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Year : 2020  |  Volume : 18  |  Issue : 1  |  Page : 13-24

A systematic review of randomized trials on effects of probiotic on oral Candida

Department of Public Health Dentistry, SCB Dental College and Hospital, Cuttack, Odisha, India

Date of Submission14-Aug-2019
Date of Decision12-Sep-2019
Date of Acceptance14-Jan-2020
Date of Web Publication2-Mar-2020

Correspondence Address:
Dr. Hemamalini Rath
SCB Dental College and Hospital, Cuttack, Odisha - 753 007
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/jiaphd.jiaphd_88_19

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Oral candidiasis is caused by an unregulated overgrowth of candidal species which remains in saprophytic form under healthy conditions. Probiotics can be a biologically acceptable alternative in promoting beneficial microbial flora. This review aims to provide a potential evidence for an effect of probiotic supplementation on oral candidal count as assessed by laboratory culture in randomized controlled trials (RCTs) conducted in human. PubMed (1975 to till date), Cochrane Central Register of Controlled Trials (CENTRAL, Till August 2016, Issue– 8) and Google Scholar were searched. Randomized controlled clinical trials which compared the probiotics used as single or mixture of strains, any dosage regimen, and by any form of edible or palatable vehicle either with a placebo or other controls were selected to assess the change in oral candidal count. All the in vitro studies, animal experiments, and clinical trials which had no control group/groups in the parallel arm were excluded from our final review. We screened titles and abstracts, obtained full reports of relevant trials and independently appraised them for eligibility. A total number of nine studies were included in this review and JADAD scale was used for quality assessment. In all the included studies, oral candidal count was measured by counting the CFUs after culturing the candidal colonies on selective culture mediums. Overall, this review demonstrated that there is a lack of evidence for effects of probiotics on oral Candida in lower age group but has consistent results in elderly individuals reducing high candidal count compared to any control group.

Keywords: Candidiasis, clinical trial, mouth, oral health, probiotics, randomized controlled trial

How to cite this article:
Shah S, Rath H. A systematic review of randomized trials on effects of probiotic on oral Candida. J Indian Assoc Public Health Dent 2020;18:13-24

How to cite this URL:
Shah S, Rath H. A systematic review of randomized trials on effects of probiotic on oral Candida. J Indian Assoc Public Health Dent [serial online] 2020 [cited 2021 Oct 24];18:13-24. Available from: https://www.jiaphd.org/text.asp?2020/18/1/13/279827

  Introduction Top

Oral candidiasis is an opportunistic infectious disease of oral cavity presenting as acute candidiasis, chronic candidiasis, and angular cheilitis(stomatitis). It can be classified and diagnosed based on the clinical signs (white plaques, areas of erythema and dry mucosa, red fissures, cracking, and peeling) and site of lesions in oral cavity.[1] In most of the situation, it is limited to superficial mucosal lining and skin unless the patient is extremely immunocompromised. If left untreated, it can lead to local discomfort, altered or loss of taste sensation, aversion from food, dysphagia, resulting in poor nutrition, slow recovery, prolonged hospital stay, and is fatal in extreme cases when disseminated.[2]

The most commonly involved causative organism of candidiasis is Candida albicans which inhabits on skin and mucous membranes as normal commensal microflora (saprophytic stage). Due to some local and general predisposing factors there occurs an imbalance in host environment and instigates these fungi to undergo an unregulated overgrowth (parasitic stage) resulting in candidiasis.[3]

General factors such as extremes of age, smoking. individuals with compromised immune system (diabetes, HIV, Cushing's syndrome), hospitalized for long periods, prolonged steroid therapy, malignancies, nutritional deficiencies, and antibiotics can systemically alter the host environment precipitating oral candidiasis.[4] Other local factors such as ill-fitting dentures, oral and maxillofacial prosthesis, impaired salivary gland function, inhaled steroids, and oral cancer also predispose to this condition.[5]

