Oral candidiasis is one of the most common fungal infections affecting the oral mucosa. It is usually managed by taking antifungal medication that might result in side effects such as toxicity and drug resistance. Therefore, consumption of herbal medicine with antifungal activity and fewer side effects has become popular. This study is a systematic review to investigate the improvement and reduction of oral candidiasis symptoms by herbal compounds compared to conventional antifungal drugs.
Materials and Methods:
PubMed, Scopus, Web of Science, Cochrane, and Magiran databases were searched from 1995 to 2021 based on the keywords of the question formula – oral candidiasis (P), herbal compounds (I), antifungal drugs (C), and improvement of clinical symptoms and laboratory tests (O) – to find related randomized controlled trials (RCTs) in English and Persian languages. Related articles were extracted based on inclusion and exclusion criteria and critically appraised using the modified-CONSORT checklist. The risk of bias was also assessed using the Cochrane tool.
Results:
After removing duplicates and checking the title and abstract of the articles, 98 articles from 1995 to November 2021 of 715 were reviewed. 83 RCTs were excluded due to non-relevancy and 15 remained for critical appraisal, of which 5 articles were rejected. Finally, 10 articles were included in the systematic review. Based on the risk of bias assessment, one article had low risk, 6 articles had unclear risk, and 3 articles had a high risk of bias. Herbal compounds were applied in the form of gel in 3 articles, in the form of ointment and mouthwash in 1 and 6 articles, respectively. In terms of clinical improvement and laboratory findings, herbal compound mouthwashes and ointment did not have a significant difference from conventional antifungal drugs, but the articles related to compound gels reported variable effects (better, similar, and weaker). Furthermore, herbal compounds generally had more patient satisfaction than antifungal drugs.
Conclusion:
It seems that herbal compounds have clinical applications in the treatment of oral candidiasis and gained more patients’ satisfaction. To achieve more valid results, it is suggested to conduct more RCTs with a low risk of bias.
Oral candidiasis is one of the most prevalent fungal infections of the oral mucosa. Candida albicans – the most commonly observed species – is one of the components of normal oral microflora of 30%–50% of people. Various local and systemic factors can increase the growth of this microorganism and its pathogenicity by disrupting the balance of the microbial flora of the mouth.[1] Wearing dentures, changes in the quality and quantity of saliva, smoking, and inhalation of steroids are examples of the local factors. Systemic predisposing factors are immunodeficiency, diabetes, systemic antibiotics, hematinic deficiency, and chemotherapy.[2]
This infection is usually managed by eliminating or reducing the predisposing factors and taking antifungal drugs. Available antifungal agents for managing candidiasis belong to four drug classes: azoles, polyenes, echinocandins, and pyrimidine analogs (flucytosine). Azoles and polyenes act at the level of the fungal membrane, echinocandins on the fungal cell wall, and flucytosine impairs nucleic acid synthesis.[1] Topical antifungals such as nystatin and miconazole are at the first line of treatment.[3] However, it is not uncommon for patients to suffer from the adverse side effects of taking chemical antifungals; toxicity might occur, especially in elderly people who suffer from denture stomatitis or immunosuppressed patients who have to take antifungal drugs continuously to prevent the recurrence of fungal disease.[4,5] Moreover, drug resistance has developed because of the growing application of antifungals.[6] Furthermore, an increase in the incidence of invasive candidiasis has been reported due to the antifungal resistance of Candida species.[7]
Considering the treatment failures associated with antifungal resistance and the need to produce newer antifungals or improve existing antifungals for better efficacy and fewer side effects, the study of using plants with antifungal properties for treating candidiasis has been trending.[6] Herbal compounds have fewer adverse effects and are less expensive.[8] Herbal compounds exhibit different mechanisms of action against Candida species, including inhibition of fungal cell wall synthesis, disruption of cell membrane integrity, interference with fungal cell proliferation and metabolism, modulation of host immune responses, and attenuation of virulence factors.[4,9,10] These multifaceted mechanisms contribute to the antifungal efficacy of herbal remedies and highlight their potential as alternative therapeutic agents for candidiasis.
