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1 ORIGINAL ARTICLE PHASE II STUDY OF GEFITINIB FOR THE TREATMENT OF RECURRENT AND METASTATIC NASOPHARYNGEAL CARCINOMA Daniel T. T. Chua, MD, 1 William I. Wei, MD, 2 Maria P. Wong, MD, 3 Jonathan S. T. Sham, MD, 1 John Nicholls, MD, 3 Gordon K. H. Au, FRCR 1 1 Department of Clinical Oncology, Queen Mary Hospital, The University of Hong Kong, Pokfulam, Hong Kong SAR, China. dttchua@hkucc.hku.hk 2 Department of Surgery, Queen Mary Hospital, The University of Hong Kong, Pokfulam, Hong Kong SAR, China 3 Department of Pathology, Queen Mary Hospital, The University of Hong Kong, Pokfulam, Hong Kong SAR, China Accepted 24 October 2007 Published online 22 January 2008 in Wiley InterScience ( DOI: /hed Abstract: Background. This single-center, phase II study assessed the safety/tolerability and initial efficacy of gefitinib in patients with nasopharyngeal carcinoma (NPC) pretreated with platinum-based chemotherapy. Methods. Patients with recurrent and metastatic NPC who had treatment failure with at least 2 lines of chemotherapy including platinum were given gefitinib at a fixed dose of 250 mg daily. Treatment was continued until the patient experienced unacceptable side effects or disease progression. Results. Nineteen patients were enrolled, having had treatment failure with a median of 2 chemotherapy regimens. Treatment was well tolerated, and only grades 1 to 2 adverse events were observed. None of the patients achieved partial or complete response. Median time-to-progression was 4 months, and median overall survival was 16 months. Conclusion. Gefitinib was well tolerated, but the response rate was poor in this heavily pretreated study population, and its use in NPC is not recommended outside the context of clinical trial. VC 2008 Wiley Periodicals, Inc. Head Neck 30: , 2008 Keywords: nasopharyngeal carcinoma; gefitinib; epidermal growth factor receptor; recurrence; distant metastases Correspondence to: D. T. T. Chua VC 2008 Wiley Periodicals, Inc. Nasopharyngeal carcinoma (NPC) is highly responsive to chemotherapy, and effective palliation of symptoms and prolongation of survival can often be achieved after chemotherapy for recurrent and metastatic disease, with occasional observation of long-term survivors after treatment. 1,2 Platinum-based chemotherapy regimens are among the most effective regimens for NPC and they are often used as first line chemotherapy for recurrent or metastatic disease. For those with disease recurrence or progression after platinumbased chemotherapy, the use of chemotherapeutic agents such as taxane, gemcitabine, and capecitabine have been reported to achieve a response rate of 29% to 56% in platinum-pretreated patients. 3 5 In heavily pretreated patients who are already exposed to multiple lines of chemotherapy, response to conventional chemotherapy regimens is generally poor with toxicity becoming a major issue. Similar to squamous cell carcinoma of the head and neck, a high percentage of NPC Gefitinib in Nasopharyngeal Cancer HEAD & NECK DOI /hed July

2 also expressed epidermal growth factor receptor (EGFR), 6 8 and strong expression of EGFR was found to correlate with poor survival. 9,10 Gefitinib is an oral aniline-quinazoline that reversibly inhibits EGFR tyrosine kinase activity. In a phase II trial using gefitinib in patients with recurrent and metastatic head and neck squamous cell carcinomas, the objective response rate and disease control rate were 10.4% and 53%, respectively, indicating that gefitinib has single-agent activity in head and neck squamous cell carcinoma. 11 In view of these findings, the use of new therapy targeting the EGFR pathway may also have therapeutic effect in NPC. This single-center, openlabel, phase II study was conducted to assess the safety/tolerability and efficacy of gefitinib in patients with recurrent and metastatic NPC pretreated with platinum-based chemotherapy. PATIENTS AND METHODS This phase II, single-center, open-label study enrolled patients with recurrent and/or metastatic NPC that were not amenable to surgery or reirradiation. Patients must have had histologically proven NPC of undifferentiated or poorly differentiated type, recurrent or metastatic disease documented by biopsy and/or imaging, and disease relapse or progression after 2 or more lines of chemotherapy including at least 1 platinumbased regimen. Additional eligibility criteria included presence of measurable disease, age 18 years or above, Eastern Cooperative Oncology Group (ECOG) performance score 2, adequate hematological reserve (white cell count / L and platelet count /L), and completion of other forms of therapy including chemotherapy at least 4 weeks before entering study. The study protocol was approved by the hospital institutional review board, and written informed consent was required prior to enrollment. Treatment Protocol. Eligible patients were treated with gefitinib