PHYTOTHERAPY RESEARCH Phytother. Res. 24: 240244 (2010) Published online 7 July 2009 in Wiley InterScience (www.interscience.wiley.

com) DOI: 10.1002/ptr.2919

Efcacy of Purslane in the Treatment of Oral Lichen Planus

Farzaneh Agha-Hosseini,1,2* Katayun Borhan-Mojabi,3 Hamid-Reza Monsef-Esfahani,4 Iraj Mirzaii-Dizgah,5 Shahroo Etemad-Moghadam2 and Aida Karagah3
1 2 3

Department of Oral Medicine, Faculty of Dentistry, Tehran University of Medical Sciences, Tehran, Iran Dental Research Center, Faculty of Dentistry, Tehran University of Medical Sciences, Tehran, Iran Department of Oral Medicine, Faculty of Dentistry, Qazvin University of Medical Sciences, Qazvin, Iran 4 Department of Pharmacognosy, Faculty of Pharmacy, Tehran University of Medical Sciences, Tehran, Iran 5 Department of Physiology, Faculty of Medicine, AJA University of Medical Sciences, Tehran, Iran

This study evaluated the effectiveness of antioxidant-rich purslane in the treatment of oral lichen planus (OLP). A total of 37 biopsy-proven symptomatic OLP patients were selected for this randomized double-blind placebocontrolled trial. All subjects were divided into two groups to receive purslane (n = 20) or placebo (n = 17) for 3 months. Assessments were made at baseline, after 2 weeks and each month for 6 months, based on the visual analog scale (VAS) and clinical improvement including lesion type and size. Approximately 83% of the purslane patients showed partial to complete clinical improvement but 17% had no response. In the placebo group 17% experienced partial improvement, 73% did not respond and 10% showed worsening. According to VAS scores, a partial to complete response was observed in all purslane-treated patients, while 71%, 15% and 14% of the controls demonstrated partial response, no response and worsening of the symptoms, respectively. A signicant decrease in VAS scores was seen at the end of the study period (p < 0.001). No serious side-effects occurred in either of the groups. According to our ndings purslane is clinically effective in the treatment of OLP. Considering the lack of side-effects during the study period, it may be a favorable alternative treatment for OLP. Copyright 2009 John Wiley & Sons, Ltd.
Keywords: oral lichen planus; herbal medicine; purslane; treatment; visual analog scale; clinical trial.

INTRODUCTION Lichen planus (LP), rst described by Erasmus Wilson in 1869, is a chronic inammatory disease involving the skin and mucous membranes (Conrotto et al., 2006; Wilson, 1869; Scully et al., 2000). Three clinical subtypes including reticular, erythematous (atrophic) and erosive (ulcerated, bullous), have been recognized for oral lichen planus (OLP). Lesions of the reticular form are asymptomatic, while those presenting as atrophic and erosive types may produce various symptoms ranging from a mild burning sensation to intense pain. These latter types may also interfere with speaking and cause difculties during eating and swallowing (Scully et al., 2000; Carrozzo and Gandolfo, 1999; Eisen, 2002). Oral lichen planus is a relatively common disease and occurs in 12% of the population (Bouquot and Gorlin, 1986), with a marked female predilection. It usually affects middle-aged adults in the fth to sixth decades, but may develop in individuals of all ages (Eisen et al., 2005). Despite the controversy surrounding the malignant potential of OLP, transformation of this lesion to squamous cell carcinoma is considered an important issue for the patient (Scully et al., 2000).
* Correspondence to: Farzaneh Agha-Hosseini, Department of Oral Medicine, Faculty of Dentistry, Tehran University of Medical Sciences, Tehran, Iran. E-mail: aghahose@sina.tums.ac.ir

