Clinicopathological and demographical characteristics of non-small cell lung cancer patients with ALK rearrangements: A systematic review and meta-analysis

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Fan, Liang ^a   Feng, Yun ^a   Wan, Huanying ^a   Shi, Guochao ^a   Niu, Wenquan ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANAPLASTIC LYMPHOMA KINASE; EPIDERMAL GROWTH FACTOR RECEPTOR; K RAS PROTEIN; PROTEIN TYROSINE KINASE;

AGE; CANCER STAGING; DEMOGRAPHY; DISEASE ASSOCIATION; ENZYME POLYMORPHISM; ENZYME REARRANGEMENT; GENE MUTATION; HISTOLOGY; HUMAN; INTERESTERIFICATION; LUNG ADENOCARCINOMA; LUNG NON SMALL CELL CANCER; PATHOLOGY; RACE DIFFERENCE; REVIEW; RISK FACTOR; SEX DIFFERENCE; SMOKING HABIT; SYSTEMATIC REVIEW; ADENOCARCINOMA; ADULT; CARCINOMA, NON-SMALL-CELL LUNG; FEMALE; GENE REARRANGEMENT; GENETICS; LUNG NEOPLASMS; MALE; META ANALYSIS; ODDS RATIO;

ADENOCARCINOMA; ADULT; AGE FACTORS; CARCINOMA, NON-SMALL-CELL LUNG; FEMALE; GENE REARRANGEMENT; HUMANS; LUNG NEOPLASMS; MALE; ODDS RATIO; RECEPTOR PROTEIN-TYROSINE KINASES; SEX FACTORS;

EID: 84903525241     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0100866     Document Type: Review

References (78)

1. Lynch TJ, Bell DW, Sordella R, Gurubhagavatula S, Okimoto RA, et al. (2004) Activating mutations in the epidermal growth factor receptor underlying responsiveness of non-small-cell lung cancer to gefitinib. N Engl J Med 350: 2129-2139. (Pubitemid 38637993)
2. Soda M, Choi YL, Enomoto M, Takada S, Yamashita Y, et al. (2007) Identification of the transforming EML4-ALK fusion gene in non-small-cell lung cancer. Nature 448: 561-566. (Pubitemid 47206930)
3. Mano H (2008) Non-solid oncogenes in solid tumors: EML4-ALK fusion genes in lung cancer. Cancer Sci 99: 2349-2355.
4. Shinmura K, Kageyama S, Tao H, Bunai T, Suzuki M, et al. (2008) EML4-ALK fusion transcripts, but no NPM-, TPM3-, CLTC-, ATIC-, or TFG-ALK fusion transcripts, in non-small cell lung carcinomas. Lung Cancer 61: 163-169.
5. Chen Z, Sasaki T, Tan X, Carretero J, Shimamura T, et al. (2010) Inhibition of ALK, PI3K/MEK, and HSP90 in murine lung adenocarcinoma induced by EML4-ALK fusion oncogene. Cancer Res 70: 9827-9836.
6. Kwak EL, Bang YJ, Camidge DR, Shaw AT, Solomon B, et al. (2010) Anaplastic lymphoma kinase inhibition in non-small-cell lung cancer. N Engl J Med 363: 1693-1703.
7. Shaw AT, Yeap BY, Solomon BJ, Riely GJ, Gainor J, et al. (2011) Effect of crizotinib on overall survival in patients with advanced non-small-cell lung cancer harbouring ALK gene rearrangement: a retrospective analysis. Lancet Oncol 12: 1004-1012.
8. Paik JH, Choi CM, Kim H, Jang SJ, Choe G, et al. (2012) Clinicopathologic implication of ALK rearrangement in surgically resected lung cancer: a proposal of diagnostic algorithm for ALK-rearranged adenocarcinoma. Lung Cancer 76: 403-409.
9. Soda M, Isobe K, Inoue A, Maemondo M, Oizumi S, et al. (2012) A Prospective PCR-Based Screening for the EML4-ALK Oncogene in Non-Small Cell Lung Cancer. Clin Cancer Res 11: 11.
10. Takahashi T, Sonobe M, Kobayashi M, Yoshizawa A, Menju T, et al. (2010) Clinicopathologic features of non-small-cell lung cancer with EML4-ALK fusion gene. Ann Surg Oncol 17: 889-897.
