Antimicrobial Efficacy of Fluoride Varnish with Quercetin against Candida albicans and Enterococcus faecalis: An In Vitro Study

Abstract

Objective Fluoride varnish is a preventive management of dental caries. Matrix metalloproteinases (MMPs) play a major role in the degradation of the extracellular matrix in the process of dental caries progression. Quercetin, a natural flavonoid, has a literature background with marked MMP inhibitor activity. Till date, there is no fluoride varnish that has both remineralizing effect and prevention of the dentin matrix breakdown at the same time. Therefore, a novel fluoride varnish containing tricalcium phosphate, quercetin, and sodium fluoride is formulated to have a greater remineralizing action while also preventing the deterioration of the dentinal matrix. So, this study aimed to evaluate the antimicrobial efficacy of the novel fluoride varnish with quercetin against Enterococcus faecalis and Candida albicans.

Materials and Methods The novel fluoride varnish with quercetin was prepared and tested for potential applications. The antimicrobial activity of the prepared fluoride varnish with quercetin at different concentrations (25, 50, and 100 μL) against oral pathogens (E. faecalis and C. albicans) was evaluated using the agar well diffusion method, protein leakage assay, cytoplasmic leakage assay, and time kill curve assay.

Results The novel fluoride varnish with quercetin showed significant inhibition zone against C. albicans and E. faecalis in the agar diffusion method. The protein leakage and cytoplasmic leakage assays showed dose-dependent relationships with increased antimicrobial action at higher concentrations of fluoride varnish with quercetin (p < 0.05).

Conclusion The novel fluoride varnish with quercetin has better antimicrobial efficacy than the commercial fluoride varnish.

Keywords

quercetin - fluoride varnish - varnish - MMP inhibitor

Introduction

Dental caries is one of the microbiological diseases affecting the oral cavity worldwide. Prevention and minimal intervention strategies, applied upon early detection of the lesion, are increasingly advocated for the management of dental caries.[1] Dental caries when left untreated usually result in loss of crown, pain, and subsequently leading to the loss of the teeth affecting the oral health-related quality of life.[2] The dental caries usually can be prevented, reversed, and treated.[3] Bacteria metabolize dietary carbohydrates, producing acids that penetrate the tooth and initiate the demineralization of hydroxyapatite, leading to the development and progression of caries. Tooth remineralization agents play a crucial role in preventing dental caries.[4]

Fluoride has been a pivotal strategy in caries prevention since the implementation of water fluoridation.[5] For many years, fluoride varnishes are used around the developed countries as it prolongs the contact of fluoride to the enamel in tooth surface.[5] A well-established negative correlation exists between the fluoride concentration in enamel and the incidence of dental caries. Fluoride ions strengthen enamel crystals, increasing their resistance to acid erosion. This not only helps remineralize early carious lesions but also provides antimicrobial benefits.[6] [7] The use of low fluoridated products like toothpaste is recommended for everyone. Fluoride varnish, gel, and solutions having high fluoride concentration are usually used in case of high caries risk.[8]

Following demineralization, dentin-derived latent matrix metalloproteinases (MMPs), specifically MMP-2, MMP-8, and MMP-9, are exposed and activated under acidic conditions. The dentin organic matrix breaks down as a result of the critical role played by active enzymes in the breakdown of collagen fibrils revealed during demineralization.[9] Quercetin is a natural flavonoid found in apples, cranberries, cherries, onions, peppers, asparagus, and medicinal herbs. The diverse biological activities of quercetin have been the primary driving force behind its use in the prevention and treatment of oral diseases.[10] In a previous study, it is mentioned that quercetin has the promising therapeutic effects on mineralized dental tissues, including remineralization and enhancement of bond strength. It shows potential as a multifunctional agent in preventing erosion and dental caries.[11]

A fluoride varnish with quercetin is formulated. The increased concentration of fluoride usually has an inhibitory effect on microorganisms.[10] Candida albicans and Enterococcus faecalis are commonly found in higher quantities in the oral cavities of children with severe early childhood caries compared with those without caries, with its presence being positively correlated with the severity of caries and the presence of Streptococcus mutans. The aim of this study is to assess the antimicrobial effectiveness of a commercially available dental varnish and a fluoride varnish containing quercetin against C. albicans and E. faecalis. The present in vitro study was designed to evaluate the antimicrobial activity of fluoride varnish with quercetin and commercial dental varnish on both C. albicans and E. faecalis thereby assessing the dual effectiveness of the fluoride varnish with enhanced antimicrobial efficacy in preventing microbial load and its potent remineralizing effect.

