Skip to main content
Top
Published in: BMC Cancer 1/2014

Open Access 01-12-2014 | Research article

Epidermal growth factor receptor mutations and anaplastic lymphoma kinase rearrangements in lung cancer with nodular ground-glass opacity

Authors: Sung-Jun Ko, Yeon Joo Lee, Jong Sun Park, Young-Jae Cho, Ho Il Yoon, Jin-Haeng Chung, Tae Jung Kim, Kyung Won Lee, Kwhanmien Kim, Sanghoon Jheon, Hyojin Kim, Jae Ho Lee, Choon-Taek Lee

Published in: BMC Cancer | Issue 1/2014

Login to get access

Abstract

Background

Nodular ground-glass opacities (nGGO) are a specific type of lung adenocarcinoma. ALK rearrangements and driver mutations such as EGFR and K-ras are frequently found in all types of lung adenocarcinoma. EGFR mutations play a role in the early carcinogenesis of nGGOs, but the role of ALK rearrangement remains unknown.

Methods

We studied 217 nGGOs resected from 215 lung cancer patients. Pathology, tumor size, tumor disappearance rate, and the EGFR and ALK markers were analyzed.

Results

All but one of the resected nGGOs were adenocarcinomas. ALK rearrangements and EGFR mutations were found in 6 (2.8%) and 119 (54.8%) cases. The frequency of ALK rearrangement in nGGO was significantly lower than previously reported in adenocarcinoma. Advanced disease stage (p = 0.018) and larger tumor size (p = 0.037) were more frequent in the ALK rearrangement-positive group than in ALK rearrangement-negative patients. nGGOs with ALK rearrangements were associated with significantly higher pathologic stage and larger maximal and solid diameter in comparison to EGFR-mutated lesions.

