The Influence of Probiotics in Halitosis and Cariogenic Bacteria: A Systematic Review and Meta-Analysis
Abstract
:1. Introduction
2. Materials and Methods
2.1. Eligibility Criteria
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- Population: individuals with halitosis and/or carious lesions/risk factors for caries formation
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- Intervention: administration of probiotics
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- Comparison: placebo/no administration
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- Outcome: reducing halitosis parameters/improving oral health parameters
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- Study design: randomized controlled trials (RCTs)
2.2. Search Strategy
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- Probiotics AND Halitosis
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- Probiotics AND Prevention AND Oral Health
2.3. Data Management, Selection Process, and Data Collection Process
2.4. Inclusion and Exclusion Criteria
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- Full text available
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- Article available in English or Spanish
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- Published in 2013 and onwards
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- RCT performed on humans
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- Adults
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- Patients with halitosis
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- Patients with carious lesions or presenting caries formation risk factors
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- Administration of probiotics in any form
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- Assessment of at least one of the following parameters: volatile sulfur compound levels, organoleptic scores, plaque, or saliva samples to assess cariogenic bacteria counts and/or pH levels
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- In vitro studies
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- Case report studies
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- Case series studies
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- Case–control studies
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- Cross-sectional studies
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- Clinical trial studies
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- Performed on animals
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- Periimplantitis
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- Small sample sizes (n < 20)
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- Children
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- Pregnant patients
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- Patients with intellectual disability
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- Effect of probiotics on oral candida
2.5. Risk of Bias Assessment
- Bias arising from the randomization process.
- Bias due to deviations from included interventions.
- Bias due to missing outcome data.
- Bias in measurement of the outcome.
- Bias in the selection of the reported result.
2.6. Statistical Analysis
3. Results
3.1. Study Selection
3.2. Risk of Bias Assessment
3.3. Study Characteristics
3.4. Limitations
3.5. Meta-Analysis Results
4. Discussion
4.1. Probiotics as a Treatment Option for Halitosis
4.2. Probiotics as a Preventative Tool in Oral Health
4.3. The Effect of Probiotic Administration on Oral-Health-Related Quality of Life
4.4. Safety and Tolerability of Probiotic Administration
5. Conclusions
Future Expectations
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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Authors, Year | Study Design | Sample Size | Health Status | Probiotic (Administration) | Treatment Duration | Other Treatments | Oral Hygiene Instructions | Outcomes Investigated | Key Findings |
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Han et al., 2023 [20] | RCT, double-blind, placebo-controlled | n = 91 | Healthy | W. cibaria (1 tablet/night) | 2 months | None | Not mentioned | VSC levels (Oral Chroma), BBI scores, W. cibaria, psychosocial health | Probiotic administration may be considered an adjunctive treatment of halitosis. |
Lee et al., 2021 [32] | RCT, double-blind, placebo- controlled, pretest-posttest | n = 62 | Healthy | W. cibaria (1 tablet/night) | 2 months | None | Yes | Subjective halitosis, subjective oral health status, psychosocial health | Probiotic administration can help reduce subjective halitosis and improved OHQoL. |
Mousquer et al., 2020 [29] | RCT, double-blind, placebo-controlled, parallel, phase II | n = 44 | Healthy | L. salivarius (1 gum every 12 hours) | 10 days | Inulin (prebiotic) | Yes | OLT, VSC levels (Halimeter), tongue coating index, QOL | Treatment with probiotics combined or not with inulin can reduce halitosis. However, there was no significant difference between the groups. |
He et al., 2020 [21] | RCT, double-blind, placebo-controlled | n = 28 | Healthy, gingivitis or mild periodontitis | S. salivarius (2 lozenges/day) | 1 month (2-week follow-up) | None | Yes | OLT score, VSC levels (Halimeter), tongue coating, PI, PD, BI, BOP | The use of probiotics alone did not influence halitosis with tongue coating cause when the tongue coating was not removed beforehand. |
Lee et al., 2020 [22] | RCT, double-blind, placebo-controlled | n = 68 | Healthy | W. cibaria (1 tablet/night) | 2 months | None | Yes | OLT, VSC levels (Oral Chroma), BBI scores, W. cibaria | Oral ingestion of probiotics can help to reduce halitosis. |
