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ORIGINAL ARTICLE |
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| Year : 2022 | Volume
: 67
| Issue : 6 | Page : 651-656 |
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| Salivary antioxidants levels in patients with oral lichen planus |
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Masoomeh Shirzaiy1, Mohammad Ali Salehian2, Zohreh Dalirsani3
1 Associate Professor of Oral and Maxillofacial Medicine, Oral and Dental Disease Research Center, Zahedan University of Medical Science, Zahedan, Iran
2 Specialist of Oral and Maxillofacial Medicine, Tehran, Iran
3 Professor of Oral and Maxillofacial Medicine, Oral and Maxillofacial Diseases Research Center, Mashhad University of Medical Sciences, Mashhad, Iran
| Date of Web Publication | 23-Feb-2023 |
Correspondence Address:
Zohreh Dalirsani
Oral and Maxillofacial Diseases Research Center, Department of Oral Medicine of Mashhad Faculty of Dentistry, Vakilabad Blvd. Mashhad
Iran
 Source of Support: None, Conflict of Interest: None  | Check |
DOI: 10.4103/ijd.ijd_295_22
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 Abstract | | |
Background: Oral lichen planus (OLP) is one of the most common diseases of the oral mucosa, which exact pathogenesis remains unknown. Free radicals and reactive oxygen species could play an important role in the pathogenesis of oral lichen planus. Aims and Objectives: This study aimed to compare the salivary levels of uric acid, superoxide dismutase, glutathione peroxidase, and albumin in the patients with oral lichen planus and healthy subjects. Materials and Methods: Thirty patients with oral lichen planus and 30 healthy subjects, who were matched for age and sex, were enrolled in this case-control study. The salivary concentration of uric acid, superoxide dismutase, glutathione peroxidase, and albumin were examined in these individuals using the spectrophotometry and coulometric technique. The data were analyzed through Mann-Whitney test and T test by SPSS software (ver. 19). Results: Salivary uric acid and albumin levels in patients with oral lichen planus and healthy controls were not statistically different (p > 0.05); however, the concentrations of salivary superoxide dismutase in OLP patients (660.4 ± 266.4 U/g protein) and healthy controls (935.73 ± 561.9 U/g protein) were significantly different (p < 0/05). Also, salivary glutathione peroxidase levels in healthy controls (1049.98 ± 964.56 mU/mL) were remarkably higher than OLP patients (244.12 ± 170.78 mU/mL) (p < 0/001). Conclusion: The salivary superoxide dismutase concentration, as an indicator of antioxidant system, in OLP patients was significantly higher than healthy subjects. The glutathione peroxidase levels in these patients were remarkably lower than healthy controls. It is suggestive that these markers could be effective in pathogenesis of OLP.
Keywords: Albumin, antioxidant, glutathione peroxidase, oral lichen planus, superoxide dismutase, uric acid
How to cite this article:
Shirzaiy M, Salehian MA, Dalirsani Z. Salivary antioxidants levels in patients with oral lichen planus. Indian J Dermatol 2022;67:651-6 |
How to cite this URL:
Shirzaiy M, Salehian MA, Dalirsani Z. Salivary antioxidants levels in patients with oral lichen planus. Indian J Dermatol [serial online] 2022 [cited 2023 Mar 31];67:651-6. Available from: https://www.e-ijd.org/text.asp?2022/67/6/651/370287 |
| Introduction | |  |
Lichen planus (LP) is a chronic mucocutaneous inflammatory disease, which immune system plays a role in its development and progression.[1],[2] Skin manifestations include little and itchy red to purple papules in the extremities and are commonly self-limited.[1],[2],[3]
Oral lichen planus (OLP) is one of the most common non-infectious diseases of the oral mucosa, which affects women more than men and often occurs in people, who are in the Middle Ages. OLP usually presents bilaterally on buccal mucosa, tongue, and the gingival mucosa.[1],[2],[3]
In oral mucosa, it can present as fine white striae, or/and popular, plaque-like, erythematous (atrophic), ulcerative lesions. Although the lesions might be asymptomatic, sometimes, the patients suffer from pain or burning for several years. Moreover, OLP is a pre-malignant condition and the lesions could progress to oral cancer during the years.[1],[4]