11. Takeuchi K, Soda M, Togashi Y, Suzuki R, Sakata S, et al. (2012) RET, ROS1 and ALK fusions in lung cancer. Nat Med 18: 378-381.
12. Dai Z, Kelly JC, Meloni-Ehrig A, Slovak ML, Boles D, et al. (2012) Incidence and patterns of ALK FISH abnormalities seen in a large unselected series of lung carcinomas. Mol Cytogenet 5: 1755-8166.
13. Moher D, Liberati A, Tetzlaff J, Altman DG (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med 151: 264-269, W264.
14. Sweeting MJ, Sutton AJ, Lambert PC (2004) What to add to nothing? Use and avoidance of continuity corrections in meta-analysis of sparse data. Stat Med 23: 1351-1375. (Pubitemid 38594143)
15. Hozo SP, Djulbegovic B, Hozo I (2005) Estimating the mean and variance from the median, range, and the size of a sample. BMC medical research methodology 5: 13.
16. Niu W, Qi Y, Qian Y, Gao P, Zhu D (2009) The relationship between apolipoprotein E epsilon2/epsilon3/epsilon4 polymorphisms and hypertension: a meta-analysis of six studies comprising 1812 cases and 1762 controls. Hypertens Res 32: 1060-1066.
17. Zhou JX, Yang H, Deng Q, Gu X, He P, et al. (2013) Oncogenic driver mutations in patients with non-small-cell lung cancer at various clinical stages. Ann Oncol 24: 1319-1325.
18. Conde E, Angulo B, Izquierdo E, Munoz L, Suarez-Gauthier A, et al. (2013) The ALK translocation in advanced non-small-cell lung carcinomas: preapproval testing experience at a single cancer centre. Histopathology 62: 609-616.
19. Wang R, Hu H, Pan Y, Li Y, Ye T, et al. (2012) RET fusions define a unique molecular and clinicopathologic subtype of non-small-cell lung cancer. J Clin Oncol 30: 4352-4359.
20. Soda M, Isobe K, Inoue A, Maemondo M, Oizumi S, et al. (2012) A prospective PCR-based screening for the EML4-ALK oncogene in non-small cell lung cancer. Clin Cancer Res 18: 5682-5689.
21. Seo JS, Ju YS, Lee WC, Shin JY, Lee JK, et al. (2012) The transcriptional landscape and mutational profile of lung adenocarcinoma. Genome Res 22: 2109-2119.
22. Sakai K, Okamoto I, Takezawa K, Hirashima T, Kaneda H, et al. (2012) A novel mass spectrometry-based assay for diagnosis of EML4-ALK-positive non-small cell lung cancer. J Thorac Oncol 7: 913-918.
23. Rimkunas VM, Crosby KE, Li D, Hu Y, Kelly ME, et al. (2012) Analysis of receptor tyrosine kinase ROS1-positive tumors in non-small cell lung cancer: identification of a FIG-ROS1 fusion. Clin Cancer Res 18: 4449-4457.
24. Cardarella S, Ortiz TM, Joshi VA, Butaney M, Jackman DM, et al. (2012) The introduction of systematic genomic testing for patients with non-small-cell lung cancer. J Thorac Oncol 7: 1767-1774.
25. Paik PK, Johnson ML, D'Angelo SP, Sima CS, Ang D, et al. (2012) Driver mutations determine survival in smokers and never-smokers with stage IIIB/IV lung adenocarcinomas. Cancer 118: 5840-5847.
26. Lee JK, Kim TM, Koh Y, Lee SH, Kim DW, et al. (2012) Differential sensitivities to tyrosine kinase inhibitors in NSCLC harboring EGFR mutation and ALK translocation. Lung Cancer 77: 460-463.
27. Kanaji N, Bandoh S, Ishii T, Tadokoro A, Watanabe N, et al. (2012) Detection of EML4-ALK fusion genes in a few cancer cells from transbronchial cytological specimens utilizing immediate cytology during bronchoscopy. Lung Cancer 77: 293-298.
28. Jin G, Jeon HS, Lee EB, Kang HG, Yoo SS, et al. (2012) EML4-ALK fusion gene in Korean non-small cell lung cancer. J Korean Med Sci 27: 228-230.