Conclusion

ALK rearrangement is rare in lung cancer with nGGOs, but is associated with advanced stage and larger tumor size, suggesting its association with aggressive progression of lung adenocarcinoma. ALK rearrangement may not be important in early pathogenesis of nGGO.
Literature
1.
go back to reference Aberle DR, Adams AM, Berg CD, Black WC, Clapp JD, Fagerstrom RM, Gareen IF, Gatsonis C, Marcus PM, Sicks J: Reduced lung-cancer mortality with low-dose computed tomographic screening. N Engl J Med. 2011, 365 (5): 395-409.CrossRefPubMed Aberle DR, Adams AM, Berg CD, Black WC, Clapp JD, Fagerstrom RM, Gareen IF, Gatsonis C, Marcus PM, Sicks J: Reduced lung-cancer mortality with low-dose computed tomographic screening. N Engl J Med. 2011, 365 (5): 395-409.CrossRefPubMed
2.
go back to reference Godoy MC, Naidich DP: Subsolid Pulmonary Nodules and the Spectrum of Peripheral Adenocarcinomas of the Lung: Recommended Interim Guidelines for Assessment and Management. Radiology. 2009, 253 (3): 606-622. 10.1148/radiol.2533090179.CrossRefPubMed Godoy MC, Naidich DP: Subsolid Pulmonary Nodules and the Spectrum of Peripheral Adenocarcinomas of the Lung: Recommended Interim Guidelines for Assessment and Management. Radiology. 2009, 253 (3): 606-622. 10.1148/radiol.2533090179.CrossRefPubMed
3.
go back to reference Lee HY, Lee KS: Ground-glass opacity nodules: histopathology, imaging evaluation, and clinical implications. J Thorac Imaging. 2011, 26 (2): 106-118. 10.1097/RTI.0b013e3181fbaa64.CrossRefPubMed Lee HY, Lee KS: Ground-glass opacity nodules: histopathology, imaging evaluation, and clinical implications. J Thorac Imaging. 2011, 26 (2): 106-118. 10.1097/RTI.0b013e3181fbaa64.CrossRefPubMed
4.
go back to reference Travis WD, Brambilla E, Noguchi M, Nicholson AG, Geisinger KR, Yatabe Y, Beer DG, Powell CA, Riely GJ, Van Schil PE, Garg K, Austin JH, Asamura H, Rusch VW, Hirsch FR, Scagliotti G, Mitsudomi T, Huber RM, Ishikawa Y, Jett J, Sanchez-Cespedes M, Sculier JP, Takahashi T, Tsuboi M, Vansteenkiste J, Wistuba I, Yang PC, Aberle D, Brambilla C, Flieder D, et al: International Association for the Study of Lung Cancer/American Thoracic Society/European Respiratory Society international multidisciplinary classification of lung adenocarcinoma. J Thorac Oncol. 2011, 6 (2): 244-285. 10.1097/JTO.0b013e318206a221.CrossRefPubMedPubMedCentral Travis WD, Brambilla E, Noguchi M, Nicholson AG, Geisinger KR, Yatabe Y, Beer DG, Powell CA, Riely GJ, Van Schil PE, Garg K, Austin JH, Asamura H, Rusch VW, Hirsch FR, Scagliotti G, Mitsudomi T, Huber RM, Ishikawa Y, Jett J, Sanchez-Cespedes M, Sculier JP, Takahashi T, Tsuboi M, Vansteenkiste J, Wistuba I, Yang PC, Aberle D, Brambilla C, Flieder D, et al: International Association for the Study of Lung Cancer/American Thoracic Society/European Respiratory Society international multidisciplinary classification of lung adenocarcinoma. J Thorac Oncol. 2011, 6 (2): 244-285. 10.1097/JTO.0b013e318206a221.CrossRefPubMedPubMedCentral
5.
go back to reference Takeuchi T, Tomida S, Yatabe Y, Kosaka T, Osada H, Yanagisawa K, Mitsudomi T, Takahashi T: Expression profile-defined classification of lung adenocarcinoma shows close relationship with underlying major genetic changes and clinicopathologic behaviors. J Thorac Oncol. 2006, 24 (11): 1679-1688. Takeuchi T, Tomida S, Yatabe Y, Kosaka T, Osada H, Yanagisawa K, Mitsudomi T, Takahashi T: Expression profile-defined classification of lung adenocarcinoma shows close relationship with underlying major genetic changes and clinicopathologic behaviors. J Thorac Oncol. 2006, 24 (11): 1679-1688.
6.
go back to reference Maemondo M, Inoue A, Kobayashi K, Sugawara S, Oizumi S, Isobe H, Gemma A, Harada M, Yoshizawa H, Kinoshita I: Gefitinib or chemotherapy for non–small-cell lung cancer with mutated EGFR. N Engl J Med. 2010, 362 (25): 2380-2388. 10.1056/NEJMoa0909530.CrossRefPubMed Maemondo M, Inoue A, Kobayashi K, Sugawara S, Oizumi S, Isobe H, Gemma A, Harada M, Yoshizawa H, Kinoshita I: Gefitinib or chemotherapy for non–small-cell lung cancer with mutated EGFR. N Engl J Med. 2010, 362 (25): 2380-2388. 10.1056/NEJMoa0909530.CrossRefPubMed
7.
go back to reference Mitsudomi T, Morita S, Yatabe Y, Negoro S, Okamoto I, Tsurutani J, Seto T, Satouchi M, Tada H, Hirashima T: Gefitinib versus cisplatin plus docetaxel in patients with non-small-cell lung cancer harbouring mutations of the epidermal growth factor receptor (WJTOG3405): an open label, randomised phase 3 trial. Lancet Oncol. 2010, 11 (2): 121-128. 10.1016/S1470-2045(09)70364-X.CrossRefPubMed Mitsudomi T, Morita S, Yatabe Y, Negoro S, Okamoto I, Tsurutani J, Seto T, Satouchi M, Tada H, Hirashima T: Gefitinib versus cisplatin plus docetaxel in patients with non-small-cell lung cancer harbouring mutations of the epidermal growth factor receptor (WJTOG3405): an open label, randomised phase 3 trial. Lancet Oncol. 2010, 11 (2): 121-128. 10.1016/S1470-2045(09)70364-X.CrossRefPubMed