Therefore, this systematic review aimed to investigate the improvement of oral candidiasis by herbal compounds compared to conventional antifungal drugs.
MATERIALS AND METHODS
The present study is a systematic review of English or Persian articles comparing the effectiveness of herbal compounds with conventional antifungals in treating oral candidiasis in adults (Project ID: 3400898, Code of Ethics: IR.MUI.RESEARCH.REC.1400.439). The protocol has been also registered in Center for Reviews and Dissemination, University of York, UK with the registration number of CRD42024604440.
PICO was determined as follows:
Population: Oral candidiasis infections of adult patients
Intervention: herbal drugs in different forms such as mouthwash, gel, ointment, etc.
Comparison: Antifungal available drugs in different forms such as mouthwash, gel, and ointment (nystatin, miconazole, clotrimazole, fluconazole, ketoconazole, amphotericin B, posaconazole, and itraconazole)
Outcomes:
Primary outcome: clinical improvement including the reduction in severity of the disease based on the Newton’s classification[11] (Newton’s type I (localized erythematous), Newton’s type II (diffuse erythematous), or Newton’s type III (hyperplastic granular)), clinical cure rate, reduction of white plaque or erythema by measuring the length of the lesion or surface, pain reduction using VAS or qualitative questions, and itching
Secondary outcome: improvement of mycological analysis (reduction of Colony-Forming Unit [CFU] in culture experiments), minimum inhibitory concentration, minimal fungicidal concentration, and zone of inhibition
Safety outcome: side effects and drug tolerance by patients. English databases including Medline (via PubMed), Scopus, Web of Science, Cochrane Library, and the Persian Magiran database were searched. In the manual search, the references of the related extracted articles were checked and new related articles were added. The search protocol was developed by one of the principal investigators (BT). The search strategy is available in Appendix 1.
Inclusion and exclusion criteria
The title and abstract of the articles that were in English or Persian were reviewed. Randomized controlled trials (RCTs) that were conducted on adult (above 18 years old) patients with stomatitis with good general health or having systematic disease and tested herbal compounds compared to one of the antifungals (nystatin, miconazole, clotrimazole, etc.) were included. Studies that were conducted on animal samples or compared their herbal compounds with other substances such as chlorhexidine, triclosan, and placebo were excluded. Then, the full text of the remaining articles was extracted.
Critical appraise
Two of the researchers (BT and NG) reviewed the extracted articles. A third-party adjudicator was involved if the scores differed dramatically (more than 3 points). The modified CONSORT checklist [Appendix 2] was used for the critical appraisal of RCT articles. Articles that scored at least 70% (21 out of 30) were accepted.[12] Therefore, they were categorized as low quality or reject (scoring 20 or below), moderate quality (scoring 21–25), and high quality (Scoring 26 or more). To assess the risk of bias the Cochrane tool adapted from Higgins and Altman[13] was used [Appendix 3]. Based on this tool, five main sources of bias needed to be assessed; to address the selection bias, a description about the method used to generate the allocation sequence and to conceal the allocation sequence should be provided in the article. Performance bias might be resolved if the measures to blind trial participants and researchers have been used. Detection bias could be addressed by assessing the explanations about the measures used to blind outcome assessment from knowledge of which intervention a participant received. Attrition bias describes the completeness of outcome data for each main outcome, including attrition and exclusions from the analysis. Reporting bias states how selective outcome reporting was examined and what was found. The total bias level was judged based on the fact that how much they were to alter the results seriously.
RESULTSSearch results
After removing duplicates and checking the title and abstract of the articles, 98 articles from 1995 to November 2021 remained, and their full text was reviewed. 83 RCTs were excluded due to non-relevancy and 15 remained for critical appraisal [Figure 1].
PRISMA chart of included articles.
