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Salivary iron and Candida colonization in oral lichen planus patients undergoing topical steroid therapy

BMC Oral Health volume 25, Article number: 589 (2025) Cite this article

Abstract

Background

The most common adverse event in oral lichen planus (OLP) patients undergoing topical corticosteroid therapy is opportunistic infection with oral Candida. Oral candidiasis superimposed on OLP can worsen the patient’s symptoms and obscure the true clinical appearance making the treatment of OLP more complex and difficult. The aim of this study was to investigate the salivary iron level in OLP patients undergoing topical steroid therapy with a history of oral candidiasis compared with OLP patients undergoing topical steroid therapy without a history of oral candidiasis and healthy individuals.

Materials and methods

The 68 OLP patients treated with a topical steroid were divided into 34 OLP patients with a history of oral candidiasis, 34 OLP patients without a history of oral candidiasis and 34 healthy individuals were enrolled in the study. Unstimulated whole saliva was collected from the participants to determine the salivary iron level and to investigate the presence of oral Candida colonization.

Results

The salivary iron level was significantly higher in OLP patients undergoing topical steroid therapy with a history of oral candidiasis compared with OLP patients undergoing topical steroid therapy without a history of oral candidiasis and healthy individuals (P = 0.04 and P < 0.001, respectively). Moreover, the Candida colony count in OLP patients undergoing topical steroid therapy with a history of oral candidiasis was significantly higher compared with OLP patients undergoing topical steroid therapy without a history of oral candidiasis and healthy Individuals (P < 0.001 and P < 0.001, respectively).

Conclusion

High salivary iron level associates with a high amount of oral Candida colonization in OLP patients undergoing topical steroid therapy with a history of oral candidiasis.

Trial registration

This study was registered at the Thai Clinical Trials Registry on 2nd June 2022 (TCTR identifier: TCTR20220602006).

Peer Review reports

Introduction

Oral lichen planus (OLP) is a chronic inflammatory disorder affecting the oral epithelium. Although the exact etiology is still unknown, it is hypothesized to result from abnormal T-cell mediated immunity [1]. Several types of OLP are described in the literature, i.e., reticular, papule, plaque, atrophic, erosive and bullous, that cause different severities of signs and symptoms ranging from asymptomatic, rough oral mucosa, and a burning sensation to severe pain [2, 3]. Symptomatic OLP usually affects the daily life of the patient, especially when eating, speaking and swallowing. Currently, the effective and well-known modality in treating symptomatic OLP is topical corticosteroids due to their effectiveness in reducing the signs and symptoms of OLP and low risk of adrenal suppression [4]. However, the most common adverse event during OLP treatment with topical corticosteroids is oral candidiasis [5,6,7,8].

Candida, a polymorphic fungus, can be found as normal oral flora in the oral cavity of healthy individuals. However, disturbance in the host immune system or alterations in the oral microenvironment, such as low pH, anaerobic environment or change in the oral flora leads to the adhesion and colonization of Candida, resulting in the overgrowth of Candida and penetration into the oral mucosa [9,10,11,12]. Commensal Candida will then become an opportunistic pathogen resulting in oral candidiasis. Several local and systemic predisposing factors have been reported in the development of oral candidiasis. Local factors comprise hyposalivation, smoking, poor oral hygiene and denture wearing. Moreover, the use of topical corticosteroids increases the adhesion and growth of Candida in the oral cavity by possibly suppressing cellular immunity and phagocytosis [13,14,15]. Systemic factors include age, systemic diseases, long-term broad-spectrum antibiotics or immunosuppressive agent use and nutritional deficiency [16]. Among the various nutrients, iron has been investigated and suggested to be involved in the pathogenesis of oral Candida infection [16, 17].

Iron, a trace element, is essential for both humans and microorganisms. Iron serves as a cofactor for many proteins and enzymes that are important in numerous vital biological processes, such as cellular respiration, DNA synthesis, cell proliferation and differentiation. Alterations in iron homeostasis, resulting in either iron excess or iron deficiency, have been implicated in several diseases and influenced the risk of infection [18,19,20,21].

