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Dominant Papillary Subtype Is a Significant Predictor of the Response to Gefitinib in Adenocarcinoma of the Lung

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Dominant Papillary Subtype Is a Significant Predictor of the Response to Gefitinib in Adenocarcinoma of the Lung Vol. 10, 7311–7317, November 1, 2004 Clinical Cancer Research 7311 Dominant Papillary Subtype Is a Significant Predictor of the Response to Gefitinib in Adenocarcinoma of the Lung Young Hak Kim,1,2 Genichiro Ishii,1 EGFR, phosphorylated EGFR, or c-erbB-2 were associated Koichi Goto,2 Kanji Nagai,2 Koji Tsuta,1 with the response to gefitinib. Satoshi Shiono,1,2 Junichi Nitadori,1,2 Conclusions: The results of the present study indicate 3 2 that dominant papillary subtype findings of lung adenocar- Testuro Kodama, Yutaka Nishiwaki, and cinomas can be an important predictor of the response to 1 Atsushi Ochiai gefitinib. Thus, this type of adenocarcinoma might be sus- 1Pathology Division, National Cancer Center Research Institute East, ceptible to postoperative adjuvant treatment with gefitinib. Chiba, Japan; 2Division of Thoracic Oncology, National Cancer Center Hospital East, Chiba, Japan; 3Internal Medicine and Thoracic Oncology Division, National Cancer Center Hospital, Tokyo, Japan INTRODUCTION Lung cancer is the leading cause of cancer deaths in many ABSTRACT countries, and the global incidence is rising at a rate of 0.5% per Purpose: Gefitinib (IRESSA; AstraZeneca, Osaka, Ja- annum (1, 2). Platinum-based combination chemotherapy has been pan) shows excellent antitumor activity against advanced shown to improve survival and quality-of-life in patients with non–small-cell lung cancer, especially for the treatment of advanced non–small-cell lung cancer (NSCLC; ref 3 and 4), which adenocarcinoma. However, the predictive factors for the accounts for approximately 80% of all lung cancers. New chemo- response to gefitinib are still controversial. The aim of this therapeutic agents, like gemcitabine, vinorelbine, docetaxel, pacli- study was to identify the clinicopathological and immuno- taxel, and irinotecan, were developed in the 1990s. However, histochemical features that are favorable to the use of ge- chemotherapy for advanced NSCLC has been of limited benefit, fitinib in adenocarcinoma patients. with response rates of approximately 30% and a median survival Experimental Design: Between June 2002 and October period of about 8 months, and it seems to have reached a plateau (1, 2003, 36 adenocarcinoma patients who experienced a relapse 5, 6). It is clear that additional treatment strategies are necessary. after surgical resection were treated with gefitinib at our Epidermal growth factor receptor (EGFR) has been shown hospital. The histologic patterns of the tumors were divided to play an important role in the growth of many solid tumors and into four distinctive subtypes according to the revised World is overexpressed in approximately 40 to 80% of NSCLCs (7–9). Health Organization histologic classification, and the dom- Furthermore, the overexpression of EGFR has been associated inant histologic subtype for the maximum cut surface of with a poor prognosis in several studies on lung cancer (10, 11). each resected specimen was documented. Association be- EGFR activation occurs when ligands, such as epidermal growth tween the response to gefitinib and the clinicopathological factor, transforming growth factor-␣, or amphiregulin, bind to features or immunohistochemical expression of epidermal its extracellular domain, resulting in cell proliferation, angiogene- growth factor receptor (EGFR), phosphorylated EGFR, or sis, metastasis, and antiapoptosis (8, 9). Gefitinib (IRESSA; Astra- c-erbB-2 were then investigated. Zeneca, Osaka, Japan) is an orally active, selective EGFR tyrosine Results: A significant association between the response kinase inhibitor that blocks downstream of the EGFR signal trans- to gefitinib and dominant papillary subtype findings was duction pathway (12). In this context, gefitinib has a quite different .the survival time of papillary sub- profile from chemotherapeutic agents that have ever been used ;(0.0021 ؍ observed (P type patients was also significantly prolonged compared After phase I studies, two multicenter, randomized, double- No blind phase II studies (IDEAL1, ref. 13; IDEAL2, ref. 14) were .