8.
go back to reference Zhou C, Wu YL, Chen G, Feng J, Liu XQ, Wang C, Zhang S, Wang J, Zhou S, Ren S, Lu S, Zhang L, Hu C, Luo Y, Chen L, Ye M, Huang J, Zhi X, Zhang Y, Xiu Q, Ma J, Zhang L, You C: Erlotinib versus chemotherapy as first-line treatment for patients with advanced EGFR mutation-positive non-small-cell lung cancer (OPTIMAL, CTONG-0802): a multicentre, open-label, randomised, phase 3 study. Lancet Oncol. 2011, 12 (8): 735-742. 10.1016/S1470-2045(11)70184-X.CrossRefPubMed Zhou C, Wu YL, Chen G, Feng J, Liu XQ, Wang C, Zhang S, Wang J, Zhou S, Ren S, Lu S, Zhang L, Hu C, Luo Y, Chen L, Ye M, Huang J, Zhi X, Zhang Y, Xiu Q, Ma J, Zhang L, You C: Erlotinib versus chemotherapy as first-line treatment for patients with advanced EGFR mutation-positive non-small-cell lung cancer (OPTIMAL, CTONG-0802): a multicentre, open-label, randomised, phase 3 study. Lancet Oncol. 2011, 12 (8): 735-742. 10.1016/S1470-2045(11)70184-X.CrossRefPubMed
9.
go back to reference Soda M, Choi YL, Enomoto M, Takada S, Yamashita Y, Ishikawa S, Fujiwara S-i, Watanabe H, Kurashina K, Hatanaka H: Identification of the transforming EML4–ALK fusion gene in non-small-cell lung cancer. Nature. 2007, 448 (7153): 561-566. 10.1038/nature05945.CrossRefPubMed Soda M, Choi YL, Enomoto M, Takada S, Yamashita Y, Ishikawa S, Fujiwara S-i, Watanabe H, Kurashina K, Hatanaka H: Identification of the transforming EML4–ALK fusion gene in non-small-cell lung cancer. Nature. 2007, 448 (7153): 561-566. 10.1038/nature05945.CrossRefPubMed
10.
go back to reference Kwak EL, Bang Y-J, Camidge DR, Shaw AT, Solomon B, Maki RG, Ou S-HI, Dezube BJ, Jänne PA, Costa DB: Anaplastic lymphoma kinase inhibition in non–small-cell lung cancer. N Engl J Med. 2010, 363 (18): 1693-1703. 10.1056/NEJMoa1006448.CrossRefPubMedPubMedCentral Kwak EL, Bang Y-J, Camidge DR, Shaw AT, Solomon B, Maki RG, Ou S-HI, Dezube BJ, Jänne PA, Costa DB: Anaplastic lymphoma kinase inhibition in non–small-cell lung cancer. N Engl J Med. 2010, 363 (18): 1693-1703. 10.1056/NEJMoa1006448.CrossRefPubMedPubMedCentral
11.
go back to reference Shaw AT, Kim D-W, Nakagawa K, Seto T, Crinó L, Ahn M-J, De Pas T, Besse B, Solomon BJ, Blackhall F: Crizotinib versus chemotherapy in advanced ALK-positive lung cancer. N Engl J Med. 2013, 368 (25): 2385-2394. 10.1056/NEJMoa1214886.CrossRefPubMed Shaw AT, Kim D-W, Nakagawa K, Seto T, Crinó L, Ahn M-J, De Pas T, Besse B, Solomon BJ, Blackhall F: Crizotinib versus chemotherapy in advanced ALK-positive lung cancer. N Engl J Med. 2013, 368 (25): 2385-2394. 10.1056/NEJMoa1214886.CrossRefPubMed
12.
go back to reference Ettinger DS, Akerley W, Borghaei H, Chang AC, Cheney RT, Chirieac LR, D’Amico TA, Demmy TL, Ganti AKP, Govindan R: Non–Small Cell Lung Cancer. J Natl Compr Cancer Netw. 2012, 10 (10): 1236-1271. Ettinger DS, Akerley W, Borghaei H, Chang AC, Cheney RT, Chirieac LR, D’Amico TA, Demmy TL, Ganti AKP, Govindan R: Non–Small Cell Lung Cancer. J Natl Compr Cancer Netw. 2012, 10 (10): 1236-1271.
13.
go back to reference Lindeman NI, Cagle PT, Beasley MB, Chitale DA, Dacic S, Giaccone G, Jenkins RB, Kwiatkowski DJ, Saldivar J-S, Squire J: Molecular testing guideline for selection of lung cancer patients for EGFR and ALK tyrosine kinase inhibitors: guideline from the College of American Pathologists, International Association for the Study of Lung Cancer, and Association for Molecular Pathology. J Mol Diagn. 2013, 15 (4): 415-453. 10.1016/j.jmoldx.2013.03.001.CrossRefPubMed Lindeman NI, Cagle PT, Beasley MB, Chitale DA, Dacic S, Giaccone G, Jenkins RB, Kwiatkowski DJ, Saldivar J-S, Squire J: Molecular testing guideline for selection of lung cancer patients for EGFR and ALK tyrosine kinase inhibitors: guideline from the College of American Pathologists, International Association for the Study of Lung Cancer, and Association for Molecular Pathology. J Mol Diagn. 2013, 15 (4): 415-453. 10.1016/j.jmoldx.2013.03.001.CrossRefPubMed
14.
go back to reference Aoki T, Hanamiya M, Uramoto H, Hisaoka M, Yamashita Y, Korogi Y: Adenocarcinomas with Predominant Ground-Glass Opacity: Correlation of Morphology and Molecular Biomarkers. Radiology. 2012, 264 (2): 590-596. 10.1148/radiol.12111337.CrossRefPubMed Aoki T, Hanamiya M, Uramoto H, Hisaoka M, Yamashita Y, Korogi Y: Adenocarcinomas with Predominant Ground-Glass Opacity: Correlation of Morphology and Molecular Biomarkers. Radiology. 2012, 264 (2): 590-596. 10.1148/radiol.12111337.CrossRefPubMed