29. Ilie M, Long E, Butori C, Hofman V, Coelle C, et al. (2012) ALK-gene rearrangement: a comparative analysis on circulating tumour cells and tumour tissue from patients with lung adenocarcinoma. Ann Oncol 23: 2907-2913.
30. Fukui T, Yatabe Y, Kobayashi Y, Tomizawa K, Ito S, et al. (2012) Clinicoradiologic characteristics of patients with lung adenocarcinoma harboring EML4-ALK fusion oncogene. Lung Cancer 77: 319-325.
31. Chen TD, Chang IC, Liu HP, Wu YC, Wang CL, et al. (2012) Correlation of anaplastic lymphoma kinase overexpression and the EML4-ALK fusion gene in non-small cell lung cancer by immunohistochemical study. Chang Gung Med J 35: 309-317.
32. An SJ, Chen ZH, Su J, Zhang XC, Zhong WZ, et al. (2012) Identification of enriched driver gene alterations in subgroups of non-small cell lung cancer patients based on histology and smoking status. PLoS One 7: 29.
33. Salido M, Pijuan L, Martinez-Aviles L, Galvan AB, Canadas I, et al. (2011) Increased ALK gene copy number and amplification are frequent in non-small cell lung cancer. J Thorac Oncol 6: 21-27.
34. Zhang X, Zhang S, Yang X, Yang J, Zhou Q, et al. (2010) Fusion of EML4 and ALK is associated with development of lung adenocarcinomas lacking EGFR and KRAS mutations and is correlated with ALK expression. Mol Cancer 9: 1476-4598.
35. Sakairi Y, Nakajima T, Yasufuku K, Ikebe D, Kageyama H, et al. (2010) EML4-ALK fusion gene assessment using metastatic lymph node samples obtained by endobronchial ultrasound-guided transbronchial needle aspiration. Clin Cancer Res 16: 4938-4945.
36. Jokoji R, Yamasaki T, Minami S, Komuta K, Sakamaki Y, et al. (2010) Combination of morphological feature analysis and immunohistochemistry is useful for screening of EML4-ALK-positive lung adenocarcinoma. J Clin Pathol 63: 1066-1070.
37. Wong DW, Leung EL, So KK, Tam IY, Sihoe AD, et al. (2009) The EML4-ALK fusion gene is involved in various histologic types of lung cancers from nonsmokers with wild-type EGFR and KRAS. Cancer 115: 1723-1733.
38. Rodig SJ, Mino-Kenudson M, Dacic S, Yeap BY, Shaw A, et al. (2009) Unique clinicopathologic features characterize ALK-rearranged lung adenocarcinoma in the western population. Clin Cancer Res 15: 5216-5223.
39. Martelli MP, Sozzi G, Hernandez L, Pettirossi V, Navarro A, et al. (2009) EML4-ALK rearrangement in non-small cell lung cancer and non-tumor lung tissues. Am J Pathol 174: 661-670.
40. Inamura K, Takeuchi K, Togashi Y, Hatano S, Ninomiya H, et al. (2009) EML4-ALK lung cancers are characterized by rare other mutations, a TTF-1 cell lineage, an acinar histology, and young onset. Mod Pathol 22: 508-515.
41. Boland JM, Erdogan S, Vasmatzis G, Yang P, Tillmans LS, et al. (2009) Anaplastic lymphoma kinase immunoreactivity correlates with ALK gene rearrangement and transcriptional up-regulation in non-small cell lung carcinomas. Hum Pathol 40: 1152-1158.
42. Zhang YG, Jin ML, Li L, Zhao HY, Zeng X, et al. (2013) Evaluation of ALK rearrangement in Chinese non-small cell lung cancer using FISH, immunohistochemistry, and real-time quantitative RT- PCR on paraffin-embedded tissues. PLoS One 8.
43. Yamaguchi N, Vanderlaan PA, Folch E, Boucher DH, Canepa HM, et al. (2013) Smoking status and self-reported race affect the frequency of clinically relevant oncogenic alterations in non-small-cell lung cancers at a United States-based academic medical practice. Lung Cancer 7: 013.
44. Xia N, An J, Jiang QQ, Li M, Tan J, et al. (2013) Analysis of EGFR, EML4-ALK, KRAS, and c-MET mutations in Chinese lung adenocarcinoma patients. Exp Lung Res 6: 6.