Materials and Methods

Study Design and Ethical Clearance

This investigation was performed as an in vitro experimental comparative research study. The institutional review board granted ethical approval before the trial began (SRB NO- SRB/SDC/PED0–2304/24/108).

Sample Size Calculation

The sample size was calculated from a similar study done by Rodrigues Neto et al using G power software with 95 power. The sample was calculated to be 12.[12]

Preparation of the Fluoride Varnish with Quercetin

To prepare fluoride varnish with quercetin, we measured 300 micrograms of sodium fluoride, 300 micrograms of tricalcium phosphate, and 100 micrograms of quercetin powder (the quercetin dihydrate powder was purchased from Sisco Research Laboratories Pvt. Ltd., with batch no: 9582531). These components were mixed with 100 micrograms of xylitol and 10 mL of ethanol, and then centrifuged at 8,000 rpm at room temperature for 15 minutes. The formulation was done using tricalcium phosphate as the primary component for remineralization. In a previous study, it is mentioned that fluoride along with tricalcium phosphate showed significantly increased remineralizing properties.[13] Xylitol was also added to the varnish as it was found to be an effective strategy as a self-applied caries-preventive agent.[14]

To assess the antimicrobial efficacy of the fluoride varnish with quercetin and the commercially available dental varnish (VOCO Profluorid varnish, United States, containing 5% sodium fluoride, xylitol, and colophony), they are subjected to the agar well diffusion method, protein leakage analysis, and cytoplasmic leakage analysis at varying concentrations to rule out the dose-dependent relationship and its varying effect on the microbial load.

Agar Well Diffusion Method

The agar well diffusion method was used to evaluate the antibacterial activity of commercial dental varnish and fluoride varnish containing quercetin. Mueller–Hinton agar plates were readied and autoclaved for 15 to 20 minutes at 121°C to sterilize them. The medium was sterilized, then cooled to room temperature before being transferred into sterile Petri dishes. Using sterile cotton swabs, an equal mixture of C. albicans and E. faecalis bacteria was applied to the agar plates. In the agar, wells measuring 9 mm in diameter were made using a sterile polystyrene tip. These wells were then filled with varying concentrations (25, 50, and 100 µg/mL) of fluoride varnish with quercetin and the commercially available dental varnish is taken as control. As a standard, an antimicrobial agent was included, like Fluconazole for fungi and Bacteria-Amoxyrite for bacteria. The plates were incubated at 37°C for 24 hours, with fungal cultures cultured for 48 hours. By measuring the diameter of the inhibitory zone surrounding the wells and recording the result in millimeters (mm) using a ruler, antimicrobial activity has been assessed as shown in [Fig. 1(A–D)] and [Fig. 2(A–D)].[15] [16]

Fig. 1 (A–D) Zone of inhibition in agar well diffusion method of C. albicans at different concentrations. (A) Zone of inhibition at 25 µg/mL. (B) Zone of inhibition at 50 µg/mL. (C) Zone of inhibition at 100 µg/mL. (D) Zone of inhibition of commercial varnish.

Fig. 2 (A–D) Zone of inhibition in agar well diffusion method of E. faecalis at different concentrations. (A) Zone of inhibition at 25 µg/mL. (B) Zone of inhibition at 50 µg/mL. (C) Zone of inhibition at 100 µg/mL. (D) Zone of inhibition of commercial varnish.