Results of risk of bias assessment
of the 15 remaining articles, 5 had low quality and were rejected. The major areas of losing scores were randomization, concealment of interventions, and reporting the results. In total, 10 articles were eligible, with 7 articles rated as medium and 3 as high quality. Scoring details are available in Appendix 2. The risk of bias was assessed for accepted RCTs. 1 article had low risk, 6 articles had unclear risk and 3 articles had a high risk of bias. The details are available in Table 1. Considering that most of the articles had an unclear risk, the overall risk of bias was unclear.
Risk of bias scores of the included articles
The data from accepted articles were extracted for qualitative review. It included the author, year of publication, characteristics of samples and participants, study design, description of the intervention, measured outcomes (primary, secondary, and safety), and their results are available in Table 2.
Data extracted from included articles
Out of 10 reviewed articles, the type of herbal product in 6 articles was mouthwash (in one article, in addition to mouthwash, the spray was also used for dental hygiene). In 3 articles, the products were tested in the form of gel, and in one article, ointment was used. The drugs compared in these studies were nystatin mouthwash, miconazole gel, and clotrimazole ointment, respectively. (In one article, nystatin mouthwash and miconazole gel were compared with herbal product mouthwash.)
Articles related to the mouthwash of herbal products
According to the study by de Araújo et al. in 2021, mouthwash and spray containing the essential oil of Cinnamomum zeylanicum leaves (P = 0.0339) and nystatin (P = 0.0139) both showed significant clinical effects and reduced the degree of Newton’s classification in denture stomatitis. Furthermore, the number of Candida spp. was reduced after 15 days of using the spray and mouthwash in both groups.[4]
Investigations by Gonoudi et al. in 2021 showed that after 14 days, Zataria multiflora essential oil was as effective as nystatin in reducing the size of palatal erythema (P < 0.001 for both groups) and the number of Candida colonies (P < 0.001 for both groups).[14]
The study by Eslami et al. in 2015 stated that Zingiber officinale (ginger) and nystatin mouthwashes had a similar and acceptable effect on reducing the size of erythema and treating candidiasis (P < 0.001 for both groups), but patients’ satisfaction with Z. officinale mouthwash (86.7%) was more than nystatin (13.3%). Therefore, it suggested Z. officinale mouthwash as an alternative to nystatin.[15]
The study by Najafi et al. in 2015 showed that there was no significant difference between Camellia sinensis (green tea) extract mouthwash and nystatin in reducing the size of erythema and the number of fungal colonies.[16]
Pinelli et al.’s study in 2013 showed that the effectiveness of Ricinus communis mouthwash in reducing clinical signs was the same as miconazole gel and it can be a suitable alternative to conventional treatments in institutionalized elderly. In this study, nystatin drop was the other comparison group, which after 30 days, unlike R. communis (P = 0.011) and miconazole (P = 0.018), did not show significant clinical improvement in terms of reduction in Newton’s classification degree. The number of fungal colonies did not change significantly in any of the three groups after 15 and 30 days.[17]
The study by Bakhshi et al. in 2012 introduced garlic mouthwash as a suitable replacement for nystatin due to the lack of side effects and enhanced patient satisfaction. According to this study, both groups of mouthwash had a significant effect on reducing the length (P < 0.001) and width (P < 0.0001) of erythema in different time courses. There was a significant difference between the patients’ satisfaction of the two groups (P < 0.0001), which was higher in the garlic group (85%).[10]
Articles related to the gel of herbal products
In the study by Tay et al. in 2014, the effect of Uncaria tomentosa gel was measured in comparison with miconazole gel and placebo. The severity of the disease based on Newton’s classification (P < 0.05 for all groups) and the number of fungal colonies (P < 0.05 for all groups) reduced with no significant difference among the groups. Therefore, it suggested U. tomentosa gel as an effective topical adjuvant treatment.[18]
The study by Amanlou et al. in 2006 stated that Z. multiflora essential oil gel can be used to treat denture stomatitis and has the same effect as miconazole gel. Both had improved palatal erythema and decreased the number of fungal colonies of the mucosa with no significant difference. Miconazole was more effective than Z. multiflora in decreasing the colony counts of the denture surface. Side effects were also reported in both groups.[19]
Vasconcelos et al.’s study in 2003 concluded that Punica granatum extract gel may be used as a topical antifungal in treating oral candidiasis. This product was not significantly different from miconazole gel in terms of laboratory results, but the difference between the two groups was significant in clinical response (P < 0.01) and miconazole gel performed better. Side effects were reported by all patients in the miconazole group, while there were no complaints in the P. granatum group.[20]