15.
go back to reference Chung J-H, Choe G, Jheon S, Sung S-W, Kim TJ, Lee KW, Lee JH, Lee C-T: Epidermal growth factor receptor mutation and pathologic-radiologic correlation between multiple lung nodules with ground-glass opacity differentiates multicentric origin from intrapulmonary spread. J Thorac Oncol. 2009, 4 (12): 1490-1495. 10.1097/JTO.0b013e3181bc9731.CrossRefPubMed Chung J-H, Choe G, Jheon S, Sung S-W, Kim TJ, Lee KW, Lee JH, Lee C-T: Epidermal growth factor receptor mutation and pathologic-radiologic correlation between multiple lung nodules with ground-glass opacity differentiates multicentric origin from intrapulmonary spread. J Thorac Oncol. 2009, 4 (12): 1490-1495. 10.1097/JTO.0b013e3181bc9731.CrossRefPubMed
16.
go back to reference Yoshida Y, Kokubu A, Suzuki K, Kuribayashi H, Tsuta K, Matsuno Y, Kusumoto M, Kanai Y, Asamura H, Hirohashi S: Molecular markers and changes of computed tomography appearance in lung adenocarcinoma with ground-glass opacity. Jpn J Clin Oncol. 2007, 37 (12): 907-912. 10.1093/jjco/hym139.CrossRefPubMed Yoshida Y, Kokubu A, Suzuki K, Kuribayashi H, Tsuta K, Matsuno Y, Kusumoto M, Kanai Y, Asamura H, Hirohashi S: Molecular markers and changes of computed tomography appearance in lung adenocarcinoma with ground-glass opacity. Jpn J Clin Oncol. 2007, 37 (12): 907-912. 10.1093/jjco/hym139.CrossRefPubMed
17.
go back to reference Yano M, Sasaki H, Kobayashi Y, Yukiue H, Haneda H, Suzuki E, Endo K, Kawano O, Hara M, Fujii Y: Epidermal growth factor receptor gene mutation and computed tomographic findings in peripheral pulmonary adenocarcinoma. J Thorac Oncol. 2006, 1 (5): 413-416. 10.1097/01243894-200606000-00006.CrossRefPubMed Yano M, Sasaki H, Kobayashi Y, Yukiue H, Haneda H, Suzuki E, Endo K, Kawano O, Hara M, Fujii Y: Epidermal growth factor receptor gene mutation and computed tomographic findings in peripheral pulmonary adenocarcinoma. J Thorac Oncol. 2006, 1 (5): 413-416. 10.1097/01243894-200606000-00006.CrossRefPubMed
18.
go back to reference Okada M, Nishio W, Sakamoto T, Uchino K, Tsubota N: Discrepancy of computed tomographic image between lung and mediastinal windows as a prognostic implication in small lung adenocarcinoma. Ann Thorac Surg. 2003, 76 (6): 1828-1832. 10.1016/S0003-4975(03)01077-4.CrossRefPubMed Okada M, Nishio W, Sakamoto T, Uchino K, Tsubota N: Discrepancy of computed tomographic image between lung and mediastinal windows as a prognostic implication in small lung adenocarcinoma. Ann Thorac Surg. 2003, 76 (6): 1828-1832. 10.1016/S0003-4975(03)01077-4.CrossRefPubMed
19.
go back to reference Goldstraw P: The 7th Edition of TNM in Lung Cancer: what now?. J Thorac Oncol. 2009, 4 (6): 671-673. 10.1097/JTO.0b013e31819e7814.CrossRefPubMed Goldstraw P: The 7th Edition of TNM in Lung Cancer: what now?. J Thorac Oncol. 2009, 4 (6): 671-673. 10.1097/JTO.0b013e31819e7814.CrossRefPubMed
20.
go back to reference Kim HJ, Lee KY, Kim Y-C, Kim K-S, Lee SY, Jang TW, Lee MK, Shin K-C, Lee GH, Lee JC: Detection and comparison of peptide nucleic acid-mediated real-time polymerase chain reaction clamping and direct gene sequencing for epidermal growth factor receptor mutations in patients with non-small cell lung cancer. Lung Cancer. 2012, 75 (3): 321-325. 10.1016/j.lungcan.2011.08.005.CrossRefPubMed Kim HJ, Lee KY, Kim Y-C, Kim K-S, Lee SY, Jang TW, Lee MK, Shin K-C, Lee GH, Lee JC: Detection and comparison of peptide nucleic acid-mediated real-time polymerase chain reaction clamping and direct gene sequencing for epidermal growth factor receptor mutations in patients with non-small cell lung cancer. Lung Cancer. 2012, 75 (3): 321-325. 10.1016/j.lungcan.2011.08.005.CrossRefPubMed
21.
go back to reference Lee HJ, Xu X, Kim H, Jin Y, Sun P, Kim JE, Chung J-H: Comparison of Direct Sequencing, PNA Clamping-Real Time Polymerase Chain Reaction, and Pyrosequencing Methods for the Detection of EGFR Mutations in Non-small Cell Lung Carcinoma and the Correlation with Clinical Responses to EGFR Tyrosine Kinase Inhibitor. Korean J Pathol. 2013, 47 (1): 52-60. 10.4132/KoreanJPathol.2013.47.1.52.CrossRefPubMedPubMedCentral Lee HJ, Xu X, Kim H, Jin Y, Sun P, Kim JE, Chung J-H: Comparison of Direct Sequencing, PNA Clamping-Real Time Polymerase Chain Reaction, and Pyrosequencing Methods for the Detection of EGFR Mutations in Non-small Cell Lung Carcinoma and the Correlation with Clinical Responses to EGFR Tyrosine Kinase Inhibitor. Korean J Pathol. 2013, 47 (1): 52-60. 10.4132/KoreanJPathol.2013.47.1.52.CrossRefPubMedPubMedCentral
22.
