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The Efficacy of Imiquimod on Dysplastic Lesions of the Oral Mucosa: an Experimental Model

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The Efficacy of Imiquimod on Dysplastic Lesions of the Oral Mucosa: an Experimental Model ANTICANCER RESEARCH 30: 2891-2896 (2010) The Efficacy of Imiquimod on Dysplastic Lesions of the Oral Mucosa: An Experimental Model VASILIKI GKOULIONI1, ANNA ELEFTHERIADOU2, IOANNIS YIOTAKIS3, ELIZA FEREKIDOU3, ARISTIDIS CHRISOVERGIS3, ANDREAS CH. LAZARIS4 and DIMITRIOS KANDILOROS3 1Center of Experimental Surgery, Foundation of Biomedical Research, Academy of Athens, Athens, Greece 2Department of Otolaryngology, General Hospital of Rethymnon, Crete, Greece; 3Department of Otolaryngology, Hippokration Hospital, University of Athens, Athens, Greece; 4Department of Pathology, University of Athens, Greece Abstract. Aim: To study the potent efficacy of the The most common precancerous lesion of the oral mucosa immunomodulatory agent imiquimod when applied on is leukoplakia, which in fact is a clinical term only. “Oral dysplastic lesions of the oral mucosa. Materials and leukoplakia is a predominant white lesion of the oral mucosa Methods: Carcinogen (DMBA) was applied to the mucosa of that cannot be characterized as any other definable lesion. the left buccal pouch of 26 male Wistar rats for 8 weeks, Some oral leukoplakias will transform into cancer” (1). until dysplastic lesions were observed and histologically Histological examination of leukoplakia is always necessary, diagnosed. At the second phase of the experiment, 5% in order to determine the exact grade of histological lesion, if imiquimod cream was applied to these dysplastic lesions for present. Hence a white lesion of the oral mucosa can either 16 weeks. Biopsies were taken before and after treatment. be dysplastic or non-dysplastic. This is why the term Results: The histological effect of imiquimod was the leukoplakia remains strictly a clinical term only, and after a regression of mild dysplasia to hyperplasia for all the biopsy is performed, the term leukoplakia is replaced by the samples. In one case, a well-differentiated squamous cell diagnosis obtained histologically (2). carcinoma was converted to a papilloma-like squamous The management of oral dysplasia consists first of all of the neoplasm with a benign morphology. Conclusion: Our elimination of the causative factor, which is usually the use of results indicate that imiquimod may be effective in treatment tobacco. According to most published studies, elimination of of precancerous lesions of the oral mucosa and thus inhibit the cause leads to regression of the lesion. However, when no the progress of carcinogenesis. possible cause can be found, or when the lesion does not disappear, it is necessary to proceed to other therapeutic Dysplasia is of critical importance in the field of cancer procedures: surgical excision, cryosurgery, CO2-laser ablation chemoprevention field, as any degree of dysplasia may and application of: vitamin E, vitamin A, retinoids, beta- progress to severe dysplasia or carcinoma in situ. In fact carotene, bleomycin, alpha-tocopherol, and calcipotriol (2). dysplasia is a precancerous lesion, that is: “a Imiquimod is a novel synthetic compound that belongs to morphologically alterated tissue in which cancer is more the class of 1H-imidazo-[4,5-c]quinolines, a nucleoside likely to occur than in its apparently normal counterpart” (1). analogue of the imidazoquinoline family known for its Hence, it always remains a challenge to discover new competence as immune response modifiers and stimulators therapeutic agents that can prevent the transformation of (3). Its main biological effect is the induction of endogenous precancerous lesions into cancer, or even cause their antiviral pro-inflammatory mediators. Besides its antiviral regression. As far as the oral cavity is concerned, it is widely activity, imiquimod has shown a very interesting efficacy accepted that dysplastic lesions are considered to be against several types of human malignancies, thus increasing precancerous lesions with a certain potential for developing the research about its exact mechanism of action and its a carcinoma in situ and more invasive forms of cancer. potential antitumoral applications The Food and Drug Administration of the USA approved imiquimod for the treatment of external anogenital and perianal warts in 1997. In 2004, imiquimod received FDA Correspondence to: Anna Eleftheriadou, MD, Ph.D., PO Box 269, approval for the treatment of actinic keratosis (AK) and 74100, Rethymnon, Crete, Greece. Mobile: +30 6974542018, e-mail: [email protected] superficial basal cell carcinoma (SBCC). Imiquimod acts on both the major divisions of the immune Key Words: Imiquimod, oral dysplasia, treatment. system: the innate and the cell-mediated system. 0250-7005/2010 $2.00+.40 2891 ANTICANCER RESEARCH 30: 2891-2896 (2010) Imiquimod exerts its predominant effect via its binding to imiquimod are topical pain, burning, itching, erythema, the toll-like receptors (TLR) 7 and 8. TLR-7 and TLR-8 erosions, edema and ulceration. These local side-effects belong to the family of ten currently known TLRs which are cause re-determination of the application dosage (7). crucially involved in the innate immune system’s recognition The aim of the present study was to evaluate any possible of various microbial antigens (4). TLR-7 and TLR-8 are regression of premalignant lesions after local administration present on dendritic cells, macrophages, and monocytes. of imiquimod. Their activation leads to the stimulation of the nuclear factor κB (NF-κB), which is a central transcription factor. NF-κB is Materials and Methods normally inactive because of its binding to inhibitory κB (IκB). After TLR-mediated stimulation, NF-κB is dissociated The animal that served as animal model in our experiment was the from IκB. This leads to the entrance of NF-κB into the Wistar rat. Thirty-six male Wistar rats that were 60 days old and nucleus, where it induces the transcription of a large number weighed about 350-400 g each at the beginning of the experimental of genes. Products of these genes include an important period were used. The animals were housed two per cage and were given standard laboratory food and water ad libitum. They were number of pro-inflammatory mediators (cytokines): tumor maintained in a controlled environment, under standard laboratory necrosis factor α (TNF-α), interferon α (IFN-α), interleukin- conditions of temperature and humidity. 1 (IL-1), (IL-6), (IL-8), (IL-10) and (IL-12). These cytokines The carcinogen used was 7,12-dimethylbenz[α]anthracene up-regulate cell-mediated Th-1 responses, which have (DMBA; Sigma Chemical Co, S. Louis MO, USA), an aromatic antitumoral and antiviral effects, while they down regulate polycyclic hydrocarbon. DMBA powder (1g) was dissolved in Th-2 responses (5). 200 ml acetone, in order to produce a solution of 0.5% DMBA, Independently from TLR-7 and TLR-8, imiquimod which was kept in a brown bottle in the refrigerator through the time of the experiment (8, 9). interacts with adenosine receptor (especially A2A) and down All the treatments on the animals were carried out under general regulates adenylyl cyclase. Both these effects result in anesthesia with isoflurane. Isoflurane was considered to be suitable suppression of a negative feedback mechanism which for this experiment because it achieves the depth and duration of normally limits inflammatory reactions. The final result is anesthesia necessary for our treatments, while it causes only slight again the increase of pro-inflammatory activity. Furthermore, side-effects. This was very important for our experiment, as it imiquimod induces 2’5’oligoadenylatesynthetase, thus assured the survival of the animals for the duration of long period stimulating natural killer (NK) cells and enhances the that lasted the experiment (24 weeks). After the inhalation of the anesthetic, the animal was held in a supine position and the mouth maturation of epidermal Langerhans cells and their migration was opened with a pair of forceps. The right buccal pouch served to regional lymph nodes, promoting a specific T-cell response. as a control and was not treated. The mucosal surface of the left The antitumoral activity of imiquimod is not only buccal pouch was cleared of food debris and dried with sterile attributed to its numerous stimulating effects on the immune gauze. Then it was painted with 0.5 ml of DMBA with the help of system, but also on the induction of apoptosis of tumour a hairbrush, in a circular motion 10 times. The application was cells. Activation of transcription-1 signaling pathway favors carried out 3 times per week for 8 weeks (10). The mouth was kept the secretion of pro-inflammatory cytokines, and takes part opened for about 2 minutes after each application, to ensure that DMBA was absorbed into the buccal pouch epithelium and not lost in the apoptosis of tumour cells. Moreover, topical or swallowed. Food and drink were not held from the animals for imiquimod increases the expression of the death receptor CD about 3 hours after each application. 95 (Fas) and its binding to the Fas-ligand (5), resulting in the At the end of 8 weeks, the lesions were photographed and biopsy apoptosis of tumour cells. In addition, imiquimod reduces specimens were taken from the left buccal pouch mucosa of all the the expression of the anti-apoptotic Bcl-2 protein. This animals. The piece of the tissue was taken under general anesthesia results in release of mitochondrial cytochrome c and with intraperitoneal injection of ketamine (200 mg/kg of body activation of caspase-9 and terminal caspases, mainly weight) and xylazine (10 mg/kg of body weight). The specimens were fixed
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