Articles related to the ointment of herbal products
The study by Tatapudi et al. in 2021 found that curcumin ointment (produced by the rhizome of Curcuma longa) could be an effective treatment as an alternative to clotrimazole ointment. There was no significant difference in the number of recovered patients between the two groups. The number of fungal colonies decreased after treatment in both groups, and there was no significant difference between them. Both treatments were tolerable for patients and had no side effects.[21]
DISCUSSION
The present study is a systematic review to investigate the effectiveness of herbal compounds compared to common antifungals in the treatment of oral candidiasis in terms of clinical improvement of the lesion, laboratory findings from fungal culture tests, and reported side effects by patients. Regarding the clinical improvement, herbal compounds have generally had the same effect as conventional antifungals. This was measured in different ways in the studies, such as the size of the erythema area, Newton’s classification, and the percentage of treated people. Patients with history of denture stomatitis with good general health were recruited in 8 out of ten studies. In two studies patients with systemic disease such as diabetes were also included. Most of the participants were in the age group of 18–60 years. 4 studies included also people above 60 years old.
Z. multiflora, Z. officinale, C. sinensis, and garlic mouthwashes reduced the size of oral erythema similarly to nystatin mouthwash.[10,14,16] Having a wide range of antimicrobial properties, Z. officinale is used in traditional medicine to treat many infectious diseases, and its antifungal effect on C. albicans along with anti-inflammatory and antibacterial activities can help to improve oral candidiasis.[15] In addition to its antimicrobial properties, C. sinensis has other properties such as anti-inflammatory, antioxidant, antimutagenic, and antidiabetic, which can play an important role in reducing erythema and mucosal inflammation.[16] Allicin is the most potent antimicrobial substance in garlic, which also plays a role in strengthening the immune system. This substance increases the production of cytokines and, at the same time, enhances the activity of macrophages, lymphocytes, and other cells of the immune system.[10] It has been also reported that herbal allicin from garlic might interfere with essential fungal processes, including DNA replication, protein synthesis, and energy metabolism, and could target specific molecular pathways within fungal cells, inhibiting cell proliferation and growth. In addition, herbal compounds may modulate fungal virulence factors, such as hyphal morphogenesis and adhesion to host tissues, thereby attenuating Candida pathogenicity and virulence.[9] Amanlou et al. reported that the use of Z. multiflora gel caused a more significant reduction in the level of erythema compared to miconazole gel, which could be due to the anti-inflammatory properties of this herbal compound.[19]
R. communis mouthwash and U. tomentosa gel reduced the severity of the disease based on Newton’s classification like miconazole gel.[17,18]C. zeylanicum mouthwash also had the same effect compared to nystatin mouthwash.[4] According to Pinelli et al.[17], R. communis mouthwash and miconazole gel caused clinical improvement in elderly people, whereas using nystatin drop was ineffective. This could be attributed to the resistance of C. albicans to nystatin as the first line of treatment and the low adherence of elderly patients to the treatment. The latter can be due to the bitter and unpleasant taste of nystatin, and the motor difficulties in the elderly; applying nystatin with a dropper seems to be more difficult than using R. communis mouthwash or miconazole gel.[15] Placebo, reported by Tay et al., reduced the severity of the disease with no significant difference from the U. tomentosa gel and miconazole; as a result, it cannot be confirmed that U. tomentosa gel was solely responsible for the reduction.[18]
In terms of the “percentage of people with complete clinical recovery” variable, the results were similar when comparing curcumin ointment with clotrimazole. This can be related to curcumin inhibiting the binding of Candida species to mucosal epithelial cells.[21] On the contrary, in the study by Vasconcelos et al., the miconazole group had a higher percentage of people with acceptable clinical results than the P. granatum gel group; this finding could be associated with better oral hygiene by the first group and greater adhesion of miconazole to the mucosa.[20] Laboratory findings also have reported that herbal compounds and antifungals had almost the same results. Some of these compounds exert their antifungal activity by affecting the fungal cell wall or membrane.[22] Some others prevent the adhesion of fungal cells to each other and biofilm formation.[23] Some have antibacterial properties that, along with antifungal activity, can prevent the formation of multispecies biofilms and co-infection.[4]