go back to reference Paik JH, Choe G, Kim H, Choe J-Y, Lee HJ, Lee C-T, Lee JS, Jheon S, Chung J-H: Screening of anaplastic lymphoma kinase rearrangement by immunohistochemistry in non-small cell lung cancer: correlation with fluorescence in situ hybridization. J Thorac Oncol. 2011, 6 (3): 466-472. 10.1097/JTO.0b013e31820b82e8.CrossRefPubMed Paik JH, Choe G, Kim H, Choe J-Y, Lee HJ, Lee C-T, Lee JS, Jheon S, Chung J-H: Screening of anaplastic lymphoma kinase rearrangement by immunohistochemistry in non-small cell lung cancer: correlation with fluorescence in situ hybridization. J Thorac Oncol. 2011, 6 (3): 466-472. 10.1097/JTO.0b013e31820b82e8.CrossRefPubMed
23.
go back to reference Paik JH, Choi C-M, Kim H, Jang SJ, Choe G, Kim DK, Kim HJ, Yoon H, Lee C-T, Jheon S: Clinicopathologic implication of ALK rearrangement in surgically resected lung cancer: a proposal of diagnostic algorithm for ALK-rearranged adenocarcinoma. Lung Cancer. 2012, 76 (3): 403-409. 10.1016/j.lungcan.2011.11.008.CrossRefPubMed Paik JH, Choi C-M, Kim H, Jang SJ, Choe G, Kim DK, Kim HJ, Yoon H, Lee C-T, Jheon S: Clinicopathologic implication of ALK rearrangement in surgically resected lung cancer: a proposal of diagnostic algorithm for ALK-rearranged adenocarcinoma. Lung Cancer. 2012, 76 (3): 403-409. 10.1016/j.lungcan.2011.11.008.CrossRefPubMed
24.
go back to reference Kim H, Shim HS, Kim L, Kim T-J, Kwon KY, Lee GK, Chung J-H: Guideline Recommendations for Testing of ALK Gene Rearrangement in Lung Cancer: a Proposal of the Korean Cardiopulmonary Pathology Study Group. Korean J Pathol. 2014, 48: 1-9. 10.4132/KoreanJPathol.2014.48.1.1.CrossRefPubMedPubMedCentral Kim H, Shim HS, Kim L, Kim T-J, Kwon KY, Lee GK, Chung J-H: Guideline Recommendations for Testing of ALK Gene Rearrangement in Lung Cancer: a Proposal of the Korean Cardiopulmonary Pathology Study Group. Korean J Pathol. 2014, 48: 1-9. 10.4132/KoreanJPathol.2014.48.1.1.CrossRefPubMedPubMedCentral
25.
go back to reference Choi H, Paeng JC, Kim D-W, Lee JK, Park CM, Kang KW, Chung J-K, Lee DS: Metabolic and metastatic characteristics of ALK–rearranged lung adenocarcinoma on FDG PET/CT. Lung Cancer. 2013, 79 (3): 242-247. 10.1016/j.lungcan.2012.11.021.CrossRefPubMed Choi H, Paeng JC, Kim D-W, Lee JK, Park CM, Kang KW, Chung J-K, Lee DS: Metabolic and metastatic characteristics of ALK–rearranged lung adenocarcinoma on FDG PET/CT. Lung Cancer. 2013, 79 (3): 242-247. 10.1016/j.lungcan.2012.11.021.CrossRefPubMed
26.
go back to reference Koh Y, Kim D-W, Kim TM, Lee S-H, Jeon YK, Chung DH, Kim Y-W, Heo DS, Kim W-H, Bang Y-J: Clinicopathologic characteristics and outcomes of patients with anaplastic lymphoma kinase-positive advanced pulmonary adenocarcinoma: suggestion for an effective screening strategy for these tumors. J Thorac Oncol. 2011, 6 (5): 905-912. 10.1097/JTO.0b013e3182111461.CrossRefPubMed Koh Y, Kim D-W, Kim TM, Lee S-H, Jeon YK, Chung DH, Kim Y-W, Heo DS, Kim W-H, Bang Y-J: Clinicopathologic characteristics and outcomes of patients with anaplastic lymphoma kinase-positive advanced pulmonary adenocarcinoma: suggestion for an effective screening strategy for these tumors. J Thorac Oncol. 2011, 6 (5): 905-912. 10.1097/JTO.0b013e3182111461.CrossRefPubMed
27.
go back to reference Aoki T, Tomoda Y, Watanabe H, Nakata H, Kasai T, Hashimoto H, Kodate M, Osaki T, Yasumoto K: Peripheral Lung Adenocarcinoma: Correlation of Thin-Section CT Findings with Histologic Prognostic Factors and Survival. Radiology. 2001, 220 (3): 803-809. 10.1148/radiol.2203001701.CrossRefPubMed Aoki T, Tomoda Y, Watanabe H, Nakata H, Kasai T, Hashimoto H, Kodate M, Osaki T, Yasumoto K: Peripheral Lung Adenocarcinoma: Correlation of Thin-Section CT Findings with Histologic Prognostic Factors and Survival. Radiology. 2001, 220 (3): 803-809. 10.1148/radiol.2203001701.CrossRefPubMed
28.
go back to reference Takashima S, Maruyama Y, Hasegawa M, Yamanda T, Honda T, Kadoya M, Sone S: CT findings and progression of small peripheral lung neoplasms having a replacement growth pattern. Am J Roentgenol. 2003, 180 (3): 817-826. 10.2214/ajr.180.3.1800817.CrossRef Takashima S, Maruyama Y, Hasegawa M, Yamanda T, Honda T, Kadoya M, Sone S: CT findings and progression of small peripheral lung neoplasms having a replacement growth pattern. Am J Roentgenol. 2003, 180 (3): 817-826. 10.2214/ajr.180.3.1800817.CrossRef
29.
go back to reference Fukui T, Yatabe Y, Kobayashi Y, Tomizawa K, Ito S, Hatooka S, Matsuo K, Mitsudomi T: Clinicoradiologic characteristics of patients with lung adenocarcinoma harboring EML4-ALK fusion oncogene. Lung Cancer. 2012, 77 (2): 319-325. 10.1016/j.lungcan.2012.03.013.CrossRefPubMed Fukui T, Yatabe Y, Kobayashi Y, Tomizawa K, Ito S, Hatooka S, Matsuo K, Mitsudomi T: Clinicoradiologic characteristics of patients with lung adenocarcinoma harboring EML4-ALK fusion oncogene. Lung Cancer. 2012, 77 (2): 319-325. 10.1016/j.lungcan.2012.03.013.CrossRefPubMed