The etiology of lichen planus is unknown but it seems to be an immunologically mediated process, probably in response to unknown antigenic stimuli in susceptible subjects. Therefore its treatment is usually nonspecic and aims to alleviate symptoms (Carrozzo et al., 2004). Numerous therapeutic modalities have been proposed over the past few years; however because OLP is generally difcult to manage and may be resistant to topical or systemic therapies, a denitive cure has not been established (Thongprasom et al., 2007). Corticosteroids, antimicrobials, immunomodulators, phenytoin, retinoids and UV-radiation have been employed for the treatment of OLP, but they are all nonspecic and only act temporarily in resolving the lesions (Eisen et al., 2005). T-cells are suggested to play a major role in the pathogenesis of LP, but the exact mechanisms involved in its development remain unclear. Previous studies have evaluated the signicance of oxidative stress in different autoimmune and inammation-based diseases such as psoriasis and erosive lichen planus. Increased oxidative damage and reduced antioxidant defense have been shown in LP of the skin (Sezer et al., 2007) and in the lipids, DNA and proteins that constitute lesional tissues of vulvar lichen planus (Sander et al., 2005). Nitrative and oxidative stresses have been proposed to participate in inammatory-mediated carcinogenesis of OLP (Chaiyarit et al., 2005; Sander et al., 2005). A recent population-based casecontrol investigation evaluated serum levels of antioxidant micronuReceived 04 December 2008 Revised 29 April 2009 Accepted 30 April 2009

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trients in patients with this disease. A decreased amount of lycopene, but not other carotenoids, was found in atrophic-erosive types of OLP (Nagao et al., 2001). Portulaca oleracea L. or purslane is an herbaceous weed from the Portulacaceae family that contains numerous biologically active compounds including omega-3 fatty acids, minerals, -carotene, melatonin and vitamins A, C and E. This herbal medicine possesses antiinammatory, antiulcerogenic, antifungal and antioxidant properties (Movahedian et al., 2007) and has been used for urinary, digestive, febrile and infectious problems worldwide (Xiang et al., 2005). The purpose of the present study was to determine the efcacy of purslane in the treatment of oral lichen planus.

MATERIALS AND METHODS Plant collection. The aerial parts of purslane were collected in the spring from Karaj, (1200 m above sea level) located in Tehran province, Iran. A sample was authenticated by Y. Ajani and a voucher specimen (Ajani 300) was preserved in the Institute of Plants, Karaj, Iran. Total extract. Aerial parts of the plant were stabilized in boiling alcohol and extracted with an 80% ethanol solution for 3 days, with three changes of the solution. The resulting extract was ltered and evaporated under vacuum to achieve a very viscose residue. Preparation of dosage form. The plant extract was granulated with an appropriate amount of lactose and some other substances which were all inert according to the pharmaceutical study. Dried granules were lled in hard capsules, so that each contained an amount of 235 mg extract. Patients. A total of 37 patients with OLP including 21 females and 16 males were selected from those referred to the Department of Oral Medicine, Faculty of Dentistry, Tehran and Qazvin Universities of Medical Sciences from 1 April 2006 to 1 May 2008. Inclusion criteria consisted of clinical and histopathological diagnosis of OLP based on a modied denition of the World Health Organization (WHO) (van der Meij and van der Waal, 2003), an age range of 2570 years, signing an informed consent approved by the Ethics Committee of Qazvin University of Medical Sciences, availability for monthly appointments up to 6 months and the presence of symptoms such as burning or pain in and around the lesions. Participants demonstrating histological signs of dysplasia, lichenoid drug reactions, drug consumption in the past month, pregnancy or any kind of localized or systemic disease, especially renal problems were excluded from the study sample. Patients receiving immunosuppressive or immunomodulatory treatments or any kind of systemic or local drugs were either eliminated or asked to discontinue their treatment for a minimum of 1 month before entering the investigation. Procedure. The present study was a randomized double-blind placebo-controlled clinical trial. All examinations were performed by calibrated clinicians and
Copyright 2009 John Wiley & Sons, Ltd.

gender, age, medical history, symptoms, lesion type and site, disease duration and form of treatment were recorded for all participants. OLP lesions were scored according to the criteria proposed by Thongprasom et al. (1992). In brief, a lesional score (LS) of 5 was assigned to cases with white striae and an erosive area of more than 1 cm2; score 4 consisted of cases with striae and an erosive area of less than 1 cm2; scores 3 and 2 indicated samples with white striae along with erythematous areas of more and less than 1 cm2, respectively; score 1 lesions demonstrated mild white striae, only; and score 0 was allocated when there were no lesions or normal mucosa was encountered. A scaled tongue blade1 was used to assess the size of the lesions as described previously (Aghahosseini et al., 2006). All patients were randomly assigned to one of two treatment groups; 2 weeks after the biopsies were taken. The case group (n = 20 with 60 lesions) received a single dose of antioxidant-rich purslane extract in the form of 235 mg capsules, while placebo was administered with the same dosage to the control group (n = 17 with 46 lesions). All participants in both groups were examined at baseline, after 2 weeks and at months 1, 2, 3, 4, 5 and 6, in order to assess the effectiveness of treatment. During each appointment, oral examination along with photography was performed and the patients response rates were determined using the visual analogue scale (VAS) and overall clinical improvement determined by LS (Scott and Huskisson, 1976; Thongprasom et al., 1992). VAS was used to rank the severity of the subjects pain and discomfort which ranged from 0, showing no pain; to 10, demonstrating extreme pain (Scott and Huskisson, 1976). The symptomatic response (SR) for each patient was calculated by subtracting the nal VAS score from the initial score. Similarly, the clinical response (CR) was estimated through subtraction of the LSs obtained in the rst and last examination sessions. Positive and negative values were considered as improvement and worsening, respectively. Statistical analysis. Analysis and comparison of VAS scores, LSs, CR and SR rates between the two groups was performed by MannWhitney U-test. A value of p < 0.05 was considered to be statistically signicant.

RESULTS The study sample consisted of 21 females and 16 males with a mean age of 47.4 10.8 years (range 2570 years) and a total of 106 lesions. The case group consisted of nine men (48.7 9.6 years) and ten women (47.3 10.8 years) with 60 lesions, while seven men (48.9 9.2 years) and ten women (46.4 12 years) with 46 lesions formed the control group. The buccal mucosa was the most common site for OLP (52% control, 56% case); followed by the gingiva (29% control, 18% case); tongue (10% control, 23% case), labial mucosa (9% control, 1% case) and palate (no controls, 2% case). Approximately 83% of the purslane-treated patients experienced partial to complete clinical improvement but 17% had no response. In the
1

A wooden tongue blade (tongue depressor) was divided into equal 5 mm sections in order to be used as a measurement device. Phytother. Res. 24: 240244 (2010) DOI: 10.1002/ptr

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F. AGHA-HOSSEINI ET AL.

control group 17% demonstrated partial improvement, 73% did not respond and 10% showed worsening of the lesions. There was a signicant difference in CR between the two groups (p < 0.001). Comparison of CR in the case and control groups at 6 months is shown in Table 1. All purslane subjects showed complete to partial SR; however 71%, 15% and 14% of the controls experienced partial response, no response and worsening of the symptoms, respectively. A signicant difference in SR was observed between the two study groups (p < 0.001). Oral symptoms including pain and burning sensation of all participants is illustrated in Table 2. There were no side-effects in either of the groups throughout the entire study period.

DISCUSSION Oral lichen planus is a relatively common inammatory disease of squamous epithelium with an unknown etiopathogenesis. It is generally accepted that OLP is a T cell-mediated autoimmune disease, in which a bandlike inltration of lymphocytes occupies the supercial lamina propria (Eisen et al., 2005). The disease develops through antigen-presentation to CD4+ helper T-cells followed by secretion of different cytokines and activation of CD8+ cytotoxic lymphocytes. During this process, the inammatory cells generate various amounts of free radicals and reactive oxygen species (ROS) that damage lipids, proteins and nucleic acids in the surrounding cells (Sander et al., 2005; Khan et al., 2003). In addition keratinocytes can release ROS subsequent to stimulation by proinammatory cytokines and endotoxins (Sander et al., 2005). Therefore it seems that oxidative stress may have a role in the pathophysiology of OLP (Sander et al., 2005; Sezer et al., 2007).
Table 1. Clinical response in case and control groups
Control group (%) 5 5 73 17 0 0 0 0 (4, 1) Case group (%) 0 0 17 29 29 13 12 2 (0, 4)a

Clinical response 4 (4 degrees worsening) 3 (3 degrees worsening) 0 (no change) +1 (1 degree improvement) +2 (2 degrees improvement) +3 (3 degrees improvement) +4 (4 degrees improvement) Median (range)
a

Signicant according to MannWhitney test (p < 0.001).

Table 2. Symptomatic response in case and control groups

Control group (%) 14 15 71 0 0 1 (1, 1) Case group (%) 0 0 43 43 14 2 (1, 3)a

Symptomatic response 1 (1 degree worsening) 0 (no change) +1 (1 degree improvement) +2 (2 degrees improvement) +3 (3 degrees improvement) Median (range)
a

Signicant according to MannWhitney test (p < 0.001).

This is further validated by the fact that antioxidant capacity has been shown to decrease in vulvar lichen planus (Sander et al., 2005) and an imbalance in antioxidant status was reported in LP of the skin (Sezer et al., 2007). The major and most common treatment strategy for OLP is the use of immunosuppressive drugs, especially corticosteroids. Additionally numerous other agents have also been employed in the management of this disease. Nevertheless, all these medicaments have demonstrated adverse side effects, were ineffective or had temporary effects (Scully et al., 2000; Eisen et al., 2005). Thus searching for new treatment modalities with fewer side effects would be logical. The use of antioxidants has been proposed for the treatment of LP (Sander et al., 2005; Sezer et al., 2007). Retinoids (Scully et al., 1998, 2000; Nagao et al., 2001; Baudet-Pommel et al., 1991), lycopene (http://clinicaltrials.gov/ct2/show/ NCT00656214) and vitamin A (Scully et al., 1998, 2000) are antioxidants that have been previously applied for the management of lichen planus with different outcomes. To our knowledge this is the rst randomized double-blind clinical trial that evaluates the effectiveness and compliance of antioxidant-rich purslane in the treatment of OLP. According to the results a downward shift of VAS scores occurred in the purslane-treated patients at the end of the follow-up period and all participants showed partial to complete SR. This was not the case in the control subjects who demonstrated no response (15%) or even worsening (14%) of the lesions. The study also showed a signicant difference in clinical response between patients receiving purslane and placebo, which included a decrease in lesion size and transformation of erosive to atrophic or reticular forms. This demonstrates a quick and prominent benecial effect in controlling symptoms related to OLP. It is noteworthy that a complete response was observed in one reticular lesion at the end of the study period. Despite the fact that reticular OLP is asymptomatic, there is always a chance that it may change to atrophic or erosive subtypes; therefore the resolution of this lesion in the current investigation can be regarded as a signicant result. In addition, considering the increased premalignant potential of erosive lesions compared with atrophic and reticular forms, transition of the former to the latter types may be an important outcome of the current investigation. It can be presumed that purslane may decrease the risk of malignant transformation in OLP lesions. It seems that purslane, similar to beta-carotene and other antioxidant nutrients, may also have an inhibitory effect on oncogenesis; however, further investigation is required. The importance of this anticarcinogenic property is especially recognized when compared with the carcinogenic effects of other treatment options for lichen planus such as tacrolimus (Niwa et al., 2003). Sun et al. (2002) found signicantly higher serum IL-6 levels in OLP patients compared with normal controls and showed a signicant reduction in this factor after treatment with levamisole alone or in conjunction with Chinese herbs. Serum levels of purslane have been shown to decrease IL-6 secreted by damaged adipose cells, leading to improved cell viability in vitro (Xiao et al., 2005). Therefore there is a possibility that this herbal medicine may exert an antiinammatory effect on OLP via lowering IL-6 levels. Other antiinammatory drugs have also been used for the management of
Phytother. Res. 24: 240244 (2010) DOI: 10.1002/ptr

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lichen planus; for example, sulfasalazine has been administered in patients with skin and/or mucosal lesions leading to partial or complete response of skin lesions and resolution of pruritus. However, this drug was not effective on mucosal lesions and approximately 40% of the patients showed side-effects resulting in abandonment of treatment in 25% (Bauz et al., 2005). Corticosteroids are the most common and effective medicaments used for the treatment of OLP. Candidiasis and tachyphylaxis are known to occur after using topical steroids and it has been suggested that meticulous and regular reexaminations should be performed in order to monitor adrenal suppression and other adverse effects, especially considering the chronic nature of this disease and when using superpotent agents. In addition, corticosteroids are usually instructed to be used several times a day and should remain in contact with the lesion for a long time without eating and drinking for at least one hour (Scully et al., 2000; Eisen et al., 2005). Therefore their application could be difcult for the patient. These features are in contrast to the lack of adverse effects and easy usage (single dose/day) of purslane employed in the present study. For recalcitrant erosive OLP lesions, intralesional injections or the administration of systemic corticosteroids have been proposed. Repeated steroid injections are painful, can be absorbed systemically or may not be capable of completely resolving the lesions (Scully et al., 2000; Eisen et al., 2005). Systemic corticosteroids such as prednisone may be toxic or cause a long list of adverse effects in the patient (Fardet et al., 2007). Other forms of therapy include the prescription of immunomodulatory agents, retinoids, antimicrobials or a number of modalities such as ultraviolet radiation, surgery, magnetism, etc. (Scully et al., 2000). Tacrolimus is a steroid-free topical immunosuppressive drug that has been reported to be effective for intractable erosive OLP. However, some patients experience burning following application and recurrences after cessation of treatment (Eisen et al., 2005). In addition, animal studies have shown an increased risk of skin carcinogenesis in mice (Niwa et al., 2003) and its use in humans has been recommended to be: in minimal doses, for a limited amount of time and only as labeled for atopic dermatitis (Eisen et al., 2005). Retinoids are vitamin A metabolites with antioxidant, antikeratinizing and antiinammatory properties (Nagao et al., 2001; Buajeeb et al., 1997; Pawson et al., 1982). They have been used both topically and systemically for the treatment of OLP; however, some types

have been reported to be ineffective. Additionally, several adverse effects including a burning sensation and irritation in topical forms; and cheilitis, conjunctivitis, dry skin, xerostomia, headache, generalized itching and hair loss in systemic forms have occurred in the patient, leading to discontinuation of treatment (Scully et al., 2000; Eisen et al., 2005). Purslane contains a considerable amount of melatonin which is known to function directly as a free radical scavenger and indirectly as an antioxidant agent, through stimulating antioxidant enzymes. Melatonin can also synergistically affect the other antioxidants that were previously found in purslane. Furthermore this herbal medicine is a rich source of omega-3 fatty acids with antiinammatory and anticancer effects. Omega-3 fatty acids and melatonin both use similar mechanisms to prevent the progression of malignancies (Movahedian et al., 2007; Simopoulos et al., 2005). Antimicrobial (Lim and Quah, 2007), along with antifungal, effects have also been reported in different extracts of purslane (Movahedian et al., 2007). All of the above mentioned features have been used in other treatment methods for OLP; for example, retinoids as an antioxidant (Scully et al., 1998, 2000; Nagao et al., 2001; Baudet-Pommel et al., 1991), sulfasalazine as an antiinammatory drug (Bauz et al., 2005) and penicillin as an antimicrobial (Scully et al., 2000). However, as previously stated, none of them could completely eliminate the lesions and most of them demonstrated side effects. In conclusion, considering that purslane has numerous properties that are benecial in the management of OLP, it may be considered as an alternative or supplementary medicine for patients with this disease. In addition, since no adverse effects were found during the entire study period, it seems that antioxidant-rich purslane, given as a daily single-dose of 235 mg capsules, may be less harmful to the patients compared with other drugs with similar effects. Nevertheless, further investigation with a larger sample size and prolonged follow-up period is proposed in order to conrm the efcacy of purslane in the treatment of OLP lesions.

Acknowledgements
The present study was supported by a grant (no. NCT00746772) from Qazvin University of Medical Sciences. We wish to thank Tehran and Qazvin Universities of Medical Sciences and also Dr Reza Hajiaghhaee for his skillful technical assistance.

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Phytother. Res. 24: 240244 (2010) DOI: 10.1002/ptr