The exact etiology of lichen planus is unknown; however, genetic background, autoimmunity, stress, dental materials, drugs, infectious factor, habits, trauma, food allergies, some systemic diseases including diabetes, bowel disease, and malignant neoplasms are reported to be associated with OLP.[5] Cellular and humoral immune deficiencies are involved in the pathogenesis of LP. Activation of the auto-cytotoxic CD8+ T cells that causes apoptosis of keratinocytes of the oral epithelium is considered as one of the primary factors in the pathogenesis of OLP.[2],[3],[5]
Some studies have proved that free radicals contribute in the pathogenesis of several diseases such as OLP. When the balance between the production of free radicals and antioxidant defense system does not exist, a situation arises that is called oxidative stress.[6],[7]
Antioxidant mechanisms are responsible for balancing oxidation-reduction. Any imbalance in antioxidant system can lead to overproduction of reactive oxygen species (ROS) and cell damage. An increase in ROS and lipid peroxides has been implicated in the pathogenesis of lichen planus.[8]
Generally, there are some enzymatic and non-enzymatic molecules in the antioxidant system. Albumin, glutathione, melatonin, mycothiol, phenolics, ascorbate, and fibrin are non-enzymatic molecules and glutathione peroxidase, glutathione reductase, glutathione-S-transferase, dehydroascorbate reductases, NADPH oxidase, peroxiredoxin, superoxide dismutase, alpha-dioxygenase, ascorbate peroxidase, and catalase are enzymatic elements, which are effective in antioxidant system.[9] Assessment of antioxidants elements could be effective in evaluation of ability of antioxidant system in protection of body cells from oxidative damage.
Glutathione peroxidase and superoxide dismutase in combination with other enzymes have an important role in protection of cells from damage related to reactive oxygen species.[10]
Sezer et al.[11] showed an increase in the serum superoxide dismutase and a decrease in the serum erythrocyte catalase levels in lichen planus patients as compared to control group.
In a study conducted by Hassan et al.[8] in Kashmir, levels of malondialdehyde (MDA), nitric oxide (NO), and superoxide dismutase (SOD) were higher in patients with OLP comparing to the control group, while plasma levels of reduced glutathione (GSH) and glutathione peroxidase (GPx) were lower in the patient group comparing the control group. Superoxide dismutase is an antioxidant enzyme and the first line of defense against oxidative stress.[8],[11] Oxidative agents deplete GSH, this enzyme cofactor decreases in the patients with lichen planus.[8] It is suggested that an imbalance in the antioxidant status may lead to the accumulation of H2O2 and consequently vacuolization of the basal cell layer, in lichen planus.[8]
ROS causes DNA damage, lipid peroxidation, and protein oxidation. Antioxidant elements including superoxide dismutase, glutathione peroxidase, catalase, and micronutrients such as vitamin C, vitamin E as well as trace metals counteract cellular damage due to free radicals and protect the cell membranes against oxidative damage.[12]
Respect to a remarkable relationship between salivary and serum oxidant and antioxidant levels,[13] saliva could be used for evaluation of oxidative stress levels, since collecting saliva is a safe, painless, and noninvasive procedure.[10],[13]
However, in previous studies, some antioxidant elements were evaluated in the OLP patients, a few of them were conducted on salivary antioxidant levels and reported contradictory results.[14],[15]
In respect to the role of decreased antioxidant capacity in the pathogenesis of various chronic inflammatory lesions as well as the paradoxical results about lichen planus, this study aimed to compare salivary uric acid and superoxide dismutase, glutathione peroxidase, and albumin in the patients with oral lichen planus and healthy subjects.
| Materials and Methods | | |
Since a few numbers of studies investigated the oxidant-antioxidant status in patients with OLP, the sample size was calculated based on these previous studies performed on oral type of this condition [Upadhyay[34] and Shirzad.[6]] In this case—control study, 30 erosive-atrophic OLP and 30 healthy subjects referring to Zahedan Dental School, Zahedan, Iran, over one year period (2018-2019), who met the inclusion criteria were included by simple random sampling method. All participants signed an informed consent form.