45. To KF, Tong JH, Yeung KS, Lung RW, Law PP, et al. (2013) Detection of ALK rearrangement by immunohistochemistry in lung adenocarcinoma and the identification of a novel EML4-ALK variant. J Thorac Oncol 8: 883-891.
46. Takamochi K, Takeuchi K, Hayashi T, Oh S, Suzuki K (2013) A Rational Diagnostic Algorithm for the Identification of ALK Rearrangement in Lung Cancer: A Comprehensive Study of Surgically Treated Japanese Patients. PLoS One 8.
47. Sakai Y, Nakai T, Ohbayashi C, Imagawa N, Yanagita E, et al. (2013) Immunohistochemical Profiling of ALK Fusion Gene-Positive Adenocarcinomas of the Lung. Int J Surg Pathol 20: 20.
48. Martinez P, Hernandez-Losa J, Montero MA, Cedres S, Castellvi J, et al. (2013) Fluorescence in situ hybridization and immunohistochemistry as diagnostic methods for ALK positive non-small cell lung cancer patients. PLoS One 8: 24.
49. Li Y, Pan Y, Wang R, Sun Y, Hu H, et al. (2013) ALK-Rearranged Lung Cancer in Chinese: A Comprehensive Assessment of Clinicopathology, IHC, FISH and RT-PCR. PLoS One 8.
50. Li Y, Li Y, Yang T, Wei S, Wang J, et al. (2013) 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 8: 14.
51. Perner S, Wagner PL, Demichelis F, Mehra R, Lafargue CJ, et al. (2008) EML4-ALK fusion lung cancer: a rare acquired event. Neoplasia 10: 298-302. (Pubitemid 351328588)
52. Koivunen JP, Mermel C, Zejnullahu K, Murphy C, Lifshits E, et al. (2008) EML4-ALK fusion gene and efficacy of an ALK kinase inhibitor in lung cancer. Clin Cancer Res 14: 4275-4283.
53. Lee HY, Ahn HK, Jeong JY, Kwon MJ, Han JH, et al. (2013) Favorable clinical outcomes of pemetrexed treatment in anaplastic lymphoma kinase positive non-small-cell lung cancer. Lung Cancer 79: 40-45.
54. Gainor JF, Varghese AM, Ou SH, Kabraji S, Awad MM, et al. (2013) ALK Rearrangements Are Mutually Exclusive with Mutations in EGFR or KRAS: An Analysis of 1,683 Patients with Non-Small Cell Lung Cancer. Clin Cancer Res 19: 4273-4281.
55. Desai SS, Shah AS, Prabhash K, Jambhekar NA (2013) A year of anaplastic large cell kinase testing for lung carcinoma: Pathological and technical perspectives. Indian J Cancer 50: 80-86.
56. Laszlo A, Thotala D, Hallahan DE (2013) Membrane phospholipids, EML4-ALK, and Hsp90 as novel targets in lung cancer treatment. Cancer J 19: 238-246.
57. Zhang Y, Sun Y, Pan Y, Li C, Shen L, et al. (2012) Frequency of driver mutations in lung adenocarcinoma from female never-smokers varies with histologic subtypes and age at diagnosis. Clin Cancer Res 18: 1947-1953.
58. Yoon HJ, Lee HY, Lee KS, Choi YL, Ahn MJ, et al. (2012) Repeat biopsy for mutational analysis of non-small cell lung cancers resistant to previous chemotherapy: adequacy and complications. Radiology 265: 939-948.
59. Yang P, Kulig K, Boland JM, Erickson-Johnson MR, Oliveira AM, et al. (2012) Worse disease-free survival in never-smokers with ALK+ lung adenocarcinoma. J Thorac Oncol 7: 90-97.
60. Wu SG, Kuo YW, Chang YL, Shih JY, Chen YH, et al. (2012) EML4-ALK translocation predicts better outcome in lung adenocarcinoma patients with wild-type EGFR. J Thorac Oncol 7: 98-104.
61. Wang Z, Zhang X, Bai H, Zhao J, Zhuo M, et al. (2012) EML4-ALK rearrangement and its clinical significance in Chinese patients with advanced non-small cell lung cancer. Oncology 83: 248-256.
