard dental treatments and mouthwashes often recommended provide only temporary relief. Antimicrobial treatment indiscriminately depletes populations of both the problematic bacteria and those bacteria that are not thought to be implicated in halitosis, but which are likely to be important in the maintenance of a normal oral microenvironment. The outcome of antimicrobial treatment is inevitably only a temporary reduction in malodor, until the halitosis-causing bacteria become reestablished. Thus, probiotic therapy for the treatment of halitosis was applied.
Few problems arose while doing the analysis, first, the types of probiotic studied varied across the trials, second and the most important issue, the variables were not reported properly in some of the studies. Information on the outcomes of interest was only found in graphs and tables,,,,, which did not allow obtaining the exact value of the final measurement in each group. Only 11 studies contributing to the results and conclusions are a very small number compared to a large number of population affected from oral malodor. All the studies are of shorter duration varying from 24 h to 7 weeks, hence, do not throw light over the prevention aspect of probiotics over oral malodor, it still lacks the evidence even though few studies have showed significant decrease in the oral malodor parameters as in two pilot studies , have concluded that there was a significant decrease in the organoleptic scores and in production of the VSCs. A randomized clinical trial  used commercially available probiotic drink, Yakult, as a vehicle of administration of probiotic revealed no broad ecologic changes in the mouth and no significant effect on the oral malodor parameters, thus concludes that simply oral ingestion of probiotic has no effect on oral malodor.
Given the large number of internet sites dedicated to the sale of probiotic products to people with halitosis, one would anticipate that there are many well-substantiated scientific claims of the efficacy of these products. In reality, there are only countable few trials conducted to evaluate the efficacy of probiotics in the treatment of oral malodor. There are several studies which have used probiotics in adjunct with other oral prophylactic products, but exclusive use of probiotics is scarce.
Despite these limitations, we believe that this is the best possible summary of evidence of the topic. We recommend conducting trials with appropriate sample sizes to have enough power to detect differences among the groups and further extensive studies to find out the potential of the probiotics in the prevention of halitosis.
| Conclusion|| |
Based on the results of this review, the effectiveness of probiotics on the prevention and treatment of oral malodor is questionable for several studies have moderate-to-high risk of bias as there is no clear mention of the method of randomization and allocation concealment. The results of this systematic review confirm that more studies are necessary to evaluate the efficacy of probiotics with correct methodological design, in broader population samples, and over longer periods. Comparative trials of different strains of probiotic species would be recommended.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Lu DP. Halitosis: An etiologic classification, a treatment approach, and prevention. Oral Surg Oral Med Oral Pathol 1982;54:521-6.
Krespi YP, Shrime MG, Kacker A. The relationship between oral malodor and volatile sulfur compound-producing bacteria. Otolaryngol Head Neck Surg 2006;135:671-6.
Food and Health Agricultural Organization of the United Nations and World Health Organization. Guidelines for the Evaluation of Probiotics in Food. Joint 3. Food and Health Agricultural Organization/World Health Organization. Working Group Report on Drafting Guidelines for the Evaluation of Probiotics in Food; c2002. Available from: https://www.who.int/foodsafety/fs_management/en/probiotic_guidelines.pdf
. [Last accessed on 2016 Dec 14].
Lilly DM, Stillwell RH. Probiotics: Growth-promoting factors produced by microorganisms. Sci 1965;147:747-8.
Teughels W, Loozen G, Quirynen M. Do probiotics offer opportunities to manipulate the periodontal oral microbiota? J Clin Periodontol 2011;38 Suppl 11:159-77.
Gill HS. Probiotics to enhance anti-infective defences in the gastrointestinal tract. Best Pract Res Clin Gastroenterol 2003;17:755-73.
Haukioja A. Probiotics and oral health. Eur J Dent 2010;4:348-55.
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;100:754-64.
Kang MS, Kim BG, Chung J, Lee HC, Oh JS. Inhibitory effect of Weissella cibaria
isolates on the production of volatile sulphur compounds. J Clin Periodontol 2006;33:226-32.
Iwamoto T, Suzuki N, Tanabe K, Takeshita T, Hirofuji T. Effects of probiotic Lactobacillus salivarius
WB21 on halitosis and oral health: An open-label pilot trial. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2010;110:201-8.
Keller MK, Bardow A, Jensdottir T, Lykkeaa J, Twetman S. Effect of chewing gums containing the probiotic bacterium Lactobacillus reuteri
on oral malodour. Acta Odontol Scand 2012;70:246-50.
Suzuki N, Tanabe K, Takeshita T, Yoneda M, Iwamoto T, Oshiro S, et al.
Effects of oil drops containing Lactobacillus salivarius
WB21 on periodontal health and oral microbiota producing volatile sulfur compounds. J Breath Res 2012;6:017106.
Masdea L, Kulik EM, Hauser-Gerspach I, Ramseier AM, Filippi A, Waltimo T. Antimicrobial activity of Streptococcus salivarius
K12 on bacteria involved in oral malodour. Arch Oral Biol 2012;57:1041-7.
Sutula J, Coulthwaite LA, Thomas LV, Verran J. The effect of a commercial probiotic drink containing Lactobacillus casei
strain Shirota on oral health in healthy dentate people. Microb Ecol Health Dis 2013;24:21003.