Protein Leakage Assay

The Bradford test was used to carry out the protein leakage investigation. Bacterial cells from Staphylococcus aureus, Pseudomonas aeruginosa, and Escherichia coli were subjected to various concentrations of green-produced Ag nanoparticles (AgNPs) for 24 to 48 hours. These concentrations were 25, 50, and 100 µg/mL, respectively. An antibiotic (e.g., Bacteria-Amoxyrite, Fungi-Fluconazole) was used as a standard. Following treatment, the bacterial suspension underwent centrifugation at 3,000 rpm for 10 minutes, separating a supernatant phase, which was subsequently collected. A total of 200 µL of supernatant was used for each sample and added to 96-well ELISA plates. To these, 50 µL of Bradford reagent was added and maintained for 10 minutes of incubation in a dark environment at room temperature. The sample's optical density was measured at 595 nm.[17]

Cytoplasmic Leakage Assay

In this study, we aimed to evaluate the cytoplasmic leakage of bacterial cells following treatment with fluoride varnish containing quercetin. Upon treatment of bacterial cells with NPs, cytoplasmic materials, such as DNA and protein, are released from cells. Hence, in this study, we have taken an attempt to evaluate the cytoplasmic leakage of bacterial cells upon SeNP treatment. For the estimation of DNA, microbial broth of UTI pathogens (10 mL) was cultured in MHA broth in an incubator and kept overnight. On the following day, the culture was harvested by centrifugation at 5,000 rpm for 10 minutes. The pellet was washed and resuspended in 1× phosphate-buffered saline buffer (pH 7.2). The number of the bacterial cells was adjusted to 10⁵ cells per mL. Different aliquots of cell suspensions were treated with SeNPs and incubated at room temperature for 3 and 5 hours. The bacterial culture without SeNPs was treated as control. An antibiotic (e.g., Bacteria-Amoxyrite, Fungi-Fluconazole) was used as a standard. Then, the cultures were centrifuged at 5,000 rpm for 10 minutes in an incubator and the absorbance of supernatants was recorded at 260 nm.[18]

Results

Antimicrobial Activity

The fluoride varnish prepared with quercetin and the commercially available dental fluoride varnish were evaluated for its antimicrobial activity against oral pathogens. As shown, organisms exhibited a higher zone of inhibition of 16 mm at a 100 μL concentration and 20 mm at a 100 μL concentration of the prepared fluoride varnish with quercetin for C. albicans and E. faecalis, respectively. The antimicrobial activity of the prepared fluoride varnish is dose-dependent. However, when compared with the commercial varnish, the novel fluoride varnish with quercetin showed higher antimicrobial activity.

[Table 1] shows significance testing between the groups for C. albicans. This table shows the mean, standard deviation (SD), F-value which shows the extent of significance and p-value, and ANOVA (analysis of variance) results for different treatment groups (25, 50, 100 μg/mL, and commercial varnish). A significant F-value of 64.167 (p < 0.001) suggests significant differences among the groups. [Table 2] shows multiple intergroup comparison between the groups for C. albicans. This table provides Tukey's post-hoc test results, showing pairwise comparisons between the groups, along with the 95% confidence intervals for mean differences, standard errors, t-values, and adjusted p-values. Significant differences were found between multiple groups, with the comparison of 100 μg/mL versus commercial varnish yielding the largest mean difference of 7.66 (p < 0.001). [Table 3] shows significance testing between the groups for E. faecalis. Similar to [Table 1], this table presents the mean, SD, F-value, and p-value for the different treatment groups. A significant F-value of 108.458 (p < 0.001) suggests substantial differences between the groups. [Table 4] shows multiple intergroup comparison between the groups for E. faecalis. Pairwise comparisons using Tukey's post-hoc test highlight significant differences between groups. The largest mean difference was observed between the 100 μg/mL and commercial varnish groups, with a mean difference of 11.667 (p < 0.001). These tables collectively show that the different concentrations of treatments (25, 50, 100 μg/mL) exhibit statistically significant differences in their effects on C. albicans and E. faecalis.

Table 1 Significance testing between the groups of C. albicans

Groups	Mean	SD	SE	Coefficient of variation	F	p
25 μg/mL	10.333	0.577	0.333	0.056	64.167	<0.001
50 μg/mL	12.333	0.577	0.333	0.047
100 μg/mL	16	1	0.577	0.063
Commercial varnish	8.333	0.577	0.333	0.069

Abbreviations: SD, standard deviation; SE, standard error.

Note: One-way ANOVA was used for significance testing. p ≤ 0.05 is considered to be significant.

Table 2 Multiple intergroup comparison between the groups of C. albicans

		Mean difference	95% CI for mean difference		SE	t	p Tukey
			Lower	Upper
(25 μg/mL)	(50 μg/mL)	−2	−3.849	−0.151	0.577	−3.464	0.035[*]
	(100 μg/mL)	−5.667	−7.516	−3.818	0.577	−9.815	<0.001[***]
	Commercial varnish	2	0.151	3.849	0.577	3.464	0.035[*]
(50 μg/mL)	(100 μg/mL)	−3.667	−5.516	−1.818	0.577	−6.351	<0.001[***]
	Commercial varnish	4	2.151	5.849	0.577	6.928	<0.001[***]
(100 μg/mL)	Commercial varnish	7.667	5.818	9.516	0.577	13.279	<0.001[***]

Abbreviations: CI, confidence interval; SE, standard error.

Note: *p < 0.01, ***p < 0.001. Tukey's post-hoc test was used for analysis.

Table 3 Significance testing between the groups of E. faecali s

Groups	Mean	SD	SE	Coefficient of variation	F	p
25 μg/mL	15	1	0.577	0.067	108.458	<0.001
50 μg/mL	17	1	0.577	0.059
100 μg/mL	20.333	0.577	0.333	0.028
Commercial varnish	8.667	0.577	0.333	0.067

Abbreviations: SD, standard deviation; SE, standard error.

Note: One-way ANOVA was used for significance testing. p ≤ 0.05 is considered to be significant.

Table 4 Multiple intergroup comparison between the groups of E. faecalis

		Mean difference	95% CI for mean difference		SE	t	p Tukey
			Lower	Upper
(25 μg/mL)	(50 μg/mL)	−2	−4.135	0.135	0.667	−3	0.067
	(100 μg/mL)	−5.333	−7.468	−3.198	0.667	−8	<0.001[***]
	Commercial varnish	6.333	4.198	8.468	0.667	9.5	<0.001[***]
(50 μg/mL)	(100 μg/mL)	−3.333	−5.468	−1.198	0.667	−5	0.005[**]
	Commercial varnish	8.333	6.198	10.468	0.667	12.5	<0.001[***]
(100 μg/mL)	Commercial varnish	11.667	9.532	13.802	0.667	17.5	<0.001[***]

Abbreviations: CI, confidence interval; SE, standard error.

**p < 0.01, ***p < 0.001. Tukey's post-hoc test was used for analysis.

Protein Leakage Analysis

[Fig. 3] denotes that E. Faecalis and C. albicans exhibit relatively constant levels of protein leakage in response to quercetin incorporation into fluoride varnish at all tested concentrations (25, 50, and 100 µg/mL), as well as the standard treatment, according to the protein leakage analysis results. When quercetin concentration rises, there is a discernible increase in the optical density value. This implies that fluoride varnish with quercetin causes protein leakage, that its effect does not get stronger at greater concentrations, suggesting the protein integrity. The control group provides evidence that the varnish is the cause of the observed protein leakage because it exhibits reduced optical density. Furthermore, there is no significant difference between the protein leakage analysis between the two groups.

Fig. 3 Protein leakage analysis of the fluoride varnish with quercetin and commercially available dental varnish.

Cytoplasmic Leakage Analysis

[Fig. 4] denotes greater cytoplasmic leakage, which could imply that the therapy has a stronger antibacterial action at those concentrations. To compare the efficacy of the treatment on these two species, both bacteria are examined at the same concentrations. At increasing concentrations (up to 100 µg/mL), the optical density rises, indicating that quercetin may have a dose-dependent effect on cytoplasmic leakage. Lower optical density readings in the control group imply that the cytoplasmic leakage is caused by the treatment (fluoride varnish containing quercetin). The results of this investigation show that adding quercetin to fluoride varnish can effectively cause cytoplasmic leakage in both C. albicans and E. faecalis, with the impact becoming more pronounced at increasing concentrations. This may indicate that quercetin has increasing dose-dependent antibacterial activity, making it an attractive addition in the prevention of dental caries.

Fig. 4 Cytoplasmic leakage analysis of the fluoride varnish with quercetin and the commercially available dental varnish.