C. sinensis mouthwash and P. granatum gel had similar laboratory results compared to antifungals in reducing fungal colonies. Polyphenols are the main metabolites in these two plants, which have high molecular weight and can combine with other large molecules such as proteins, starch, cellulose, and alkaloids.[24] Precipitation of cell membrane proteins is the possible mechanism of the antifungal activity of these metabolites.[20]Z. multiflora essential oil mouthwash and gel acted the same as antifungals in reducing fungal colonies on the palate.[14,19] The essential oil of this plant contains thymol and carvacrol, which disrupt the integrity of the fungal cell membrane by inhibiting ergosterol biosynthesis.[22] Furthermore, they prevent cell adhesion and biofilm formation.[23] Regarding the reduction of denture surface colonies, Z. multiflora gel was less effective than miconazole gel; it seems that miconazole could penetrate denture plaque better. On the other hand, C. zeylanicum essential oil contains eugenol, which similar to the thymol and carvacrol, has antiadhesion and antibiofilm effects and also affects the fungal cell wall synthesis.[4,25] de Araújo et al. reported that the use of mouthwash and spray of this product are effective in reducing the number of mucosa and denture colonies.[4]
Pinelli et al.[17] in a study conducted on R. communis mouthwash, miconazole gel, and nystatin drop reported that despite the clinical improvement in the first two groups, the average number of fungal colonies did not decrease significantly after treatment in any of the groups. It could be partly justified by the fact that C. albicans is found in the normal oral microflora. According to studies, the colony count in 50% of carriers is about 1000 CFU/mL, while it ranges from 4000 to 20,000 CFU/mL in infected patients, and if a treatment decreases the counts from 10,000 to 20,000 CFU/mL to a few hundred could be considered successful. Moreover, non-invasive forms of Candida may grow in the culture medium. Therefore, a positive result of the cell culture does not necessarily indicate a pathogenic condition and the presence of invasive species. Another possible explanation might be related to bacterial coinfection and its role in pathogenesis. As a result of the antibacterial activity of R. communis and miconazole, clinical manifestations improved without a reduction in fungal colonies.[15,26] In the study on U. tomentosa, miconazole, and placebo, the number of fungal colonies decreased in all three groups without a significant difference. This might be associated with reducing predisposing factors – including patients’ compliance with oral hygiene and removing dentures while sleeping – as the first step in treating candidiasis.[18]
Side effects and patient satisfaction with treatment were reviewed in 6 articles. The findings of 4 articles show that herbal compounds have fewer adverse effects than usual antifungals[4,10,15,20] and one article stated that no side effects were observed in any of the groups.[21] Complaints of unpleasant taste were less frequent with using cinnamon and garlic mouthwashes than with nystatin.[4,10] According to de Araújo et al., burning and numbness were the side effects of cinnamon mouthwash and nystatin caused tongue sensitivity.[4] Bakhshi et al. reported nausea, diarrhea, anorexia, and burning as side effects of nystatin and itching for garlic mouthwash. In this study, overall patient satisfaction with garlic mouthwash was significantly higher than with nystatin.[10] The satisfaction of patients was also assessed by Eslami et al., and was reported that patients were significantly more satisfied with Z. officinale mouthwash than with nystatin as Z. officinale has gastroprotective and antiemetic effects. In contrast, nystatin caused gastrointestinal problems such as nausea and diarrhea that might result in poor patient adherence to treatment.[15] In the study by Amanlou et al., Z. multiflora gel application was associated with burning, itching, dizziness, nausea, or a bad taste in some patients (59.3%), and some patients (50%) in the miconazole group complained of burning, nausea, or a bad taste. In total, the side effects of both groups were relatively high, and this rate was higher in the Z. multiflora group.[19] Furthermore, Vasconcelos et al. reported miconazole had adverse effects on all the patients in the group, commonly nausea and gastric disorders, while there were no complications in the P. granatum gel group.[20]
It seems that mouthwashes of herbal compounds have the same performance as conventional antifungal drugs, but in the case of the gel of herbal compounds, it is not possible to declare a single conclusion and results have been variable (better, similar, and weaker). Perhaps, in addition to the antifungal activity, the effectiveness of the product in gel form depends on its ability to adhere to the oral mucosa and not be washed away by saliva. The different stickiness of the herbal compound gels that-were prepared manually in the studies- and the usual antifungal gels -that had standard formulations might have affected the retention and concentration of the product at the site and altered its effectiveness.[19,20] On the other hand, the washing effect of mouthwashes helps them reduce the overall count of fungal colonies in the mouth, thereby reducing the severity of the disease.