Benic et al., 2019 [30] | Prospective RCT, triple-blind, two-arm parallel group, placebo-controlled | n = 64 | Healthy | S. salivarius (2 lozenges/day) | 1 month (3-month follow-up) | Fixed orthodontic appliances | Not mentioned | PI, GI, VSC levels (Halimeter), plaque samples, metagenomic analysis | The use of oral probiotics resulted in a reduction of halitosis in individuals with orthodontic braces; however, it did neither decrease their PIs nor GIs. |
Gurpinar et al., 2020 [23] | Prospective, multicenter, controlled RCT | n = 100 | Healthy | B. lactis, S. thermophilus, L. bulgaricus (probiotic product) | 1 month (1-month follow-up) | Tongue scraping | Yes | VSC levels (Halimeter), Winkel scores, Wood’s light scores | Tongue scraping in combination with probiotics can maintain its effect in halitosis therapy, even after cessation of the treatment. |
Soares et al., 2019 [26] | RCT, double-blind, placebo-controlled | n = 60 | Periodontitis stage III and IV, grade B and C | L. reuteri, L. salivarius, L. acidophilus (diluted with water) | 3 months (follow-up at 30, 60 and 90 days) | Periodontal therapy | Only if necessary | PPD, CAL, BOP, PI, GBI, VSC levels (TTS), OLS | Oral administration of probiotics reduced periodontal parameters and halitosis. |
Penala et al., 2015 [24] | RCT, double-blind, placebo-controlled, parallel design | n = 29 | Systemically healthy with chronic periodontitis | L. salivarius, L. reuteri (mouthwash and subgingival delivery of PB solution) | 1 month (3-month follow-up) | Full-mouth SRP (at baseline) | Yes | PD, CAL, PI, MGI, BI, ORG, PDR, CAG, BANA scores | The adjunctive use of probiotics offers clinical benefits in terms of PDR in moderate pockets and in halitosis. |
Suzuki et al., 2014 [28] | RCT, double-blind, crossover, placebo-controlled | n = 23 | Healthy | L. salivarius (3 tablets/day) | 2 weeks | None | Yes | OLT scores, VSC levels, PPD, BOP, PI, TCS, bacterial quantitative analysis | Daily consumption of tablets containing probiotic lactobacilli can help control halitosis. |
Authors, Year | Study Design | Aim of Study | Sample Size | Health Status | Probiotic (Administration) | Treatment Duration | Outcomes Investigated | Key Findings |
---|---|---|---|---|---|---|---|---|
Lin et al., 2022 [27] | RCT, single-blind, placebo-controlled | To test the effect of postbiotic and heat-killed probiotic lozenges on oral health. | n = 75 | Healthy | L. salivarius, L. paracasei, L. plantarum (3 lozenges/day) | 1 month | Oral microbiota, IgA levels, oral pathogens, plaque, and oral health questionnaire | Lozenges containing postbiotics or heat-killed probiotics may effectively enhance oral immunity, inhibit the growth of oral pathogens, and increase the quantity of beneficial oral microbiota. |
Kang et al., 2021 [31] | RCT, double-blind, placebo- controlled | To assess whether there is caries activity after the ingestion of W. cibaria. | n = 68 | Healthy | W. cibaria (1 tablet/night) | 2 months | Acidogenic potential of dental plaque (Cariview kit) | Oral probiotics are safe to consume since the Cariview test showed that there was no risk for caries activity. |
Ferrer et al., 2020 [33] | RCT, double-blind, placebo-controlled, parallel | To evaluate the clinical efficacy of S. dentisani. | n = 50 | Healthy | S. dentisani (buccoadhesive gel, applied with splints every 48 h) | 1 month (follow-up on day 15, 30, 45 post-treatment) | Plaque samples, saliva samples, odontogram, DMFT index, PI, GI and salivary flow, lactic acid, pH, electrolytes | The topic application of probiotics appears to improve oral health, such as plaque accumulation, saliva quality and salivary flow. |
Zare Javid et al., 2019 [34] | RCT, double-blind, parallel | To investigate the effect of consumption of probiotic yogurt on salivary S. mutans and lactobacilli in students with initial stages of caries. | n = 66 | Healthy | B. lactis (yoghurt, 300 g/day) | 2 weeks | Saliva samples (isolating S. mutans and lactobacilli) | It is suggested that short-term consumption of probiotic yogurt may prevent the progression of dental caries through reducing the population of cariogenic bacteria in saliva. |
Rungsri et al., 2017 [35] | Prospective RCT, double-blind | To evaluate whether short-term consumption of fermented milk containing L. rhamnosus affects levels of oral microbiota and whether it can colonize the human mouth. | n = 43 | Healthy | L. rhamnosus (fermented milk, 100 mL/day) | 1 month (1-month follow-up) | DMFT, PI, GI, saliva samples (S. mutans and lactobacilli) | The daily consumption of fermented milk containing probiotics may have beneficial effects on oral health by reducing salivary levels of cariogenic bacteria. |
Ghasemi et al., 2017 [36] | RCT | To investigate the effects of probiotic yogurts on reducing salivary S. mutans levels. | n = 50 | Healthy | L. acidophilus, B. bifidum (yoghurt, 200 g/night) | 3 weeks (1-day, two-week, 1-month follow-up) | Saliva samples (S. mutans) | Probiotic yoghurt is an effecting method to reduce salivary S. mutans counts. |
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Offenbächer, V.; Lo Giudice, R.; Nart, J.; Real-Voltas, F.; Arregui, M.; Greethurst, A.R.; Galletti, C. The Influence of Probiotics in Halitosis and Cariogenic Bacteria: A Systematic Review and Meta-Analysis. Appl. Sci. 2024, 14, 6639. https://doi.org/10.3390/app14156639
Offenbächer V, Lo Giudice R, Nart J, Real-Voltas F, Arregui M, Greethurst AR, Galletti C. The Influence of Probiotics in Halitosis and Cariogenic Bacteria: A Systematic Review and Meta-Analysis. Applied Sciences. 2024; 14(15):6639. https://doi.org/10.3390/app14156639
Chicago/Turabian StyleOffenbächer, Victoria, Roberto Lo Giudice, José Nart, Francisco Real-Voltas, María Arregui, Alice Rose Greethurst, and Cosimo Galletti. 2024. "The Influence of Probiotics in Halitosis and Cariogenic Bacteria: A Systematic Review and Meta-Analysis" Applied Sciences 14, no. 15: 6639. https://doi.org/10.3390/app14156639