30.
go back to reference Rodig SJ, Mino-Kenudson M, Dacic S, Yeap BY, Shaw A, Barletta JA, Stubbs H, Law K, Lindeman N, Mark E: Unique clinicopathologic features characterize ALK-rearranged lung adenocarcinoma in the western population. Clin Cancer Res. 2009, 15 (16): 5216-5223. 10.1158/1078-0432.CCR-09-0802.CrossRefPubMedPubMedCentral Rodig SJ, Mino-Kenudson M, Dacic S, Yeap BY, Shaw A, Barletta JA, Stubbs H, Law K, Lindeman N, Mark E: Unique clinicopathologic features characterize ALK-rearranged lung adenocarcinoma in the western population. Clin Cancer Res. 2009, 15 (16): 5216-5223. 10.1158/1078-0432.CCR-09-0802.CrossRefPubMedPubMedCentral
31.
go back to reference Takeuchi K, Soda M, Togashi Y, Suzuki R, Sakata S, Hatano S, Asaka R, Hamanaka W, Ninomiya H, Uehara H: RET, ROS1 and ALK fusions in lung cancer. Nat Med. 2012, 18 (3): 378-381. 10.1038/nm.2658.CrossRefPubMed Takeuchi K, Soda M, Togashi Y, Suzuki R, Sakata S, Hatano S, Asaka R, Hamanaka W, Ninomiya H, Uehara H: RET, ROS1 and ALK fusions in lung cancer. Nat Med. 2012, 18 (3): 378-381. 10.1038/nm.2658.CrossRefPubMed
32.
go back to reference Wang Z, Zhang X, Bai H, Zhao J, Zhuo M, An T, Duan J, Yang L, Wu M, Wang S: EML4-ALK rearrangement and its clinical significance in Chinese patients with advanced non-small cell lung cancer. Oncology. 2012, 83 (5): 248-256. 10.1159/000341381.CrossRefPubMed Wang Z, Zhang X, Bai H, Zhao J, Zhuo M, An T, Duan J, Yang L, Wu M, Wang S: EML4-ALK rearrangement and its clinical significance in Chinese patients with advanced non-small cell lung cancer. Oncology. 2012, 83 (5): 248-256. 10.1159/000341381.CrossRefPubMed
33.
go back to reference Pillai RN, Ramalingam SS: The Biology and Clinical Features of Non–small Cell Lung Cancers with EML4-ALK Translocation. Curr Oncol Rep. 2012, 14 (2): 105-110. 10.1007/s11912-012-0213-4.CrossRefPubMed Pillai RN, Ramalingam SS: The Biology and Clinical Features of Non–small Cell Lung Cancers with EML4-ALK Translocation. Curr Oncol Rep. 2012, 14 (2): 105-110. 10.1007/s11912-012-0213-4.CrossRefPubMed
34.
go back to reference Jokoji R, Yamasaki T, Minami S, Komuta K, Sakamaki Y, Takeuchi K, Tsujimoto M: Combination of morphological feature analysis and immunohistochemistry is useful for screening of EML4-ALK-positive lung adenocarcinoma. J Clin Pathol. 2010, 63 (12): 1066-1070. 10.1136/jcp.2010.081166.CrossRefPubMed Jokoji R, Yamasaki T, Minami S, Komuta K, Sakamaki Y, Takeuchi K, Tsujimoto M: Combination of morphological feature analysis and immunohistochemistry is useful for screening of EML4-ALK-positive lung adenocarcinoma. J Clin Pathol. 2010, 63 (12): 1066-1070. 10.1136/jcp.2010.081166.CrossRefPubMed
35.
go back to reference Yoshida A, Tsuta K, Nakamura H, Kohno T, Takahashi F, Asamura H, Sekine I, Fukayama M, Shibata T, Furuta K: Comprehensive histologic analysis of ALK-rearranged lung carcinomas. Am J Surg Pathol. 2011, 35 (8): 1226-1234. 10.1097/PAS.0b013e3182233e06.CrossRefPubMed Yoshida A, Tsuta K, Nakamura H, Kohno T, Takahashi F, Asamura H, Sekine I, Fukayama M, Shibata T, Furuta K: Comprehensive histologic analysis of ALK-rearranged lung carcinomas. Am J Surg Pathol. 2011, 35 (8): 1226-1234. 10.1097/PAS.0b013e3182233e06.CrossRefPubMed
36.
go back to reference Park J, Yamaura H, Yatabe Y, Hosoda W, Kondo C, Shimizu J, Horio Y, Yoshida K, Tanaka K, Oguri T, Kobayashi Y, Hida H: Anaplastic lymphoma kinase gene rearrangements in patients with advanced-stage non-small-cell lung cancer: CT characteristics and response to chemotherapy. Cancer Med. 2014, 3 (1): 118-123. 10.1002/cam4.172.CrossRefPubMed Park J, Yamaura H, Yatabe Y, Hosoda W, Kondo C, Shimizu J, Horio Y, Yoshida K, Tanaka K, Oguri T, Kobayashi Y, Hida H: Anaplastic lymphoma kinase gene rearrangements in patients with advanced-stage non-small-cell lung cancer: CT characteristics and response to chemotherapy. Cancer Med. 2014, 3 (1): 118-123. 10.1002/cam4.172.CrossRefPubMed
37.
go back to reference Yatabe Y, Kosaka T, Takahashi T, Mitsudomi T: EGFR mutation is specific for terminal respiratory unit type adenocarcinoma. Am J Surg Pathol. 2005, 29 (5): 633-639. 10.1097/01.pas.0000157935.28066.35.CrossRefPubMed Yatabe Y, Kosaka T, Takahashi T, Mitsudomi T: EGFR mutation is specific for terminal respiratory unit type adenocarcinoma. Am J Surg Pathol. 2005, 29 (5): 633-639. 10.1097/01.pas.0000157935.28066.35.CrossRefPubMed
38.