While there are some other systematic reviews performed on the subject of comparing herbal medicine and antifungal drugs on Candidiasis, they did not fully covered the aims of the current study; In a systematic review conducted by Li et al.[27] in 2023, they evaluated the clinical efficacy of traditional Chinese medicine compounds in the treatment of oral candidiasis and found that total effective rate of the experimental groups was better than that of the control group (chemical drugs). However, most of the articles included in their systematic review were written in Chinese and there was no clinical or objective definition of effectiveness rate provided. In another study conducted by Megawati et al. in 2021[28], articles in a 5-year interval (2016–2021) and just limited to Asian products were included. In their study also, just one clinical trial was included and the remaining articles were all in vitro studies.
Limitations
most of the articles had an unclear or high risk of bias; it is suggested to conduct more RCTs with higher accuracy in random sequence generation, allocation concealment, and blinding the personnel or outcome assessment domains to achieve more reliable results.
CONCLUSION
In general, herbal compounds with different chemical substances have a wide range of therapeutic effects that work in synergy to treat diseases.[29] In the reviewed articles, potential anti-inflammatory, antibacterial, antioxidant, analgesic, and other properties found in the investigated herbal compounds along with their antifungal activity, could improve oral candidiasis.[4,10,16] The combination of active ingredients in herbal compounds with other substances brings a biological balance and reduces toxicity and side effects. This can increase patients’ satisfaction and encourage them to complete their treatment process.[30] Factors such as safety, availability, and compatibility with the philosophy of holistic treatment that integrates emotional, mental, and spiritual levels and emphasizes the use of natural products lead to a higher acceptance of herbal compounds and a positive attitude toward them.[29,30] It is important to know that herbal medications are currently used by about 80% of the world’s population for health-related purposes, mostly by a majority of citizens at rural communities of developing countries.[31]
In addition to a suitable drug prescription and treatment method, items like the severity of the disease, patient cooperation, and elimination of local or systemic predisposing factors play a significant role in the successful treatment and prevention of recurrence. In the reviewed studies, there was no significant difference between the tested groups in terms of the initial severity of the disease; however, factors such as neglecting the treatment protocol, poor oral hygiene habits, or unreported systemic conditions by patients may have affected the effectiveness of the therapeutic intervention.[4,30]
Declaration of generative AI and AI-assisted technologies in the writing proce
No AI or AI technologies were used.
Financial support and sponsorship
This study was financially supported by the Research Vice-Chancellor of Isfahan University of Medical Sciences.
Conflicts of interest
The authors of this manuscript declare that they have no conflicts of interest, real or perceived, financial or non-financial in this article.
Search strategy
Critical appraise checklist and scores
CONSORT 2010 checklist of information to include when reporting a randomised trial*
Cochrane Collaboration’s tool for assessing risk of bias
Acknowledgment
we would like to appreciate the Research Vice-Chancellor of Isfahan University of Medical Sciences for financial and administrative support.
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