62. Wallander ML, Geiersbach KB, Tripp SR, Layfield LJ (2012) Comparison of reverse transcription-polymerase chain reaction, immunohistochemistry, and fluorescence in situ hybridization methodologies for detection of echinoderm microtubule-associated proteinlike 4-anaplastic lymphoma kinase fusion-positive non-small cell lung carcinoma: implications for optimal clinical testing. Arch Pathol Lab Med 136: 796-803.
63. Takeda M, Okamoto I, Sakai K, Kawakami H, Nishio K, et al. (2012) Clinical outcome for EML4-ALK-positive patients with advanced non-small-cell lung cancer treated with first-line platinum-based chemotherapy. Ann Oncol 23: 2931-2936.
64. Shaozhang Z, Xiaomei L, Aiping Z, Jianbo H, Xiangqun S, et al. (2012) Detection of EML4-ALK fusion genes in non-small cell lung cancer patients with clinical features associated with EGFR mutations. Genes Chromosomes Cancer 51: 925-932.
65. Ren S, Kuang P, Zheng L, Su C, Li J, et al. (2012) Analysis of driver mutations in female non-smoker Asian patients with pulmonary adenocarcinoma. Cell Biochem Biophys 64: 155-160.
66. Park HS, Lee JK, Kim DW, Kulig K, Kim TM, et al. (2012) Immunohistochemical screening for anaplastic lymphoma kinase (ALK) rearrangement in advanced non-small cell lung cancer patients. Lung Cancer 77: 288-292.
67. Kim HR, Shim HS, Chung JH, Lee YJ, Hong YK, et al. (2012) Distinct clinical features and outcomes in never-smokers with nonsmall cell lung cancer who harbor EGFR or KRAS mutations or ALK rearrangement. Cancer 118: 729-739.
68. Just PA, Cazes A, Audebourg A, Cessot A, Pallier K, et al. (2012) Histologic subtypes, immunohistochemistry, FISH or molecular screening for the accurate diagnosis of ALK-rearrangement in lung cancer: a comprehensive study of Caucasian non-smokers. Lung Cancer 76: 309-315.
69. Doebele RC, Lu X, Sumey C, Maxson DA, Weickhardt AJ, et al. (2012) Oncogene status predicts patterns of metastatic spread in treatment-naive nonsmall cell lung cancer. Cancer 118: 4502-4511.
70. Li C, Fang R, Sun Y, Han X, Li F, et al. (2011) Spectrum of oncogenic driver mutations in lung adenocarcinomas from East Asian never smokers. PLoS One 6: 30.
71. Lee JO, Kim TM, Lee SH, Kim DW, Kim S, et al. (2011) Anaplastic lymphoma kinase translocation: a predictive biomarker of pemetrexed in patients with non-small cell lung cancer. J Thorac Oncol 6: 1474-1480.
72. Koh Y, Kim DW, Kim TM, Lee SH, Jeon YK, et al. (2011) 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 6: 905-912.
73. Shaw AT, Yeap BY, Mino-Kenudson M, Digumarthy SR, Costa DB, et al. (2009) Clinical features and outcome of patients with non-small-cell lung cancer who harbor EML4-ALK. J Clin Oncol 27: 4247-4253.
74. Kobayashi M, Sonobe M, Takahashi T, Yoshizawa A, Kikuchi R, et al. (2012) Detection of ALK fusion in lung cancer using fluorescence in situ hybridization. Asian Cardiovasc Thorac Ann 20: 426-431.
75. Ettinger DS, Akerley W, Borghaei H, Chang AC, Cheney RT, et al. (2012) Non-small cell lung cancer. J Natl Compr Canc Netw 10: 1236-1271.
76. Shaw AT, Engelman JA (2013) ALK in lung cancer: past, present, and future. J Clin Oncol 31: 1105-1111.
77. Ren S, Kuang P, Zheng L, Su C, Li J, et al. (2012) Analysis of Driver Mutations in Female Non-Smoker Asian Patients with Pulmonary Adenocarcinoma. Cell Biochem Biophys 17: 17.
78. Yoshida A, Tsuta K, Nakamura H, Kohno T, Takahashi F, et al. (2011) Comprehensive histologic analysis of ALK-rearranged lung carcinomas. Am J Surg Pathol 35: 1226-1234.