at a continuous daily dose of 250 mg. Treatment was continued until disease progression, unacceptable side effect, or patient refusal. Patients were assessed every 4 weeks during treatment for compliance and adverse events. Adverse effects were graded according to National Cancer Institute Common Toxicity Criteria version 2.0. No dose reduction was allowed in the protocol. Temporary discontinuation of treatment was allowed in the event of grade 3 or above adverse events, and treatment was restarted upon resolution of adverse events to grade 1 or 0. Patients with treatment discontinued for more than 2 weeks were removed from the study. Response Assessment and Follow-Up. Patients were assessed for response by physical examination every 4 weeks and imaging every 8 weeks during treatment. Response criteria were defined based on Response Evaluation Criteria in Solid Tumors. Patients without disease progression at the time of treatment discontinuation were followed up in the same way during treatment. After documentation of disease progression, patients were followed up every 12 weeks for additional anticancer treatment and survival status. Statistical Analysis. The Simon s 2-stage optimal design was used in this trial to determine the sample size with a planned enrollment of 19 patients to the first stage and additional 31 patients to the second stage. The trial was designed to differentiate a response rate of 10% and 24% with a50.05 and b If there were 3 or more responses observed at the end of the first stage, the study was allowed to enter the second stage, and a total of 9 or more responses were considered a success indicating the study regimen was active and warranted further study. If there were 2 or fewer responses observed in the first stage or 8 or fewer responses in total, then the study drug was considered to have limited activity in NPC. The primary endpoint was response rate and the secondary endpoints were time-to-progression, symptomatic improvement, toxicity, and survival. Analysis was based on intent-to-treat, and all patients were included. Actuarial overall survival and progression-free survival probabilities were estimated by the Kaplan Meier method. Time to progression was calculated from the first day of study treatment until the date of progression or last follow-up in patients without disease progression. Likewise, survival time was calculated from the first day of study treatment until the date of death or last follow-up. RESULTS Patient Characteristics. Between May 2004 and June 2006, 19 patients were enrolled into the trial. There were 15 men and 4 women, with a median age of 51 years (range, years). Sites of disease were locoregional in 5, distant metastases in 11, and locoregional plus distant metastases in 864 Gefitinib in Nasopharyngeal Cancer HEAD & NECK DOI /hed July 2008

3 Table 1. Characteristics of patients with recurrent and metastatic nasopharyngeal carcinoma treated by gefitinib. No. of patients (%) Characteristic (n 5 19) Sex Male 15 (79) Female 4 (21) Age 45 8 (42) >45 11 (58) Median, y 51 Range, y Relapse sites Locoregional 5 (26) Distant 11 (58) Locoregional 1 distant 3 (16) ECOG performance status 0 8 (42) 1 7 (37) 2 4 (21) No. of relapse First relapse 15 (79) Second relapse 3 (16) Third relapse 1 (5) No. of chemotherapy regimens received 2 regimens 16 (84) 3 regimens 3 (16) Previous treatment for relapse Chemotherapy 19 (100) Reirradiation 4 (21) Surgery 2 (11) 3. Fifteen patients were treated for first relapse and 4 for repeated relapse. All patients had prior radical radiotherapy for NPC, and all had previously received platinum-based chemotherapy in the adjuvant and/or palliative setting. The median lines of patients who received chemotherapy prior to study enrollment was 2. Table 1 summarizes the patient characteristics. FIGURE 1. Progression-free survival curve in patients with recurrent and metastatic nasopharyngeal carcinoma treated with gefitinib. Adverse Events. Treatment was generally well tolerated with no grade 3 or 4 adverse events. Only grades 1 to 2 adverse events were observed, with acneiform rash (68.5%), fatigue (36.9%), diarrhea (31.6%), and anorexia (31.6%) most common. Dose interruption was required in 3 patients because of unbearable grade 2 skin rash, but all 3 patients were able to resume treatment after resolution of toxicity. Mild elevation of liver transaminase was observed in 4 patients (21.1%), but no dose interruption was needed. There were no treatment-related deaths. Response and Survival. There were no complete or partial responses observed in this trial. Two patients with local recurrence had mild shrinkage of tumor not meeting the criteria for partial response. Median time-to-progression was 4 months (95% confidence interval: 2.6 and 5.4 months), and median overall survival was 16 months (95% confidence interval: 11.8 and 20.2 months). The 6-month progression-free survival rate was 22% (Figure 1) and 12-month overall survival rate was 71.5% (Figure 2). Of the 15 Treatment. All enrolled patients received gefitinib for a median duration of 10 weeks (range, 4 50 weeks). Compliance was good, and all except 1 received a minimum of 8 weeks of treatment. Reasons for discontinuing treatment included disease progression in 12 (63.2%) and patient decision in 7 (36.8%). Nine patients received additional chemotherapy after discontinuation of gefitinib. Median follow-up time was 11 months (range, 7 23 months). FIGURE 2. Overall survival curve in patients with recurrent and metastatic nasopharyngeal carcinoma treated with gefitinib. Gefitinib in Nasopharyngeal Cancer HEAD & NECK DOI /hed July

4 patients with symptomatic disease, 5 (33%) reported improvement after treatment. Of the 5 patients with subjective improvement in symptoms after treatment, 4 were treated for locoregional recurrence and 1 for distant metastases. DISCUSSION EGFR is frequently expressed in head and neck squamous cell carcinoma, and overexpression of EGFR is associated with poor survival. 12,13 Although NPC has a different etiology and clinical course compared with head and neck squamous cell carcinoma, expression of EGFR is also commonly reported in NPC with positive staining rate ranging from 73% to 89% In a previous study reported by us, strong expression of EGFR (25%) was an independent prognostic factor for tumor control and survival in stages III IV NPC treated by induction chemotherapy and radiotherapy. 10 In another study by Ma et al 9 that examined the prognostic value of several biomarkers including EGFR, human epidermal growth factor receptor type 2 (HER2), p53, Ki-67, and microvessel density in NPC, only EGFR expression was found to be associated with survival. These findings suggest that EGFR expression is also an important prognostic factor in NPC, and treatment targeting the EGFR pathway may offer therapeutic benefit. In head and neck squamous cell carcinoma, preliminary experience suggests that gefitinib has single-agent activity in recurrent and metastatic disease. In a multicenter, phase II study conducted by Cohen et al, patients with recurrent and metastatic head and neck squamous cell carcinoma received gefitinib at a continuous daily dose of 500 mg after failing a median of 2 lines of chemotherapy. Of the 47 patients with assessable disease, 5 (10.6%) achieved partial response. The median time-to-progression was 3.4 months and median survival was 8.1 months. In another study using a similar protocol but with a reduced daily dose of 250 mg of gefitinib, only 1 (1.4%) partial response was observed in 70 study subjects, and the median progression-free survival was 1.8 months and median survival was 5.5 months. 14 These 2 studies suggest that a dose response relationship may exist for gefitinib in head and neck squamous cell carcinoma because little activity was seen when a lower dose of gefitinib was used. The current recommended dose of gefitinib for non-small cell lung cancer is 250 mg based on results from randomized trials that failed to show any differences in response rate and survival with 250 or 500 mg of gefitinib, but adverse events were more common with the higher dose. 15,16 In the present trial, a dose of 250 mg was chosen largely based on the experience of gefitinib in lung cancer. Although the lack of objective responses observed in our trial may be related to the gefitinib dose that we used, it is uncertain whether a similar dose response relationship observed in squamous cell carcinoma of head and neck will also apply in the treatment of NPC. In fact, the activity of higher gefitinib dose in NPC was being investigated by another group of researchers concurrently with our trial, and a preliminary report of that study showed no objective response in 11 patients with evaluable disease after treatment. 17 It is still uncertain whether a dose response relationship exists for gefitinib in NPC, and more studies are needed to address this issue. In this study, some patients were treated for locoregional recurrence only without evidence of distant metastases. Patients with locoregionally recurrent NPC has a different prognosis and response to treatment compared with metastatic NPC. In general, the former group has a slower disease progression rate and longer survival compared with the latter group, despite chemotherapy response is usually better in the latter group. Two recently published papers described the outcome of patients with NPC with isolated local failures or distant metastases and both were based on the outcome of the same cohort of 2915 patients with newly diagnosed NPC who were treated in Hong Kong from 1996 to In the study by Yu et al, patients developed isolated local failures on follow-up, and the 3-year overall survival rate was 74%. Patients who received salvage treatment for local recurrence had a 3-year survival rate of 80% compared with 56% in those without treatment. In the study by Hui et al, patients developed distant metastases alone on follow-up, and the 3-year overall survival rate was 37%. In our study, minor shrinkage of tumor was observed in 2 patients treated for locoregional disease and symptomatic improvement was also observed mainly in this group. Given the distinct clinical course and possibly therapeutic response in patients with locoregional recurrence, further study exploring the role of gefitinib in this subgroup may be warranted. In conclusion, gefitinib was well tolerated in patients with recurrent and metastatic NPC pretreated with platinum-based chemotherapy, but 866 Gefitinib in Nasopharyngeal Cancer HEAD & NECK DOI /hed July 2008

5 the response rate was poor in this heavily pretreated study population. Based on the results of the present trial, the use of gefitinib in recurrent and metastatic NPC is not recommended outside the context of clinical trial. Acknowledgments. The study drug gefitinib used in this trial was provided by Astra Zeneca Pharmaceuticals. REFERENCES 1. Teo PML, Kwan WH, Lee WY, et al. Prognosticators determining survival subsequent to distant metastases from nasopharyngeal carcinoma. Cancer 1996;77: Fandi A, Bachouchi M, Azli N, et al. Long-term diseasefree survivors in metastatic undifferentiated carcinoma of the nasopharyngeal type. J Clin Oncol 2000;18: Yeo W, Leung TW, Chan AT, et al. A phase II study combination of paclitaxel and carboplatin in advanced nasopharyngeal carcinoma. Eur J Cancer 1998;34: Chua DT, Kwong DL, Sham JS, et al. A phase II study of ifosfamide, 5-fluorouracil and leucovorin in patients with recurrent nasopharyngeal carcinoma previously treated with platinum chemotherapy. Eur J Cancer 2000;36: Ngan RK, Yiu HH, Lau WH, et al. Combination gemcitabine and cisplatin chemotherapy for metastatic or recurrent nasopharyngeal carcinoma: report of a phase II study. Ann Oncol 2002;13: Fujii M, Yamashita T, Ishiguro R, Tashiro M, Kameyama K. Significance of epidermal growth factor receptor and tumor associated tissue eosinophilia in the prognosis of patients with nasopharyngeal carcinoma. Auris Nasus Larynx 2002;29: Sheen TS, Huang YT, Chang YL, et al. Epstein-Barr virus-encoded latent membrane protein 1 co-expresses with epidermal growth factor receptor in nasopharyngeal carcinoma. Jpn J Cancer Res 1999;90: Putti TC, To KF, Hsu HC, et al. Expression of epidermal growth factor receptor in head and neck cancers correlates with clinical progression: a multicentre immunohistochemical study in the Asia-Pacific region. Histopathology 2002;41: Ma BB, Poon TC, To KF, et al. Prognostic significance of tumor angiogenesis, KI-67, P53 oncoprotein, epidermal growth factor receptor and HER2 receptor protein expression in undifferentiated nasopharyngeal carcinoma: a prospective study. Head Neck 2003;25: Chua DT, Nicholls JM, Sham JS, Au GK. Prognostic value of epidermal growth factor receptor expression in patients with advanced stage nasopharyngeal carcinoma treated with induction chemotherapy and radiotherapy. Int J Radiat Oncol Biol Phys 2004;59: Cohen EE, Rosen F, Stadler WM, et al. Phase II trial of ZD1839 in recurrent or metastatic squamous cell carcinoma of the head and neck. J Clin Oncol 2003;21: Grandis JR, Melhem MF, Barnes EL, Tweardy DJ. Quantitative immunohistochemistry analysis of transforming growth factor-a and epidermal growth factor receptor in patients with squamous cell carcinoma of the head and neck. Cancer 1996;78: Ang KK, Berkey BA, Tu X, et al. Impact of epidermal growth factor receptor expression on survival and pattern of relapse in patients with advanced head and neck carcinoma. Cancer Res 2002;62: Cohen EE, Kane MA, List MA, et al. Phase II trial of gefitinib 250mg daily in patient with recurrent and/or metastatic squamous cell carcinoma of the head and neck. Clin Cancer Res 2005;21: Kris MG, Natale RB, Herbst RS, et al. Efficacy of gefitinib, an inhibitor of the epidermal growth factor receptor tyrosine kinase, in symptomatic patients with non-small cell lung cancer: a randomized trial. JAMA 2003;290: Fukuoka M, Yano S, Giaccone G, et al. Multi-institutional randomized phase II trial of gefitinib for previously treated patients with advanced non-small-cell lung cancer (The IDEAL 1 Trial). J Clin Oncol 2003;21: Chan AT, Ma B, Hui EP, et al. Phase II study of gefitinib in metastatic or locoregionally recurrent nasopharyngeal carcinoma (NPC) [abstract 15509]. J Clin Oncol 2006; Yu KH, Leung SF, Tung SY, et al. Survival outcome of patients with nasopharyngeal carcinoma with first local failure: a study by the Hong Kong nasopharyngeal carcinoma study group. Head Neck 2005;27: Hui EP, Leung SF, Au JS, et al. Lung metastasis alone in nasopharyngeal carcinoma: a relatively favourable prognostic factor. Cancer 2004;101: Gefitinib in Nasopharyngeal Cancer HEAD & NECK DOI /hed July

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