Although many studies have reported the association between oral candidiasis and alterations in iron status, the salivary iron level in OLP patients undergoing topical corticosteroid therapy with a history of oral candidiasis has not been clarified. Therefore, the aim of this study was to investigate the salivary iron level in OLP patients undergoing topical corticosteroid therapy with a history of oral candidiasis compared with OLP patients undergoing topical corticosteroid therapy without a history of oral candidiasis and healthy individuals.

Materials and methods

Study population

The participants were recruited randomly from patients diagnosed with OLP based on the clinical presentation and histopathological examination using the modified WHO diagnostic criteria 2003 [22] and healthy volunteers at the Dental Hospital, Faculty of Dentistry, Chulalongkorn University during October 2020 to February 2022. The sample size determination using a formula to estimate the sample size for comparing the difference between two independent means was performed with G power program version 3.1.9.7. The calculation based on the mean salivary iron level and oral Candida carriage levels from a previous study [23] with alpha = 0.05 and power of 80%, indicated that 34 participants were required per group. Sixty-eight OLP patients without a history of oral candidiasis or with a history of oral candidiasis within 1 year diagnosed based on the clinical presentation and microscopic examination were recruited in this observational study. The OLP patients were classified as atrophic or erosive type based on their clinical presentation and treated with 0.1% fluocinolone acetonide in orabase (0.1% FAO) 2–3 times/day for more than 1 month. The control group consisted of 34 healthy volunteers. The inclusion criteria were good oral hygiene and no signs of oral candidiasis at the beginning of the study, no history of any disease or medical condition predisposing them to oral candidiasis or the promotion of Candida carriage, and no history of taking antifungal agents and iron supplement, using an antiseptic mouthwash, or smoking for within 1 month prior to the study. The exclusion criteria were bleeding in the oral cavity and an unstimulated salivary flow rate < 0.1 ml/min.

Saliva collection

The participants were asked to refrain from eating, drinking and performing oral hygiene for 2 h before saliva collection and the appointments were scheduled at similar times of the day. Unstimulated whole saliva was collected by asking each participant to keep their mouth slightly open and allow the saliva to drain into a sterilized tube until reaching a volume of 2 ml or 10 min had passed. After measuring the salivary flow rate, 1 ml of the collected saliva was placed into a sterilized microtube for Candida culture and the rest was centrifuged at 16,000 rpm, 4 ºC for 15 min. The clear saliva samples were stored at − 80 ºC for iron level measurement.

Candida culture

The collected saliva (100 µl or 500 µl) was spread onto Sabouraud dextrose agar (Oxoid, United Kingdom) and incubated at 37 ºC for 48 h. The number of Candida colonies from each culture plate was counted and calculated as the colony-forming units (CFU)/ml. To identify the Candida species, the Candida colonies from the Sabouraud dextrose agar plate were transferred to chromogenic candida agar (Oxoid, United Kingdom) and incubated at 37 ºC for 48 h, after which the Candida species were identified from the colony color according to the manufacturer’s indicator.

Salivary iron level measurement

500 µl of each saliva sample was transferred to a 25 ml volumetric flask and diluted with 1% nitric acid before the iron level was determined by Inductively Couple Plasma-Optical Emission Spectrometry (ICP-OES). The iron concentrations in the saliva samples were determined from a calibration curve of an iron standard solution.

Statistical analysis

Data analysis was performed using the Statistical Package for the Social Science (SPSS) version 28 (IBM Corporation, Armonk, NY, USA). The Kolmogorov–Smirnov test was used to assess the normality of the data distribution. The Kruskal–Wallis test was selected to compare the salivary iron level, the geometric means of the colony-forming units in logarithmic notation and the salivary flow rate. The prevalence of oral Candida was also compared between the groups using the Pearson chi-square test. P-values < 0.05 were considered statistically significance.

Results

Participant demographics

Sixty-eight OLP patients were enrolled in this study. The majority of the OLP patients were female (82%) and most of the OLP patients presented with atrophic oral lesions (94%). The 34 OLP patients without a history of oral candidiasis comprised 5 males and 29 females with a mean age of 53.32 ± 11.17 years (range 28–72 years) and the group of OLP patients with a history of oral candidiasis consisted of 7 males and 27 females with a mean age of 60.74 ± 9.75 years (range 32–79 years). The healthy volunteer group consisted of 12 males and 22 females with a mean age of 45.21 ± 11.98 years (range 29–63 years). The average duration of 0.1% FAO treatment in the OLP patients without a history of oral candidiasis and the OLP patients with a history of oral candidiasis was 3.23 ± 3.42 years (range 0.3–14 years) and 4.37 ± 4.28 years (range 0.1–14.8 years), respectively. The participant characteristics are summarized in Table 1.

Table 1 Participant characteristics
Full size table

Salivary iron level

The level of iron in the saliva in each group was analyzed. The mean salivary iron level in the OLP patients without a history of oral candidiasis, the OLP patients with a history of oral candidiasis and healthy individuals was 0.35 ± 0.18, 0.42 ± 0.19 and 0.31 ± 0.22 ppm, respectively. The salivary iron level was significantly different among the groups (P < 0.001). The salivary iron level was significantly higher in the OLP patients undergoing topical steroid therapy with a history of oral candidiasis compared with the OLP patients undergoing topical steroid therapy without a history of oral candidiasis and healthy individuals (P = 0.04 and P < 0.001, respectively). Moreover, there was a significantly higher salivary iron level in the OLP patients without a history of oral candidiasis compared with healthy individuals (P = 0.04) (Table 2).

Table 2 Salivary iron concentrations
Full size table

Prevalence of salivary Candida species

Eleven (32%) OLP patients undergoing topical steroid therapy without a history of oral candidiasis, 28 (82%) OLP patients undergoing topical steroid therapy with a history of oral candidiasis and 15 (44%) healthy individuals had positive Candida cultures. The prevalence of salivary Candida was significantly higher in OLP patients undergoing topical steroid therapy with a history of oral candidiasis compared with OLP patients undergoing topical steroid therapy without a history of oral candidiasis and healthy individuals (P < 0.001 and P < 0.001, respectively). However, there was no significant difference between the prevalence of salivary Candida in OLP patients without a history of oral candidiasis and healthy individuals (P = 0.32). Two Candida species were isolated from the participants’ saliva. Candida albicans was the most frequently isolated Candida species detected among the participants. In contrast, multiple Candida species, Candida albicans and Candida krusei were observed from 2 (7%) OLP patients undergoing topical steroid therapy with a history of oral candidiasis and 1 (7%) healthy individual (Table 3).

Table 3 Candida species isolation from saliva OLP patients and healthy volunteers
Full size table

Oral Candida colonization

To determine the presence of oral Candida, the number of colony-forming units from the salivary cultures were calculated and presented in logarithmic notation. The mean amount of Candida in the saliva of OLP patients undergoing topical steroid therapy without a history of oral candidiasis, OLP patients undergoing topical steroid therapy with a history of oral candidiasis and healthy individuals was 0.41 ± 0.70 log CFU/ml, 1.5 6 ± 1.09 log CFU/ml and 0.58 ± 0.81 log CFU/ml, respectively. There was a significant difference in the amount of salivary Candida in OLP patients undergoing topical steroid therapy with a history of oral candidiasis compared with OLP patients undergoing topical steroid therapy without a history of oral candidiasis and healthy individuals (P < 0.001 and P < 0.001, respectively). Importantly, the statistical analysis demonstrated no significant difference between the amount of salivary Candida in the OLP patients without a history of oral candidiasis and healthy individuals (P = 0.36) (Table 4).

Table 4 Candida colonization in the saliva of the OLP patients and healthy volunteers
Full size table

Salivary flow rate

The mean salivary flow rate in the OLP patients undergoing topical steroid therapy without a history of oral candidiasis, OLP patients undergoing topical steroid therapy with history of oral candidiasis and healthy individuals was 0.28 ± 0.17, 0.29 ± 0.26 and 0.44 ± 0.30 ml/min, respectively. There was a significantly lower decrease in the salivary flow rate in both OLP patients undergoing topical steroid therapy groups compared with healthy individuals (P = 0.004 and P = 0.02). However, the salivary flow rate between the OLP patients undergoing topical steroid therapy without a history of oral candidiasis and the OLP patients undergoing topical steroid therapy with a history of oral candidiasis was not significantly different (P = 0.61) (Table 5).

Table 5 Salivary flow rate
Full size table

Discussion

Iron is required in cellular activities and fundamental processes, including immune function and host defense. Thus, dysregulation in iron metabolism can affect the host-immune response and lead to several diseases. Decreased iron levels may impair immune cell proliferation and activation however, increased iron levels may enhance the growth of several pathogens by iron acquisition systems influencing the risk of infection [18, 24]. Under high iron condition, fungal pathogens, especially Candida albicans, possess an alternative oxidase (AOX) that protect the mitochondrion from high iron-induced reactive oxygen species (ROS) resulting in enhanced fungal pathogen growth [25]. A murine model study also reported a significantly higher level of the Candida albicans CAI4 strain in the tongue, stomach and intestine tissue of high iron mice compared with the untreated control mice [26].

Iron is a crucial active element for the activity of transferrin in inhibiting the occurrence of oral Candida infection. Interestingly, previous studies of salivary lactoferrrin, one of the transferrin proteins, and salivary iron showed no meaningful correlation between the level of salivary lactoferrin and salivary iron in OLP patients [27, 28]. In contrast, low serum ferritin in OLP patients was reported in a prior study [29]. Nevertheless, our study in OLP patients treated with topical corticosteroid determined that OLP patients undergoing topical corticosteroid therapy with a history of oral candidiasis had a significantly higher salivary iron level and amount of Candida colonization compared with OLP patients undergoing topical corticosteroid therapy without a history of oral candidiasis and healthy individuals.

Invading pathogens require iron, therefore, the host immune system has developed a mechanism to sequester free iron, resulting in limited iron for invading pathogens. This iron regulation mechanism is a part of innate immunity, known as nutritional immunity [21, 30]. In contrast, invading pathogens try to overcome the iron sequestration mechanism by evolving mechanisms to scavenge iron within the host, including reductive iron uptake, siderophore utilization and heme iron acquisition [21, 30, 31]. In our study, although the salivary iron level in OLP patients undergoing topical corticosteroid therapy without a history of oral candidiasis was significant higher compared with healthy individuals, there was no significant difference in the amount of Candida colonies. This may suggest that the increase in iron level in these OLP patients is still controlled by nutritional immunity, inhibiting the development of oral candidiasis in these patients.

The etiology of oral candidiasis, one of the common oral diseases, has numerous predisposing factors. Using a topical corticosteroid is well known as a potentially predisposing factor for increasing the incidence of oral Candida infection. Currently, topical corticosteroids are effective drugs that are widely used for treating OLP. However, the increased incidence of oral Candida infection in OLP patients undergoing topical corticosteroid treatment has been reported in several studies [7, 14, 32,33,34]. As found in prior studies, our study demonstrated a markedly increased prevalence of oral Candida in the OLP patients undergoing topical corticosteroid treatment. Opportunistic infection with oral Candida exacerbates the severity of OLP, causing uncomfortable symptoms and increases the treatment duration, resulting in a decrease in the remission rate of OLP lesions [35, 36].

The salivary flow rate is a predisposing factor that contributes to the pathogenesis of oral candidiasis. Saliva contains many antimicrobial proteins, such as lysozyme, lactoferrin, immunoglobulins and histatin [17]. A decreased salivary flow rate reduces the flushing mechanism of saliva and decreases the number of antimicrobial proteins that promote the adhesion and colonization of Candida to the oral epithelium leading to an increased risk of oral Candida infection [37, 38]. Our study found an association between a decreased salivary flow rate and an increased number of Candida colonies in OLP patients undergoing topical corticosteroid therapy with a history of oral candidiasis compared with healthy individuals. Although we found no significant difference in the salivary flow rate between the OLP patient groups, the Candida colony count was significantly higher in the OLP patients undergoing topical corticosteroid therapy with a history of oral candidiasis group. This may possibly relate to the importance of other predisposing factors in causing oral candidiasis.