Currently, a wide spectrum of anti-fungals along with antibiotics are prescribed for treating oral candidiasis, but as per the Cochrane review database 2010, sufficient evidence to come to a consensus that any single or combination of antifungal agents in effective treatment of candidiasis, is lacking.[6] Given the increasing incidence of non-C. albicans Candida species in oral infection and the development of resistance against some of the traditionally used antifungals, there is a constant need for research into new and effective agents to treat and prevent oral candidosis.[7]

Probiotics as defined by WHO are “live micro-organisms which, when administered in adequate amounts, confer a health benefit on the host”. Many decades passed and the novel medicine was not paid much attention because of the World War II. Then came the era of antibiotic resistance and search for a better alternative, led to re-discovery of probiotics and its potential health benefits. With this new outlook of medicine and its significance in treating diseases, oral conditions were also not spared. Pioneer studies were conducted on the effect of probiotics on caries, periodontitis, halitosis and later oral candidiasis as well.[8],[9],[10],[11]

As compared to antibiotics and antifungals, probiotics are involved in promoting beneficial microbial flora rather than non-specifically affecting both the non-pathogenic and pathogenic microorganism, disturbing the consonance of commensalism.[9] In recent years, number of in-vitro studies,[12],[13],[14],[15] pilot studies,[16] nonrandomized trials,[17],[18],[19],[20] randomized trials[21],[22],[23],[24],[25],[26],[27],[28],[29] and reviews[30],[31],[32],[33] have been documented stating the beneficial effect of probiotics on oral Candida but scientific literature lacks a proper overall qualitative and quantitative synthesis of the evidences about its effect on oral candidal count, thus demand for a systematic review is entitled. So, this systematic review has been undertaken to unveil the effects of probiotics on oral candidal count and discern its role as an alternative preventive modality.

  Methodology Top

A systematic review was undertaken to explore the effect of oral preparations of probiotics on oral Candida in human beings. After a thorough literature search of articles published in English language only, relevant data were extracted, and results were reported according to Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA).[34] The study protocol was previously registered with PROSPERO.

Eligibility criteria

The criteria for eligibility were participants irrespective of age, gender, geographic profile and oral health status as study population, any probiotics as intervention, alteration in count of oral Candida assessed by microbiological culture as the primary outcome, and RCT as the study design with no criteria on study duration. No limits were applied for language or time. We included randomized controlled clinical trials comparing probiotics used as single or mixture of strains, any dosage regimen and by any form of edible or palatable vehicle either with a placebo or other controls. All the in vitro studies, animal experiments and clinical trials which had no control group/groups in the parallel arm were excluded from our final review.

Search methods for identification of studies

Electronic search

An extensive and comprehensive electronic search was carried out independently by two review authors irrespective of publication status, date or language. We searched the PUBMED (1975-till date), Cochrane Central Register of Controlled Trials (CENTRAL) (The Cochrane Library– August 2016, Issue– 8) and Google Scholar. For any registered ongoing or completed but unpublished trial were searched using the following websites – ClinicalTrials.gov (http://clinicaltrial.gov/), ISRCTN (http://www.controlled-trials. com/isrctn/) and World Health Organization (WHO) International Clinical Trials Registry Platform (ICTRP) (http://www.who. int/ictrp/en/).


Abstracts of major national conferences relevant to the review subject was searched to identify trials that may have not been completed or published in full but are in agreement with our inclusion criteria. References of the recent reviews and published randomized controlled trials were cross-checked for any additional studies which were not identified by electronic searches. We contacted relevant field experts (particularly probiotics) by telephony identified from other reviews and original research. We also contacted the secretary of scientific associations dedicated to probiotic research and/or oral candidiasis. We asked the association to forward this query even to their active members. We carried out a tedious search by collecting recent souvenirs of relevant national conferences having the list of study titles presented. We contacted the various professors and departmental head of our institution involved actively in peer reviewing to provide us with any relevant research detail.