Lee SH, Baek DH. Effects of Streptococcus thermophilus
on volatile sulfur compounds produced by Porphyromonas gingivalis
. Arch Oral Biol 2014;59:1205-10.
Suzuki N, Yoneda M, Tanabe K, Fujimoto A, Iha K, Seno K, et al. Lactobacillus salivarius
WB21 – Containing tablets for the treatment of oral malodor: A double-blind, randomized, placebo-controlled crossover trial. Oral Surg Oral Med Oral Pathol Oral Radiol 2014;117:462-70.
Suzuki N, Higuchi T, Nakajima M, Fujimoto A, Morita H, Yoneda M, et al.
Inhibitory effect of Enterococcus faecium
WB2000 on volatile sulfur compound production by Porphyromonas gingivalis
. Int J Dent 2016;2016:8241681.
Moon JE, Moon YM, Cho JW. The effect of Streptococcus salivarius
K12 against Prevotella intermedia
on the reduction of oral malodor. Int J Clin Prev Dent 2016;12:153-61.
Reid G; Food and Agricultural Organization of the United Nation and the WHO. The importance of guidelines in the development and application of probiotics. Curr Pharm Des 2005;11:11-6.
Gill H, Prasad J. Probiotics, immunomodulation, and health benefits. In: Bioactive Components of Milk. New York: Springer; 2008. p. 423-54.
Fuller R. Probiotics: An overview. In: Human Health. London: Springer; 1994. p. 63-73.
Bonifait L, Chandad F, Grenier D. Probiotics for oral health: Myth or reality? J Can Dent Assoc 2009;75:585-90.
Comelli EM, Guggenheim B, Stingele F, Neeser JR. Selection of dairy bacterial strains as probiotics for oral health. Eur J Oral Sci 2002;110:218-24.
Suzuki N, Tanabe K, Takeshita T, Yoneda M, Iwamoto T, Oshiro S, et al
. Effects of oil drops containing Lactobacillus salivarius WB21 on periodontal health and oral microbiota producing volatile sulfur compounds. J Breath Res 2012;6:017106.
Burton JP, Chilcott CN, Tagg JR. The rationale and potential for the reduction of oral malodour using Streptococcus salivarius
probiotics. Oral Dis 2005;11 Suppl 1:29-31.
Reid G, Jass J, Sebulsky MT, McCormick JK. Potential uses of probiotics in clinical practice. Clin Microbiol Rev 2003;16:658-72.
Bernaola Aponte G, Bada Mancilla CA, Carreazo NY, Rojas Galarza RA. Probiotics for treating persistent diarrhoea in children. Cochrane Database of Systematic Reviews 2013;(8):CD007401.
Goldenberg JZ, Yap C, Lytvyn L, Lo CK, Beardsley J, Mertz D, et al
. Probiotics for the prevention of Clostridium difficile-associated diarrhea in adults and children. Cochrane Database of Systematic Reviews 2017;(12):CD006095.
Hao Q, Dong BR, Wu T. Probiotics for preventing acute upper respiratory tract infections. Cochrane Database of Systematic Reviews 2015;(2):CD006895.
Stamatova I, Meurman JH. Probiotics and periodontal disease. Periodontol 2000 2009;51:141-51.
Bhushan J, Chachra S. Probiotics–their role in prevention of dental caries. J Oral Health Comm Dent 2010;4:78-82.
Yanine N, Araya I, Brignardello-Petersen R, Carrasco-Labra A, González A, Preciado A, et al.
Effects of probiotics in periodontal diseases: A systematic review. Clin Oral Investig 2013;17:1627-34.
Kazor CE, Mitchell PM, Lee AM, Stokes LN, Loesche WJ, Dewhirst FE, et al.
Diversity of bacterial populations on the tongue dorsa of patients with halitosis and healthy patients. J Clin Microbiol 2003;41:558-63.
Loesche WJ, Kazor C. Microbiology and treatment of halitosis. Periodontol 2000 2002;28:256-79.
De Boever EH, Loesche WJ. Assessing the contribution of anaerobic microflora of the tongue to oral malodor. J Am Dent Assoc 1995;126:1384-93.
Outhouse TL, Fedorowicz Z, Keenan JV, Al-Alawi R. A cochrane systematic review finds tongue scrapers have short-term efficacy in controlling halitosis. Gen Dent 2006;54:352-9.
Quirynen M, Avontroodt P, Soers C, Zhao H, Pauwels M, Coucke W, et al.
The efficacy of amine fluoride/stannous fluoride in the suppression of morning breath odour. J Clin Periodontol 2002;29:944-54.
McBain AJ, Bartolo RG, Catrenich CE, Charbonneau D, Ledder RG, Gilbert P. Effects of a chlorhexidine gluconate-containing mouthwash on the vitality and antimicrobial susceptibility ofin vitro
oral bacterial ecosystems. Appl Environ Microbiol 2003;69:4770-6.
Meurman JH, Stamatova I. Probiotics: Contributions to oral health. Oral Dis 2007;13:443-51.
[Table 1], [Table 2], [Table 3]