The protocol of research was approved by the Ethics Committee of Zahedan University of Medical Sciences (code: IR.ZAUMS.AC.IR.1394.160).
A checklist regarding to demographic characteristics was filled out for every subject before saliva collection.
Selection and description of participants
The erosive-atrophic OLP patients, in whom the disease was confirmed by clinical examination through an oral medicine specialist as well as histopathological evaluation, included in this study as case group. Histopathological examination was performed according to the WHO criteria modified by the American Academy of Oral and Maxillofacial Pathology (AAOMP/2016).[16] The exclusion criteria for the cases were moderate to severe dysplasia, lichenoid reaction, or lesions in close contact with amalgam fillings, pregnancy, chronic inflammatory diseases, and use of any vitamin supplements in the past three months.[17] The control group consisted of healthy individuals, who referred only for dental treatments. They did not have OLP or any other diseases, which could influence on antioxidant activity. They were without history of smoking, or taking any drugs or supplements in the past three months and were matched for age and sex with the case group [Figure 1].
Technical information
After selecting the participants, unstimulated saliva was collected by spitting method between 9 and 11 a.m. Participants were asked avoid eating, drinking, and brushing 90 minutes before sampling. In this method, the patient should be sitting down comfortably, while collecting the saliva. While leaning slightly forward, the patient drained the saliva in the tube by spitting in 1-2 times every 1 minutes for 5 minutes.[18] After collecting the saliva, the test tube was closed with the plastic cap and was transmitted to biochemistry laboratory as soon as possible. In the laboratory, saliva samples were centrifuged for 10 minutes at 2000 rpm to separate cell debris and were kept at -70 ° C. Based on the protocol presented by the kit manufacturer's company, spectrophotometric and coulometric methods were used to determine the types of salivary antioxidants. Available commercial kits for superoxide dismutase (SOD; Ransod; Randox Laboratories Ltd, UK); uric acid (UA, uric acid liquicolor, Germany), glutathione peroxidase (Ransod; Randox Laboratories Ltd, UK), and albumin (ALB, albumin liquicolor, Germany) were used.
Statistical analysis
All subjects' data were entered into SPSS software (version.19). Kolmogorov- Smirnoff test was used to assess the normal distribution of data in the two groups. For statistical analysis, T test was used for normally distributed data and for data with non-normal distribution, non-parametric test of Mann-Whitney was used. The significant level for statistical analysis was considered as 0.05.
| Results | | |
In this study, 30 patients with erosive-atrophic OLP (including 20 women (66.7%), and 10 men (33.3%)) with an age range of 30–60 years (with an average of 45 ± 7.8 years), and 30 healthy people (including 18 women (60%) and 12 men (40%)) with an age range of 28–55 (with an average of 41.5 ± 8.6 years) were studied for evaluation of some salivary antioxidants.
Salivary uric acid in the healthy subjects (4.09 ± 1 mg/dL) and subjects with oral lichen planus (4.27 ± 1.39 mg/dL) had no significant difference (p = 0.55).But salivary SOD in OLP patients (660.4 ± 266.4 U/g protein) significantly lower than healthy subjects (935.73 ± 561.9 U/g protein) (p = 0.03) [Table 1]. | Table 1: Comparison of salivary markers in healthy and oral lichen planus subjects
Click here to view |
Moreover, concentration of salivary glutathione peroxidase in the healthy controls (1049.98 ± 964.56 mU/mL) was remarkably higher than OLP patients (244.12 ± 170.78 mU/mL) (p < 0.001). Also, statistical analysis did not show any significant difference between two groups regarding to salivary albumin levels (p = 0.12).
The mean salivary antioxidants in studied population with respect to gender have been shown in [Table 2]. | Table 2: Comparison of salivary markers in healthy and oral lichen planus subjects regarding to the gender
Click here to view |
The amounts of uric acid in healthy males and females, as well as, in OLP men and women, were not any significant difference (p = 0.96, P = 0.97, respectively).
Also, the SOD levels in healthy men and women were not different (p = 0.09), the concentrations of this factor in OLP patients were not significantly different, regarding to the gender (P = 0.63) [Table 2].