Discussion

This study investigated the antibacterial and antifungal activities of fluoride varnish with quercetin against C. albicans and E. faecalis, comparing it with a standard commercial dental varnish. The assessment utilized the agar well diffusion method, protein leakage assay, and cytoplasmic leakage assay to provide a comprehensive evaluation of the antimicrobial efficacy of these varnishes.[19]

The agar well diffusion method revealed that the fluoride varnish with quercetin produced significantly larger inhibition zones for both C. albicans and E. faecalis compared with the commercial dental varnish.[20] This indicates that the addition of quercetin enhances the antimicrobial activity of fluoride varnish. Quercetin, a flavonoid with known antimicrobial properties, likely contributes to this effect by disrupting microbial cell walls and membranes, which is supported by the enhanced inhibition observed.[21] The larger inhibition zones underscore the potential of quercetin to augment fluoride varnish's effectiveness against a broad range of oral pathogens.[22]

The protein leakage assay showed that fluoride varnish with quercetin caused more significant protein leakage from microbial cells than the commercial varnish. This increased leakage suggests that quercetin enhances the varnish's ability to compromise microbial cell membrane integrity.[23] Proteins, which are crucial for microbial cell structure and function, are released when cell membranes are disrupted, leading to cell death. The greater protein leakage observed with the fluoride varnish with quercetin indicates a more effective antimicrobial action, as quercetin likely facilitates greater damage to the cell membranes of C. albicans and E. faecalis.[24]

Similarly, the cytoplasmic leakage assay revealed more pronounced leakage in cells exposed to the fluoride varnish with quercetin. This result corroborates the findings from the protein leakage assay and further supports the enhanced antimicrobial activity of the varnish with quercetin.[25] Cytoplasmic leakage is indicative of severe membrane damage, which aligns with the larger inhibition zones observed in the agar well diffusion method. The enhanced cytoplasmic leakage underscores the role of quercetin in increasing the permeability of microbial membranes, leading to more effective inhibition of microbial growth.[26]

While the commercial dental varnish demonstrated antimicrobial properties, it was less effective than the fluoride varnish with quercetin. This difference highlights the additional benefit of quercetin in enhancing the antimicrobial properties of fluoride varnish.[21] [27] The standard varnish, lacking quercetin, exhibited lower inhibition zones and less disruption of microbial integrity, suggesting that its efficacy is limited compared with the enhanced formulation.[28]

The superior antibacterial and antifungal activities of fluoride varnish with quercetin suggest that this formulation could offer significant advantages in clinical settings, particularly in managing and preventing oral infections. By combining fluoride's caries-preventive effects with quercetin's antimicrobial properties, this varnish could provide a more comprehensive approach to oral health care.

Further research, including clinical trials, is needed to confirm these in vitro findings and to evaluate the effectiveness and safety of fluoride varnish with quercetin in real-world dental applications. Such studies could provide valuable insights into the potential benefits of this enhanced varnish in preventing and managing oral infections. In summary, the study demonstrates that fluoride varnish with quercetin exhibits enhanced antimicrobial properties compared with commercial dental varnish, making it a promising candidate for improving oral infection management and prevention.

Conclusion

This study evaluated the antibacterial and antifungal efficacy of fluoride varnish combined with quercetin against C. albicans and E. faecalis, comparing it with a standard commercial dental varnish. Using the agar well diffusion method, protein leakage assay, and cytoplasmic leakage assay, the fluoride varnish with quercetin demonstrated significantly greater antimicrobial activity.

The agar well diffusion method showed larger inhibition zones for both C. albicans and E. faecalis with the quercetin-enhanced varnish. The protein and cytoplasmic leakage assays further confirmed that this varnish caused more extensive disruption of microbial cell membranes.

In contrast, the commercial dental varnish was less effective in comparison. Because the structural and metabolic characteristics of each microorganism are different from those of other microorganisms, the results of studies that are related to C. albicans cannot be generalized to E. faecalis. Another issue is that the formulation properties, concentration, and release behavior of fluoride vary in different varnishes and therefore differentiate the antimicrobial effects of these products. Within the limitations of the study findings, it highlights the enhanced antimicrobial potential of fluoride varnish with quercetin, suggesting its superior capability in managing oral infections. Future clinical trials are needed to validate these in vitro results and explore the practical benefits of this enhanced varnish in dental practice.

Conflict of Interest

None declared.

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Publication History

Article published online:
25 April 2025