Our results revealed the importance of higher salivary iron levels and oral Candida colonization in OLP patients undergoing topical corticosteroid therapy with a history of oral candidiasis compared with OLP patients undergoing topical corticosteroid therapy without a history of oral candidiasis. This may imply an association between a high salivary iron level and high Candida colony counts in OLP patients undergoing topical corticosteroid therapy with a history of oral candidiasis. In the present study, the eligible participants meeting the stringent selection criteria were OLP patients and healthy controls without a history of systemic disease or conditions that are known to affect oral Candida colonization or salivary iron levels. Although the strict inclusion and exclusion criteria enhanced the reliability of the findings, they limited the pool of the eligible sample population. Therefore, age and sex matching participants among the groups may be a key limitation of the present study. Furthermore, the limitation of the cross-sectional design of the present study is also a concern. Thus, we suggest that these findings should be investigated in future studies with a prospective design and matching subjects. In addition, future studies should focus on the factors that predispose to the occurrence of oral candidiasis to advance the understand of the pathogenesis of oral candidiasis to minimize the risk of oral candidiasis in patients undergoing topical corticosteroid treatment.

Conclusion

Our results indicate an association between a high salivary iron level and a high amount of oral Candida colonization in oral lichen planus patients undergoing topical corticosteroid therapy with a history of oral candidiasis.

Data availability

All data generated or analysed during this study are included in this published article.

Abbreviations

CFU:

Colony-forming units

FAO:

Fluocinolone acetonide in orabase

ICP-OES:

Inductively Couple Plasma-Optical Emission Spectrometry

OLP:

Oral lichen planus

SD:

Standard deviation

Tx:

Treatment

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Acknowledgements

We greatly appreciate the valuable advice given by Emeritus Professor Kobkan Thongprasom. We thank Dr. Kevin Tompkins for language revision of the manuscript and the participants in this study. Our thanks also go to the staff at the departments of Oral Medicine, and Biochemistry at the Faculty of Dentistry, Chulalongkorn University, Bangkok, Thailand, for their assistance.

Funding

This research was supported by the Faculty Research Grant, Faculty of Dentistry, Chulalongkorn University 2020 (DRF 64015).

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Authors and Affiliations

  1. Department of Oral Medicine, Faculty of Dentistry, Chulalongkorn University, Bangkok, Thailand

    Auranat Prachayakul, Jaranya Chadsiri & Chanwit Prapinjumrune

  2. Phakhao Hospital, Loei, Thailand

    Auranat Prachayakul

  3. Department of Biochemistry and Center of Excellence in Integrative Immuno-Microbial Biochemistry and Bioresponsive Nanomaterials, Faculty of Dentistry, Chulalongkorn University, Bangkok, Thailand

    Jeerus Sucharitakul

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  1. Auranat Prachayakul
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Contributions

AP contributed to study design, data collection, data analysis and interpretation, manuscript writing, reviewing and editing. JS contributed to conceptualization and study design, data analysis and interpretation, manuscript writing, reviewing and editing. JC contributed to data collection, data analysis and interpretation. CP contributed to conceptualization and study design, data collection, data analysis and interpretation, manuscript writing, reviewing and editing. All authors read and approved the final version of the manuscript.

Corresponding author

Correspondence to Chanwit Prapinjumrune.

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Ethics approval and consent to participate

The study protocol was approved by the Human Research Ethics Committee of the Faculty of Dentistry, Chulalongkorn University (HREC-DCU 2020–079). The study protocol was explained to the participants. Written informed consent was obtained from the subjects before participating in this study. The privacy rights of human subjects must always be observed. All methods were performed in accordance with the principles embodied in the Declaration of Helsinki and in accordance with local statutory requirements.

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The authors declare no competing interests.

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Prachayakul, A., Sucharitakul, J., Chadsiri, J. et al. Salivary iron and Candida colonization in oral lichen planus patients undergoing topical steroid therapy. BMC Oral Health 25, 589 (2025). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12903-025-05950-2

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BMC Oral Health

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