Mann-Whitney showed that salivary GPx in the healthy men was remarkably higher than healthy women (p = 0.01), although Mann-Whitney revealed that salivary albumin in the healthy women was insignificantly higher than healthy men (p = 0.07) [Table 2].
| Discussion | | |
Free radicals are atoms or molecules, which are highly reactive in the body, could cause extended damage to the macromolecules of the living body such as nucleic acids, amino acids, lipids, and carbohydrates. There are specific systems in the body to deal with the damage of free radicals that are known as the antioxidant defense systems.[19],[20],[21] The antioxidant system is very complex and includes a variety of molecules and enzymes, which exist as intracellular and extracellular in the biological fluids such as plasma or saliva. Activity of some enzymatic factors including superoxide dismutase, catalase, and glutathione peroxidase protects the cells from free radicals damages.[22]
A variety of reactive oxygen species are produced by cells such as keratinocytes and inflammatory cells. Overproduction of reactive oxygen species, which is produced following oxidation-reduction imbalance, causes some changes in the proteins, lipids, and DNA and disturbs cellular function.[6],[23],[24]
Increased cellular damage is caused by oxidative stress and/or antioxidant system failure.[25] Measuring productions due to oxidative stress is used as a method to determine the antioxidant status. Given that the ROS activity increases during oxidative stress and free-radical-scavenging antioxidants are more consumed during oxidative stress, the activity of antioxidant components can indirectly indicate the rate of oxidative stress.[6],[24]
Some studies have shown that an imbalance between the production of free radicals and antioxidants is related to the pathogenesis of several conditions, including smoking, autoimmune, cardiovascular, periodontal, and mucocutaneous diseases.[7],[18],[25],[26],[27]
The role of oxidative stress in the etiology of lichen planus as an autoimmune disease has been studied and suggested that oxidative stress could be involved in the pathogenesis of the lichen planus.[11],[28] Rationally, in lichen planus, the inflammatory cellular infiltrate due to D4+ lymphocytes is a potential source of reactive oxygen species;[29] therefore, oxidant-antioxidant imbalance could be effective in the pathogenesis of lichen planus.[12]
Two mechanisms are suggested for pathophysiology of lichen planus: firstly, inflammatory cells, which are localized within the epithelium layer, release reactive oxygen species, which damage the cutaneous or mucosal cells. Secondly, cytokines and endotoxins stimulate keratinocytes to produce ROS.[25],[30]
A decrease in antioxidant defense and an increase in oxidant levels is associated with oxidative damage to the lipids, DNA, and proteins in OLP patients.[6],[25] In these patients, an increase in ROS or antioxidant system failure is responsible for process of oxidative stress.[6],[31] Although measuring a single element of antioxidant system alone may not be indicative of antioxidant status, evaluation of several antioxidants is expensive, difficult, and time-consuming. Therefore, the studies have been performed on special factors contributing in the antioxidant system. Some elements contributing in the antioxidant system have been assessed in previous study on LP patients. One of these elements is superoxide dismutase enzyme. Superoxide anions (SOA), which are produced from molecular oxygen, are the most common reactive oxygen species. Action of superoxide dismutase leads to conversion of superoxide anions to hydrogen peroxide, consequently it plays an important role in antioxidant system.[32]
In Hassan's study performed in Kashmir, plasma superoxide dismutase, malondialdehyde, and nitric oxide concentrations increased in OLP patients; however, that study revealed that plasma levels of glutathione (GSH) and glutathione peroxidase (GPx) reduced in the OLP patients compared to the controls.[8]
Furthermore, Aly et al.,[20] who compared the status of oxidative stress in OLP patients and healthy subjects, found an increase in the serum nitric oxide (NO), malondialdehyde (MDA), and superoxide dismutase (SOD) levels and a decrease in erythrocyte catalase levels in OLP patients as compared to the control persons, which indicate an imbalance in the antioxidant defense system in these patients. In another study, an increase in malondialdehyde concentration and a decrease in total antioxidant levels were observed in lichen planus and oral lichenoid reaction lesions.[33]
Also, in Sezer's study serum, SOD concentration in LP patients increased and erythrocyte catalase levels significantly decreased as compared to the controls. They concluded that in the LP patients an increase in oxidative stress and lipid peroxidation and consequently an imbalance in the antioxidant defense system were observed that could contribute in the pathogenesis of lichen planus.[11]
In contrast, in the present study, salivary SOD concentration in OLP patients was lower than the healthy controls. Different mean age and genetic properties of the participants and various assessed fluid samples could explain the contradictory results of the current study with others studies.[8],[20]
Also, uric acid was another antioxidant element evaluated in the present study. This molecule, which plays an role as a scavenging free radical,[34],[35] is one of indicators of salivary antioxidant capacity and might change in some diseases related to oxidative stress.[36]
In a similar study conducted by Barikbin et al.[15] compared the levels of salivary uric acid in 30 OLP patients and 30 healthy controls and showed that the levels of uric acid in healthy subjects and patients with OLP was not significantly different. Unlike the present study, Battino et al.[14] evaluated uric acid concentration in 20 patients with oral lichen planus and 20 healthy controls and found that the salivary uric acid in OLP patients remarkably decreased and total antioxidant capacity increased compared to the control group.