(0.03 ؍ with that of non-papillary subtype patients (P other clinicopathological features or the expression of carried out to evaluate the tolerability and efficacy of gefitinib in patients with advanced NSCLC who had been treated previously with platinum-based combination chemotherapy. In total, 426 patients were enrolled in the two studies, and all of the patients Received 4/26/04; revised 7/12/04; accepted 7/19/04. had been treated previously with platinum-based combination Grant support: in part by a Grant-in-Aid for Cancer Research from the chemotherapy. In both studies, the administration of two differ- Japanese Ministry of Health and Welfare and by a Grant-in-Aid for the ent gefitinib dosages (250 mg/day and 500 mg/day) were com- Second Term Comprehensive 10-Year Strategy for Cancer Control that pared. No significant differences in efficacy were seen between was also from the Ministry of Health and Welfare. the two dosages, but the 250 mg/day treatment was better The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked tolerated than the 500 mg/day treatment in both studies. For the advertisement in accordance with 18 U.S.C. Section 1734 solely to 250 mg/day gefitinib arms, the response rates were 18.4% and indicate this fact. 12.0% in IDEAL1 and IDEAL2, respectively. Requests for reprints: Atsushi Ochiai, Pathology Division, National The results of IDEAL1 showed that gefitinib was signifi- Cancer Center Research Institute East, 6-5-1 Kashiwanoha, Kashiwa, Chiba 277-8577, Japan, Phone: 81-4-7133-1111; Fax: 81-4-7131-4724; cantly more effective for the treatment of adenocarcinomas than E-mail: [email protected]. for other histologies (odds ratio, 3.45) and was also more ©2004 American Association for Cancer Research. effective in females than in males (odds ratio, 2.65). These Downloaded from clincancerres.aacrjournals.org on September 28, 2021. © 2004 American Association for Cancer Research. 7312 Histological Subtype May Predict Gefitinib Response findings were unexpected, given the mechanism of the drug, specimens, and no studies examining surgical specimens have because squamous cell carcinomas are known to overexpress been done. Lung cancer is generally characterized by histologic EGFR, the target of gefitinib, to a greater degree than adeno- heterogeneity; thus, studies examining histologic features carcinomas. On the other hand, gefitinib-induced severe acute should be done using surgically resected specimens. interstitial pneumonia resulting in a high mortality rate is a In this study, we investigated the clinicopathological and serious social problem in Japan (15). Although the precise immunohistochemical features of surgically resected adenocar- mechanism of gefitinib’s action is not yet completely under- cinoma specimens from patients who were subsequently treated stood, clinically it is more important to identify favorable char- with gefitinib after relapse to identify any characteristics that acteristics in the treatment with gefitinib. were associated with a favorable response to gefitinib. Gefitinib has been confirmed to be significantly effective for the treatment of adenocarcinomas, and some investigators have reported that gefitinib is especially effective in adenocar- PATIENTS AND METHODS cinomas with bronchiolo-alveolar features (16, 17). To the best Patients. Between June 2002 and October 2003, 253 of our knowledge, however, these studies only examined biopsy consecutive patients were treated with a 250 mg daily dosage of Table 1 Patient characteristics (N ϭ 36) Recurrent site Previous treatment Patient Age Gender Current no. (year) (M/F) PS Smoking Lung Others CT regimen (response) Response status 172F1ϪϩϩCT, RT CDDP/VNR (PR) PR Continued 257M1ϩϩϩCT, bone RT CDDP/VNR (SD) PR Continued 362M1ϩϩϩCT, bone RT CDDP/VNR (PR) PR Ceased 460M1ϩϩϪCT CDDP/VNR (SD) PR Ceased 561F1ϪϩϪCT ①CBDCA/PTX (CR) PR Continued ②GEM/VNR (SD) 664M2Ϫϩϩbrain RT PR Dead 766M1ϩϩϩCT CDDP/VNR (SD) PR Continued 869F1ϪϩϪCT, OP CDDP/VNR (PD) PR Continued 955F0ϪϩϪNone PR Continued 10 66 F 1 ϪϩϪCT ①GEM/VNR (SD) PR Continued ②CBDCA (SD) 11 61 F 0 ϪϩϪCT CDDP/VNR (SD) PR Ceased 12 69 M 0 ϩϩϪNone PR Continued 13 62 F 1 ϪϩϩCT, OP, brain RT CDDP/VNR (PR) PR Continued 14 67 M 0 ϩϩϪNone PR Continued 15 47 F 1 ϪϩϪCT CDDP/VNR (SD) PR Ceased 16 43 F 1 ϪϩϪNone PR Continued 17 73 F 1 ϪϪϩNone PR Continued 18 45 F 1 ϪϩϪCT CDDP/VNR (SD) SD Dead 19 45 F 0 ϪϩϪNone SD Ceased 20 59 M 0 ϩϩϪCT CDDP/VNR (SD) SD Continued 21 66 F 2 ϪϩϪCT, RT, OP CDDP/VDSϩMMC (SD) SD Ceased 22 62 F 0 ϩϩ- CT GEM/VNR (SD) SD Ceased 23 60 M 1 ϩϩϩCT, RT ①CDDP/GEM/VNR (SD) SD Ceased ②DTX (PD) 24 55 M 1 ϪϩϪCT CBDCA/PTX (SD) SD Ceased 25 71 F 2 ϪϪϩbone RT SD Dead 26 82 F 1 ϪϩϪOP SD Ceased 27 72 M 1 ϩϩϪOP SD Unknown 28 67 F 1 ϩϩϪNone SD Dead 29 71 M 1 ϩϩϪNone SD Continued 30 57 M 1 ϩϩϪNone SD Ceased 31 74 M 1 ϩϩϪNone SD Dead 32 65 M 2 ϩϪϩCT, brain RT CDDP/VNR (SD) SD Continued 33 73 F 1 ϪϩϪNone SD Continued 34 72 F 1 ϪϩϩRT PD Dead 35 67 M 1 ϩϩϩCT CDDP/VNR (SD) PD Dead 36 60 M 1 ϪϩϪOP PD Unknown N ϭ 36 70 (43–82) M/F: 0–1/2: Ϫ/ϩ: 33 12 Previous CT Number of regimen OR: 47% 17/19 32/4 20/16 (ϩ): 19 1 regimen: 16 2 regimen: 3 Abbreviations: F, female; M, male; PS, performance status (ECOG, Eastern Cooperative Oncology Group); CT, chemotherapy; RT, radiation therapy; OP, operation; CDDP, cisplatin; CBDCA, carboplatin; VNR, vinorelbine; PTX, paclitaxel; GEM, gemcitabine; VDS, vindesine, MMC, mitomycine C; DTX, docetaxel; PR, partial response; SD, stable disease; PD, progressive disease; OR, overall response. Downloaded from clincancerres.aacrjournals.org on September 28, 2021. © 2004 American Association for Cancer Research. Clinical Cancer Research 7313 gefitinib at our hospital.
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