go back to reference Park WY, Kim MH, Shin DH, Lee JH, Choi KU, Kim JY, Park DY, Lee CH, Sol MY: Ciliated adenocarcinomas of the lung: a tumor of non-terminal respiratory unit origin. Mod Pathol. 2012, 25 (9): 1265-1274. 10.1038/modpathol.2012.76.CrossRefPubMed Park WY, Kim MH, Shin DH, Lee JH, Choi KU, Kim JY, Park DY, Lee CH, Sol MY: Ciliated adenocarcinomas of the lung: a tumor of non-terminal respiratory unit origin. Mod Pathol. 2012, 25 (9): 1265-1274. 10.1038/modpathol.2012.76.CrossRefPubMed
39.
go back to reference Inamura K, Takeuchi K, Togashi Y, Hatano S, Ninomiya H, Motoi N, Mun M-y, Sakao Y, Okumura S, Nakagawa K: EML4-ALK lung cancers are characterized by rare other mutations, a TTF-1 cell lineage, an acinar histology, and young onset. Mod Pathol. 2009, 22 (4): 508-515. 10.1038/modpathol.2009.2.CrossRefPubMed Inamura K, Takeuchi K, Togashi Y, Hatano S, Ninomiya H, Motoi N, Mun M-y, Sakao Y, Okumura S, Nakagawa K: EML4-ALK lung cancers are characterized by rare other mutations, a TTF-1 cell lineage, an acinar histology, and young onset. Mod Pathol. 2009, 22 (4): 508-515. 10.1038/modpathol.2009.2.CrossRefPubMed
40.
go back to reference Li Y, Li Y, Yang T, Wei S, Wang J, Wang M, Wang Y, Zhou Q, Liu H, Chen J: Clinical Significance of EML4-ALK Fusion Gene and Association with EGFR and KRAS Gene Mutations in 208 Chinese Patients with Non-Small Cell Lung Cancer. PLoS One. 2013, 8 (1): e52093-10.1371/journal.pone.0052093.CrossRefPubMedPubMedCentral Li Y, Li Y, Yang T, Wei S, Wang J, Wang M, Wang Y, Zhou Q, Liu H, Chen J: Clinical Significance of EML4-ALK Fusion Gene and Association with EGFR and KRAS Gene Mutations in 208 Chinese Patients with Non-Small Cell Lung Cancer. PLoS One. 2013, 8 (1): e52093-10.1371/journal.pone.0052093.CrossRefPubMedPubMedCentral
41.
go back to reference Takahashi T, Kobayashi M, Yoshizawa A, Menju T, Nakayama E: Clinicopathologic features of non-small-cell lung cancer with EML4–ALK fusion gene. Ann Surg Oncol. 2010, 17 (3): 889-897. 10.1245/s10434-009-0808-7.CrossRefPubMed Takahashi T, Kobayashi M, Yoshizawa A, Menju T, Nakayama E: Clinicopathologic features of non-small-cell lung cancer with EML4–ALK fusion gene. Ann Surg Oncol. 2010, 17 (3): 889-897. 10.1245/s10434-009-0808-7.CrossRefPubMed
42.
go back to reference Kim H, Jang SJ, Chung DH, Yoo SB, Sun P, Jin Y, Nam KH, Paik JH, Chung JH: A comprehensive comparative analysis of the histomorphological features of ALK-rearranged lung adenocarcinoma based on driver oncogene mutations: frequent expression of epithelial-mesenchymal transition markers than other genotype. PLoS One. 2013, 8 (10): e76999-10.1371/journal.pone.0076999.CrossRefPubMedPubMedCentral Kim H, Jang SJ, Chung DH, Yoo SB, Sun P, Jin Y, Nam KH, Paik JH, Chung JH: A comprehensive comparative analysis of the histomorphological features of ALK-rearranged lung adenocarcinoma based on driver oncogene mutations: frequent expression of epithelial-mesenchymal transition markers than other genotype. PLoS One. 2013, 8 (10): e76999-10.1371/journal.pone.0076999.CrossRefPubMedPubMedCentral
43.
go back to reference Kang HJ, Lim HJ, Park JS, Cho YJ, Yoon HI, Chung JH, Lee JH, Lee CT: Comparison of clinical characteristics between patients with ALK-positive and EGFR-positive lung adenocarcinoma. Respir Med. 2014, 108 (2): 388-394. 10.1016/j.rmed.2013.11.020.CrossRefPubMed Kang HJ, Lim HJ, Park JS, Cho YJ, Yoon HI, Chung JH, Lee JH, Lee CT: Comparison of clinical characteristics between patients with ALK-positive and EGFR-positive lung adenocarcinoma. Respir Med. 2014, 108 (2): 388-394. 10.1016/j.rmed.2013.11.020.CrossRefPubMed
44.
go back to reference Lynch TJ, Bell DW, Sordella R, Gurubhagavatula S, Okimoto RA, Brannigan BW, Harris PL, Haserlat SM, Supko JG, Haluska FG: Activating mutations in the epidermal growth factor receptor underlying responsiveness of non–small-cell lung cancer to gefitinib. N Engl J Med. 2004, 350 (21): 2129-2139. 10.1056/NEJMoa040938.CrossRefPubMed Lynch TJ, Bell DW, Sordella R, Gurubhagavatula S, Okimoto RA, Brannigan BW, Harris PL, Haserlat SM, Supko JG, Haluska FG: Activating mutations in the epidermal growth factor receptor underlying responsiveness of non–small-cell lung cancer to gefitinib. N Engl J Med. 2004, 350 (21): 2129-2139. 10.1056/NEJMoa040938.CrossRefPubMed
45.
go back to reference Huang Y-s, Yang J-j, Zhang X-c, Yang X-n, Huang Y-j, Xu C-r, Zhou Q, Wang Z, Su J, Wu Y: Impact of smoking status and pathologic type on epidermal growth factor receptor mutations in lung cancer. Chin Med J. 2011, 124 (16): 2457-2460.PubMed Huang Y-s, Yang J-j, Zhang X-c, Yang X-n, Huang Y-j, Xu C-r, Zhou Q, Wang Z, Su J, Wu Y: Impact of smoking status and pathologic type on epidermal growth factor receptor mutations in lung cancer. Chin Med J. 2011, 124 (16): 2457-2460.PubMed
46.