Moreover, in the present study, glutathione peroxidase levels in healthy controls were remarkably higher than OLP patients. In Hassan's study, plasma glutathione peroxidase levels were lower in lichen planus patients as compared to healthy controls,[8] which is in accordance with our study results performed on salivary samples. Also, Scrobotă et al.[37] revealed that the glutathione concentration in biotic specimens of OLP lesions was lower than normal mucosa of controls.
Glutathione peroxidase is an enzyme that acts as the first line of defense against oxidative stress and needs to glutathione as a cofactor for its function. This enzyme scavenges free radicals in both spontaneous and catalytic reactions.[38],[39]
During oxidative stress, the ratio of reduced glutathione to oxidized glutathione has been modified. It seems that high concentration of H2O2 exists in the site of oral lesions, which leads to glutathione peroxidase consume glutathione; therefore, the glutathione concentration decreases. On the other hand, oxidative stress causes some damages to glutathione and glutathione peroxidase, consequently, the activity of glutathione peroxidase could decrease in the oral cavity.[40]
The second line of defense against oxidative stress consists of radical-scavenging antioxidants, which suppress or break the chain propagation reactions. Some of these endogenous antioxidants are hydrophilic including vitamin C, uric acid, bilirubin, and albumin, while the others are lipophilic such as vitamin E and ubiquinol.[21]
A systematic review performed on oxidative stress in OLP, published in 2021, revealed that there was a decrease in total antioxidant capacity, uric acid, and vitamin C levels in the serum or saliva of OLP patients. Furthermore, an increase in 8-hydroxy-deoxyguanosine, advanced oxidation protein product, malondialdehyde, and nitric oxide levels in saliva or serum of these patients was reported in the literatures. However, in respect to heterogenicity of evidences, more comprehensive studies were recommended.[12]
In general, the previous studies suggested the idea of implication of oxidative stress in the pathogenesis of lichen planus.[8],[20] In further comprehensive studies, it is recommended to assess the effects of antioxidant elements for elaboration of treatment strategy and monitoring sessions. If the positive effects of antioxidant factors in improvement of signs and symptoms of OLP were proved, these elements could be prescribed as conjunctive treatment.
| Conclusion | | |
The findings of the present study show that levels of salivary uric acid and albumin in healthy subjects and patients with OLP were not significantly different, but the concentrations of superoxide dismutase and glutathione peroxidase in healthy subjects were significantly higher than their levels in the OLP patients. Therefore, it is suggested that any alteration in the defensive mechanism of antioxidants may contribute to the pathogenesis of this disease. It is recommended to evaluate various antioxidant levels and their correlation with OLP prognosis.
Declaration of patient consent
The authors certify that they have obtained all appropriate patient consent forms. In the form, the patient(s) has/have given his/her/their consent for his/her/their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.
Acknowledgements
The authors would like to thank Oral and Dental Disease Research Center of Zahedan University of Medical Science for the financial support.The findings described in this article are part of a graduate student's thesis.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
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[Figure 1]
[Table 1], [Table 2] |
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