Trials' selection

SS and HR performed all the searches independently. The titles followed by abstracts from the search were screened to identify those of pertinent value to the review. In cases where we could not make a decision based on the abstract, we obtained and reviewed the full text. Duplicates were discarded after having read all the titles, abstract, and full text as and when required. An intensive analysis was done by both the authors to recognize the trials satisfying inclusion criteria and others were excluded. We resolved disagreements about trial inclusion and quality assessment by discussion and third adjudicator. Trials which were excluded after coming to consensus were mentioned in the “Characteristics of the excluded trials” [Table 1].
Table 1: Characteristics of ongoing trials

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Data extraction

Data relating to population, intervention, comparison group, and outcomes were extracted in a data extraction sheet by two investigators following PRISMA guideline. Other informations such as name of the author, year, language, country, study design, study setting, participants, intervention, comparison, inclusion and exclusion criteria, period of follow-up, results, limitations, and funding were also collected. In articles where information was not clearly reported, we contacted the primary investigator of that study for necessary information and clarification.

Quality assessment

After the final selection of the articles for the review process, a quality assessment was undertaken using “5” point scale of Jadad et al.[35] (0 = worst, 5 = best) independently by two investigators. In this scale, there are three items, i.e. randomization, blinding, and withdrawals. We gave a score of 1 point for each “yes” or 0 points for each “no.” An additional point is given if any detailed information is given regarding the three items.

  Results Top

Description of studies

We identified 246 records through searching electronic databases of which 13 records from PubMed and 11 from Cochrane search were found relevant by reading the title and abstract. We also retrieved 10 registered trials from WHO ICTRP (http://www.who.int/ictrp), ISRCTN registry (www.controlled-trials. com/isrctn) and ClinicalTrials. gov. On searching the google scholar, 4 review articles were found. The references of these review articles were searched for any record not retrieved from electronic searches.

Hand-searching of these review references, gave us 7 more articles. We also hand searched the conference proceedings, specialized journals, and conference abstracts but no extra trials were produced. We then expanded our search by contacting field experts, peer reviewers, and scientific associations for any gray literature or any unpublished record that came to their knowledge but no pertinent trial was found.

After the complete process of screening, we finally came up with 45 records and 32 after removal of the duplicates. We read the full texts of these studies and evaluated for its eligibility by inclusion and exclusion criteria. Records that were in accordance with inclusion criteria were finally selected for this systematic review. We excluded articles that were not an RCT or didn't satisfy the review PICO format or was a pilot study [Table 2].
Table 2: List of excluded studies and reason for exclusion

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All the screened ongoing clinical trials were excluded as contact details of 5 trials was not available and we received no response from the other 4 authors. Information about the trial is provided in the “Characteristics of ongoing trials” table [Table 1]. We came into consensus after discussion and 9 trials out of 45 screened records were considered for the final review [Figure 1].
Figure 1: Flow chart of systematic search

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Included studies

The trials were conducted at Finland,[21],[23],[28] New Zealand,[22] China,[29] Brazil,[24] India,[26] Sweden,[25] and Italy.[27]

Study design and method

All the included trials had a double-blinded research protocol, of which seven[1],[21],[23],[24],[25],[27],[29] used a two-arm parallel study design while the other two[26],[28] used a three-arm parallel study design. Duration for which the trials were conducted was of varied time period ranging from minimum of 1 week[26] to maximum of 2 years[28] [Table 3].
Table 3: Characteristics of included trials

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From the nine included records, eight hundred forty-one (841) participants were analysed out of nine hundred and ninety seven (997) receiving the intervention and agreeing to the eligibility criteria of their respective trials were considered for this review. The trials had participants covering every age group ranging from as small as infants of 1 month old[28] to adults of 102 years old.[25]

Participants from five studies were either health volunteers or students, school childrens, and infants.[21],[22],[26],[27],[28] Two studies had healthy elderly participants from nursing homes[25] and old people homes.[23] One trial had patients diagnosed with Candida associated stomatitis[29] and had individuals with prosthetic denture[24] [Table 3].


The included trials utilized different types of probiotics including Lactobacillus rhamnosus Scientific Name Search  GG, ATCC 53103 and Lactobacillus rhamnosus LC 705;[21]L. rhamnosus GG (ATCC 53103), L. rhamnosus LC705, and Propionibacterium freudenreichii Scientific Name Search  sspshermaniiJS;[23]Bifidobacterium animalis subsp. lactis BB-12;[28]S. salivarius M18[22]; the mixture of B. longum, L. bulgaricus and S. thermophiles;[29] combination of L. rhamnosus HS111, L. acidophilus HS101, and Bifidobacterium bifidum;[24] Probiora3 (Streptococcus oralis KJ3®, Streptococcus uberis KJ2®, and Streptococcus rattus JH145®);[26]Lactobacillus reuteri (DSM 17938 and ATCC PTA 5289;[25]La cto b a ci l l us b u l g a ri cu s and St rep t oco ccu s t h er mo P h i l u s microorganisms.[27] In three studies comparison was done with placebo, other studies had chlorhexidine and herbal oral rinse,[26] sugar substitutes,[22] cheese,[21],[23] xylitol and sorbitol,[28] and nystatin paste.[29] Characteristics of probiotics used and outcome measures in each trial is given in [Table 4].
Table 4: Characteristics of probiotics used in included studies

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Outcome measures

All nine included trials reported the difference in the growth of oral Candida in terms of colony-forming unit (CFU) on selective culture medium using various oral samples. Two trials reported the result as the percentage change in the log transformed number of CFU from the baseline. The rest of the trials reported the change in the prevalence of high Candida count but the explanation for “high candidal count varied among” the studies.

Study quality

As per Jadad et al.,[35] we scored each of the nine included trial, giving a minimum score of zero and maximum score of 5 by evaluating in terms of randomization, blinding, and description of dropouts [Table 5] and [Table 6].
Table 5: Description of quality assessment according to JADAD criteria

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Table 6: Scoring of included trials based on JADAD quality assessment criteria

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Impact factor and source of funding

We ventured this systematic review and finally came in consensus for including 9 studies. The journals corresponding to these articles were classified as per Impact Factors (IF) except one[26] which is expressed in Index Copernicus (IC) with a value of 3.99. All the included studies, those expressed in IF, had values more than 1, five had more than 2 and only two records had a score more than 4 as per the IF data of the year 2015. Six trials[21],[22],[23],[25],[28] have clearly acknowledged their source of funding and one[26] trial had only mentioned their source of intervening products provided to participants [Table 6].{Table 6}

Effects of intervention

Of the 9 included studies, we found that participant's age group was widely distributed and ambiguous.

A study conducted on infants[28] showed that there was no statistically significant differences between test and control group in terms of mucosal yeast count (P = 0.130), having similar baseline characteristics. Very few children belonging only to one of the comparison group (sorbitol) harbored mucosal yeast even 2 years after intervention [Table 3].

In studies conducted by Burton et al.[22] and Mishra et al.,[26] participants were of 5–14 years of age and showed that there was no significant difference between groups in salivary candidal levels (detail data not shown) and mean log10 CFU/ml of C. albicans, respectively.

In the study by Mishra et al.,[26] Candida albicans counts were recorded before and after intervention. The change in mean log10 CFU/ml of C. albicans in Groups A to C was 0.43 ± 0.72, 0.68 ± 1.05 and 0.22 ± 0.66 CFU/ml, respectively, and the reduction in the candidal count in probiotic and Chlorhexidine group was almost equivalent [Table 3].

In two studies,[21],[27] healthy controls of similar age group (18–37 years) were recruited and both had similar baseline characteristics between the groups. In the trial conducted by Ahola et al.[21] there was statistically significant decrease in yeast counts in 27% (P = 0.005) of all the individuals, regardless of the intervention group but the results of logistic regression shoswed a non-significant result (odds ratio [OR] =0XS. 40,0.09–1.71, P = 0.22).

The other study conducted by Petti et al.[27] showed that there was no significant differences for Candida between groups but differences in proportion of participants in test and control subgroups is significant (P = 0.0001), indicating that irrespective of intervention lower values of Candida was found during the study period (Phase – 2) [Table 3].

From all the included studies, 3 trials[23],[24],[25] were conducted on elderly individuals (60–102 years), of which participants in one study[24] are denture wearer but baseline characteristics considered for each study was the same and significant difference was found between groups in all the three trials [Table 3].

Result of the study carried by Hatakka et al.[23] showed that prevalence of a high salivary yeast count (>104 CFU/mL) decreased in the probiotic group from 30% to 21% (32% reduction) and increased in the control group from 28% to 34%. Probiotic intervention reduced the risk of high yeast counts by 75% (OR = 0.25, 95% confidence interval [CI]-0.10–0.65, P = 0.004) and the risk of hyposalivation by 56% (OR = 0.44, 95% CI-0.19–1.01, P = 0.05).

Ishikawa et al.[24] showed that detection rate of Candida spp. was 92.0% in the placebo group after the experimental period, whereas it was reduced to 16.7% in the probiotic group. The reduction promoted by the probiotic regimen was independent of baseline characteristics whereas in the third study[25] on elderly individuals revealed that there was a statistically significant reduction in the prevalence of high Candida counts in the probiotic group but not in the placebo group, and the difference was statistically significant in both saliva and plaque (P < 0.05) [Table 3].

One of the included studies[29] had a very wide age range (18–75 years) and the participants are not healthy controls instead individuals with Candida-associated stomatitis. This trial reported that detection rate of Candida spp. was 100% before treatment and 8.21% in the experimental group and 34.6% in the control group after treatment. The detection rate of Candida spp. decreased (P < 0.001) in both groups and was significantly lower in the probiotic group than the control group (P = 0.038) [Table 3]. Compliance and adverse events reported in the included trial are presented in [Table 7].
Table 7: Compliance and adverse events reported in the included trials

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  Discussion Top

This systematic review was conducted to assess the effects of probiotic bacteria on oral Candida and its adverse effects. Overall this review demonstrated that there is a lack of evidence for effects of probiotics on oral Candida in lower age group but have consistent results in elderly individuals. In all the nine included studies, oral candidal count was measured by counting the CFUs after culturing the candidal colonies on selective culture mediums, but the results were reported in different ways. Three of the studies[22],[27],[36] reported the change in the number of CFUs after intervention and the rest[21],[23],[24],[25],[28],[29] reported the change in the detection rate of candidal species after intervention. It was not possible to perform meta-analysis for this review because of the heterogeneity of the studies.

Effective reduction oral Candida count was reported in five studies.[23],[24],[25],[26],[29] Three of these studies are conducted among elderly,[23],[24],[25] one among children[26] and one among adults and elderly patients having oral candidiasis.[29] Another potential source of heterogeneity is the use of various probiotic agents which can have different impact on oral candida. All the trials used multistrain bacterial products of which lactobacillus was used in maximum number of studies followed by streptococcus strains. Probiotics were used as lozenges,[25],[29] cheese,[23] mouthwash[26] and powder form.[24] In two studies comparisons were done with placebo.[24],[25] Other studies had chlorhexidine and herbal oral rinse,[26] cheese[23] and nystatin paste[29] for comparisons.

All the study designs reported information on the baseline level of Candida. However, there is no categorization of the patients depending upon baseline risk level for oral candidiasis. Hence variation of the effectiveness with the baseline risk could not be assessed. However different population age group, different comparison group, different outcome measures, and follow-up times between these studies made it difficult to compare the results. Further, there is no data considering day to day variation in Candida count. Overall, there was not sufficient information to conclude how effective probiotics are at different risk levels.

None of the studies included in the present review comment on the rationale behind their choice of dosage, but two trials[27],[28] mentioned about the grounds over which they selected the bacterial species. As of now, it is impossible to draw any conclusions on the ideal dosage regarding effects on the oral Candida composition. Likewise, the optimal duration of intervention remains elusive. Mode of administration may also contribute to the observed impact on oral candida.

Inoculating the collected samples was also varied which made the comparison and categorization difficult. These were SDA, Nickerson, chromogenic agar, Biggy agar, and Trypton polypeptone yeast agar but Dentocult CA was used comparatively in more studies. As we know, oral cavity has many different niche harboring different microorganism, so sample collection should be done covering important and susceptible areas to avoid bias in detection and in this review, but saliva was the most common in terms of collecting samples, with few studies considering other oral sites.

Hence, homogeneity in methodological approach is also lacking. No association could be made between the compliance and the significant finding favoring the use of probiotics against oral Candida as two studies[22],[28] that reported good compliance had no significant results whereas two studies[23],[25] having significant results also had good and excellent reported compliance [Table 7]. Hence, results cannot be attributed to the compliance either.

Most of the studies did not report on other factors that might be related to the change in Candida count. Only one study[23] reported the results of logistic regression adjusting the result for other confounding variables such as baseline yeast count, salivary buffering capacity and denture wearing.

Four[22],[23],[25],[29] of nine included studies reported about any adverse events, of which gastrointestinal upset in probiotic group was detected in two studies[25],[28] [Table 7].

Overall, included trials had reasonable quality according to the JADAD assessment criteria indicating varying risk of bias. Only one trial reported among the elderly is considered to be of high quality which reported a significant effect of probiotic intervention. The rest of the trials reporting significant effect belong to moderate quality.

We were not able to access articles from other search engines except from PubMed and Cochrane (CENTRAL). We have to confine our discussion to a qualitative synthesis rather than quantitative analysis as there were very few trials and the population characteristics was unambiguous and varied widely.

After an exhaustive search we found only one review[31] on probiotics that summarizes data of animal, in vitro, and in vivo studies. It was a minireview on Therapeutic Application of Synbiotics, a Fusion of Probiotics and Prebiotics, and Biogenics as a New Concept for Oral Candida infections. In addition to clinical studies considered for review by Ohshima et al.,[31] our study reviewed five more trials[22],[26],[27],[28],[29] which was selected for this qualitative analysis, agreeing to a set of eligibility criteria. In comparison to the Ohshima et al.,[31] we selected trials with randomization, double-blinding, and having a parallel control group. As our review was purely focused on probiotics, we did not consider Prebiotics, Synbiotics, or Biogenics in our review. To the best of our knowledge, this review is the first of its kind to assess the effect of beneficial bacteria on oral candida.

  Summary and Conclusion Top

To summarize, the review revealed that topical oral probiotic preparations have inconsistent effect on oral candidal count except in elderly individuals where a significant reduction was reported, but information on the magnitude of benefit is scarce. The relative effectiveness of different types of probiotic preparations among other age groups of populations is yet to be established.

Long follow-up time trials with larger sample size with proper effect size and power are needed to establish the effectiveness of different probiotic strains and preparations related to oral Candida levels with standardized methodology for inoculation. Risk group identification with proper definition of “High Candidal count” should be done before conducting the trial as Candida is a commensal microorganism in the oral cavity. In general, different dosages should be assessed to facilitate an interpretation of the dose–response relationship of probiotic consumption on relevant outcomes, rather than on safety and viability alone.


We thank all the authors and contributors for their support and advice in collecting and organizing the information for the present review. We also declare that there was no conflict of interest.

Financial support and sponsorship


Conflicts of interest

There are no conflicts of interest.

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  [Figure 1]

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6], [Table 7]


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