go back to reference Kim HR, Ahn JR, Lee JG, Bang DH, Ha S-J, Hong YK, Kim SM, Nam KC, Rha SY, Soo RA: The Impact of Cigarette Smoking on the Frequency of and Qualitative Differences in KRAS Mutations in Korean Patients with Lung Adenocarcinoma. Yonsei Med J. 2013, 54 (4): 865-874. 10.3349/ymj.2013.54.4.865.CrossRefPubMedPubMedCentral Kim HR, Ahn JR, Lee JG, Bang DH, Ha S-J, Hong YK, Kim SM, Nam KC, Rha SY, Soo RA: The Impact of Cigarette Smoking on the Frequency of and Qualitative Differences in KRAS Mutations in Korean Patients with Lung Adenocarcinoma. Yonsei Med J. 2013, 54 (4): 865-874. 10.3349/ymj.2013.54.4.865.CrossRefPubMedPubMedCentral
47.
go back to reference Kosaka T, Yatabe Y, Endoh H, Kuwano H, Takahashi T, Mitsudomi T: Mutations of the epidermal growth factor receptor gene in lung cancer biological and clinical implications. Cancer Res. 2004, 64 (24): 8919-8923. 10.1158/0008-5472.CAN-04-2818.CrossRefPubMed Kosaka T, Yatabe Y, Endoh H, Kuwano H, Takahashi T, Mitsudomi T: Mutations of the epidermal growth factor receptor gene in lung cancer biological and clinical implications. Cancer Res. 2004, 64 (24): 8919-8923. 10.1158/0008-5472.CAN-04-2818.CrossRefPubMed
48.
go back to reference Liam C-K, Wahid MIA, Rajadurai P, Cheah Y-K, Ng TS-Y: Epidermal Growth Factor Receptor Mutations in Lung Adenocarcinoma in Malaysian Patients. J Thorac Oncol. 2013, 8 (6): 766-772. 10.1097/JTO.0b013e31828b5228.CrossRefPubMed Liam C-K, Wahid MIA, Rajadurai P, Cheah Y-K, Ng TS-Y: Epidermal Growth Factor Receptor Mutations in Lung Adenocarcinoma in Malaysian Patients. J Thorac Oncol. 2013, 8 (6): 766-772. 10.1097/JTO.0b013e31828b5228.CrossRefPubMed
49.
go back to reference Sun P-L, Seol H, Lee HJ, Yoo SB, Kim H, Xu X, Jheon S, Lee C-T, Lee J-S, Chung J-H: High Incidence of EGFR Mutations in Korean Men Smokers with No Intratumoral Heterogeneity of Lung Adenocarcinomas: Correlation with Histologic Subtypes, EGFR/TTF-1 Expressions, and Clinical Features. J Thorac Oncol. 2012, 7 (2): 323-330. 10.1097/JTO.0b013e3182381515.CrossRefPubMed Sun P-L, Seol H, Lee HJ, Yoo SB, Kim H, Xu X, Jheon S, Lee C-T, Lee J-S, Chung J-H: High Incidence of EGFR Mutations in Korean Men Smokers with No Intratumoral Heterogeneity of Lung Adenocarcinomas: Correlation with Histologic Subtypes, EGFR/TTF-1 Expressions, and Clinical Features. J Thorac Oncol. 2012, 7 (2): 323-330. 10.1097/JTO.0b013e3182381515.CrossRefPubMed
50.
go back to reference Uramoto H, So T, Nagata Y, Kuroda K, Shigematsu Y, Baba T, So T, Takenoyama M, Hanagiri T, Yasumoto K: Correlation between HLA alleles and EGFR mutation in Japanese patients with adenocarcinoma of the lung. J Thorac Oncol. 2010, 5 (8): 1136-1142. 10.1097/JTO.0b013e3181e0b993.CrossRefPubMed Uramoto H, So T, Nagata Y, Kuroda K, Shigematsu Y, Baba T, So T, Takenoyama M, Hanagiri T, Yasumoto K: Correlation between HLA alleles and EGFR mutation in Japanese patients with adenocarcinoma of the lung. J Thorac Oncol. 2010, 5 (8): 1136-1142. 10.1097/JTO.0b013e3181e0b993.CrossRefPubMed
51.
go back to reference Hsu K-H, Chen K-C, Yang T-Y, Yeh Y-C, Chou T-Y, Chen H-Y, Tsai C-R, Chen C-Y, Hsu C-P, Hsia J-Y: Epidermal growth factor receptor mutation status in stage I lung adenocarcinoma with different image patterns. J Thorac Oncol. 2011, 6 (6): 1066-1072. 10.1097/JTO.0b013e31821667b0.CrossRefPubMed Hsu K-H, Chen K-C, Yang T-Y, Yeh Y-C, Chou T-Y, Chen H-Y, Tsai C-R, Chen C-Y, Hsu C-P, Hsia J-Y: Epidermal growth factor receptor mutation status in stage I lung adenocarcinoma with different image patterns. J Thorac Oncol. 2011, 6 (6): 1066-1072. 10.1097/JTO.0b013e31821667b0.CrossRefPubMed
52.
go back to reference Lee H-J, Kim YT, Kang CH, Zhao B, Tan Y, Schwartz LH, Persigehl T, Jeon YK, Chung DH: Epidermal Growth Factor Receptor Mutation in Lung Adenocarcinomas: Relationship with CT Characteristics and Histologic Subtypes. Radiology. 2013, 268 (1): 254-264. 10.1148/radiol.13112553.CrossRefPubMed Lee H-J, Kim YT, Kang CH, Zhao B, Tan Y, Schwartz LH, Persigehl T, Jeon YK, Chung DH: Epidermal Growth Factor Receptor Mutation in Lung Adenocarcinomas: Relationship with CT Characteristics and Histologic Subtypes. Radiology. 2013, 268 (1): 254-264. 10.1148/radiol.13112553.CrossRefPubMed
Metadata
Title
Epidermal growth factor receptor mutations and anaplastic lymphoma kinase rearrangements in lung cancer with nodular ground-glass opacity
Authors
Sung-Jun Ko
Yeon Joo Lee
Jong Sun Park
Young-Jae Cho
Ho Il Yoon
Jin-Haeng Chung
Tae Jung Kim
Kyung Won Lee
Kwhanmien Kim
Sanghoon Jheon
Hyojin Kim
Jae Ho Lee
Choon-Taek Lee
Publication date
01-12-2014
Publisher
BioMed Central
Published in
BMC Cancer / Issue 1/2014
Electronic ISSN: 1471-2407
DOI
https://doi.org/10.1186/1471-2407-14-312

Other articles of this Issue 1/2014

BMC Cancer 1/2014 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine