Diagnostic algorithm for detection of targetable driver mutations in lung adenocarcinomas: Comprehensive analyses of 205 cases with immunohistochemistry, real-time PCR and fluorescence in situ hybridization methods

Lung Cancer

Volumn 101, Issue , 2016, Pages 40-47

  Kao, Hua Lin ^a,b,c   Yeh, Yi Chen ^a,b   Lin, Chin Hsuan ^a,d   Hsu, Wei Fang ^a   Hsieh, Wen Yu ^a   Ho, Hsiang Ling ^a   Chou, Teh Ying ^a,b  

^a TAIPEI VETERANS GENERAL HOSPITAL   (Taiwan)

^b NATIONAL YANG MING UNIVERSITY   (Taiwan)

^c CATHAY GENERAL HOSPITAL   (Taiwan)

^d CHENG CHING GENERAL HOSPITAL   (Taiwan)

Author keywords

Driver mutations; Immunohistochemistry; Lung adenocarcinoma; Molecular testing

Indexed keywords

ANAPLASTIC LYMPHOMA KINASE; ANTIBODY; EPIDERMAL GROWTH FACTOR RECEPTOR; PROTEIN; ROS1 PROTEIN; UNCLASSIFIED DRUG; EGFR PROTEIN, HUMAN; ONCOPROTEIN; PROTEIN TYROSINE KINASE; ROS1 PROTEIN, HUMAN;

ADULT; AGED; ARTICLE; CANCER DIAGNOSIS; CANCER TISSUE; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; GENE MUTATION; GENE REARRANGEMENT; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; INTERMETHOD COMPARISON; LUNG ADENOCARCINOMA; MAJOR CLINICAL STUDY; MALE; MOLECULAR DIAGNOSIS; MOLECULAR GENETICS; MUTATIONAL ANALYSIS; ONCOGENE; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; SENSITIVITY AND SPECIFICITY; TAIWANESE; TISSUE MICROARRAY; ADENOCARCINOMA; ALGORITHM; CANCER STAGING; GENETICS; LUNG TUMOR; MIDDLE AGED; MUTATION; PATHOLOGY; PROCEDURES; PROSPECTIVE STUDY;

ADENOCARCINOMA; AGED; ALGORITHMS; FEMALE; GENE REARRANGEMENT; HUMANS; IN SITU HYBRIDIZATION, FLUORESCENCE; LUNG NEOPLASMS; MALE; MIDDLE AGED; MUTATION; NEOPLASM STAGING; PROSPECTIVE STUDIES; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS; RECEPTOR, EPIDERMAL GROWTH FACTOR;

EID: 84988025920     PISSN: 01695002     EISSN: 18728332     Source Type: Journal    
DOI: 10.1016/j.lungcan.2016.09.007     Document Type: Article

References (42)

1. [1] Novaes, F.T., Cataneo, D.C., Ruiz Junior, R.L., Defaveri, J., Michelin, O.C., Cataneo, A.J., Lung cancer: histology, staging, treatment and survival. J. Bras. Pneumol. 34 (2008), 595–600.
2. [2] Siegel, R., Ma, J., Zou, Z., Jemal, A., Cancer statistics 2014. CA Cancer J. Clin. 64 (2014), 9–29.
3. [3] Berge, E.M., Doebele, R.C., Targeted therapies in non-small cell lung cancer: emerging oncogene targets following the success of epidermal growth factor receptor. Semin. Oncol. 41 (2014), 110–125.
4. [4] Forde, P.M., Ettinger, D.S., Targeted therapy for non-small-cell lung cancer: past, present and future. Expert Rev. Anticancer Ther. 13 (2013), 745–758.
5. [5] Wood, S.L., Pernemalm, M., Crosbie, P.A., Whetton, A.D., Molecular histology of lung cancer: from targets to treatments. Cancer Treat. Rev. 41 (2015), 361–375.
6. [6] Rosell, R., Bivona, T.G., Karachaliou, N., Genetics and biomarkers in personalisation of lung cancer treatment. Lancet 382 (2013), 720–731.
7. [7] Alamgeer, M., Ganju, V., Watkins, D.N., Novel therapeutic targets in non-small cell lung cancer. Curr. Opin. Pharmacol. 13 (2013), 394–401.
8. [8] McCourt, C.M., Boyle, D., James, J., Salto-Tellez, M., Immunohistochemistry in the era of personalised medicine. J. Clin. Pathol. 66 (2013), 58–61.
9. [9] Travis, W.D., Brambilla, E., Burke, A.P., Marx, A., Nicholson, A.G., WHO Classification of Tumours of The Lung, Pleura, Thymus and Heart. Fourth ed., 2015, IARC Press, Lyon.
10. [10] Kadota, K., Yeh, Y.C., Sima, C.S., Rusch, V.W., Moreira, A.L., Adusumilli, P.S., Travis, W.D., The cribriform pattern identifies a subset of acinar predominant tumors with poor prognosis in patients with stage I lung adenocarcinoma: a conceptual proposal to classify cribriform predominant tumors as a distinct histologic subtype. Mod. Pathol. 27 (2014), 690–700.
11. [11] Edge, S., Byrd, D.R., Compton, C.C., Fritz, A.G., Greene, F.L., Trotti, A., (eds.) AJCC Cancer Staging Manual, 7th ed., 2010, Springer, New York.
12. [12] Ho, H.L., Chang, F.P., Ma, H.H., Liao, L.R., Chuang, Y.T., Chang-Chien, Y.C., Lin, K.Y., Chou, T.Y., Molecular diagnostic algorithm for epidermal growth factor receptor mutation detection in Asian lung adenocarcinomas: comprehensive analyses of 445 Taiwanese patients with immunohistochemistry, PCR-direct sequencing and Scorpion/ARMS methods. Respirology 18 (2013), 1261–1270.
13. [13] Roma, C., Esposito, C., Rachiglio, A.M., Pasquale, R., Iannaccone, A., Chicchinelli, N., Franco, R., Mancini, R., Pisconti, S., De Luca, A., Botti, G., Morabito, A., Normanno, N., Detection of EGFR mutations by TaqMan mutation detection assays powered by competitive allele-specific TaqMan PCR technology. Biomed Res. Int., 2013, 2013, 385087.
14. [14] Mescam-Mancini, L., Lantuejoul, S., Moro-Sibilot, D., Rouquette, I., Souquet, P.J., Audigier-Valette, C., Sabourin, J.C., Decroisette, C., Sakhri, L., Brambilla, E., McLeer-Florin, A., On the relevance of a testing algorithm for the detection of ROS1-rearranged lung adenocarcinomas. Lung Cancer 83 (2014), 168–173.
15. [15] Shan, L., Lian, F., Guo, L., Qiu, T., Ling, Y., Ying, J., Lin, D., Detection of ROS1 gene rearrangement in lung adenocarcinoma: comparison of IHC, FISH and real-time RT-PCR. PLoS One, 10, 2015, e0120422.
16. [16] Simonetti, S., Molina, M.A., Queralt, C., de Aguirre, I., Mayo, C., Bertran-Alamillo, J., Sanchez, J.J., Gonzalez-Larriba, J.L., Jimenez, U., Isla, D., Moran, T., Viteri, S., Camps, C., Garcia-Campelo, R., Massuti, B., Benlloch, S., Ramon y Cajal, S., Taron, M., Rosell, R., Detection of EGFR mutations with mutation-specific antibodies in stage IV non-small-cell lung cancer. J. Transl. Med., 8, 2010, 135.
17. [17] Kitamura, A., Hosoda, W., Sasaki, E., Mitsudomi, T., Yatabe, Y., Immunohistochemical detection of EGFR mutation using mutation-specific antibodies in lung cancer. Clin. Cancer Res. 16 (2010), 3349–3355.
18. [18] Xiong, Y., Bai, Y., Leong, N., Laughlin, T.S., Rothberg, P.G., Xu, H., Nong, L., Zhao, J., Dong, Y., Li, T., Immunohistochemical detection of mutations in the epidermal growth factor receptor gene in lung adenocarcinomas using mutation-specific antibodies. Diagn. Pathol., 8, 2013, 27.
19. [19] Hofman, P., Ilie, M., Hofman, V., Roux, S., Valent, A., Bernheim, A., Alifano, M., Leroy-Ladurie, F., Vaylet, F., Rouquette, I., Validire, P., Beau-Faller, M., Lacroix, L., Soria, J.C., Fouret, P., Immunohistochemistry to identify EGFR mutations or ALK rearrangements in patients with lung adenocarcinoma. Ann. Oncol 23 (2012), 1738–1743.
20. [20] Kato, Y., Peled, N., Wynes, M.W., Yoshida, K., Pardo, M., Mascaux, C., Ohira, T., Tsuboi, M., Matsubayashi, J., Nagao, T., Ikeda, N., Hirsch, F.R., Novel epidermal growth factor receptor mutation-specific antibodies for non-small cell lung cancer: immunohistochemistry as a possible screening method for epidermal growth factor receptor mutations. J. Thorac. Oncol. 5 (2010), 1551–1558.
21. [21] Kozu, Y., Tsuta, K., Kohno, T., Sekine, I., Yoshida, A., Watanabe, S., Tamura, T., Yokota, J., Suzuki, K., Asamura, H., Furuta, K., Tsuda, H., The usefulness of mutation-specific antibodies in detecting epidermal growth factor receptor mutations and in predicting response to tyrosine kinase inhibitor therapy in lung adenocarcinoma. Lung Cancer 73 (2011), 45–50.
22. [22] Allo, G., Bandarchi, B., Yanagawa, N., Wang, A., Shih, W., Xu, J., Dalby, M., Nitta, H., To, C., Liu, N., Sykes, J., Tsao, M.S., Epidermal growth factor receptor mutation-specific immunohistochemical antibodies in lung adenocarcinoma. Histopathology 64 (2014), 826–839.
23. [23] Kim, C.H., Kim, S.H., Park, S.Y., Yoo, J., Kim, S.K., Kim, H.K., Identification of EGFR mutations by immunohistochemistry with EGFR mutation-specific antibodies in biopsy and resection specimens from pulmonary adenocarcinoma. Cancer Res. Treat. 47 (2015), 653–660.
24. [24] Mino-Kenudson, M., Chirieac, L.R., Law, K., Hornick, J.L., Lindeman, N., Mark, E.J., Cohen, D.W., Johnson, B.E., Janne, P.A., Iafrate, A.J., Rodig, S.J., A novel, highly sensitive antibody allows for the routine detection of ALK-rearranged lung adenocarcinomas by standard immunohistochemistry. Clin. Cancer Res. 16 (2010), 1561–1571.
25. [25] Paik, J.H., Choe, G., Kim, H., Choe, J.Y., Lee, H.J., Lee, C.T., Lee, J.S., 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. 6 (2011), 466–472.
26. [26] Seo, J.S., Ju, Y.S., Lee, W.C., Shin, J.Y., Lee, J.K., Bleazard, T., Lee, J., Jung, Y.J., Kim, J.O., Shin, J.Y., Yu, S.B., Kim, J., Lee, E.R., Kang, C.H., Park, I.K., Rhee, H., Lee, S.H., Kim, J.I., Kang, J.H., Kim, Y.T., The transcriptional landscape and mutational profile of lung adenocarcinoma. Genome Res. 22 (2012), 2109–2119.
27. [27] Le Quesne, J., Maurya, M., Yancheva, S.G., O'Brien, M., Popat, S., Wotherspoon, A.C., de Castro, D.G., Nicholson, A.G., A comparison of immunohistochemical assays and FISH in detecting the ALK translocation in diagnostic histological and cytological lung tumor material. J. Thorac. Oncol. 9 (2014), 769–774.
28. [28] Cruz-Rico, G., Aviles-Salas, A., Segura-Gonzalez, M., Espinosa-Garcia, A.M., Ramirez-Tirado, L.A., Morales-Oyarvide, V., Rojas-Marin, C., Cardona, A.F., Arrieta, O., Diagnosis of EML4-ALK translocation with FISH, immunohistochemistry, and real-time polymerase chain reaction in patients with non-small cell lung cancer. Am. J. Clin. Oncol., 2015 [Epub ahead of print].
29. [29] Ying, J., Guo, L., Qiu, T., Shan, L., Ling, Y., Liu, X., Lu, N., Diagnostic value of a novel fully automated immunochemistry assay for detection of ALK rearrangement in primary lung adenocarcinoma. Ann. Oncol. 24 (2013), 2589–2593.
30. [30] Marchetti, A., Di Lorito, A., Pace, M.V., Iezzi, M., Felicioni, L., D'Antuono, T., Filice, G., Guetti, L., Mucilli, F., Buttitta, F., ALK protein analysis by IHC staining after recent regulatory changes: a comparison of two widely used approaches, revision of the literature, and a new testing algorithm. J. Thorac. Oncol. 11 (2016), 487–495.
31. [31] Conde, E., Suarez-Gauthier, A., Benito, A., Garrido, P., Garcia-Campelo, R., Biscuola, M., Paz-Ares, L., Hardisson, D., de Castro, J., Camacho, M.C., Rodriguez-Abreu, D., Abdulkader, I., Ramirez, J., Reguart, N., Salido, M., Pijuan, L., Arriola, E., Sanz, J., Folgueras, V., Villanueva, N., Gomez-Roman, J., Hidalgo, M., Lopez-Rios, F., Accurate identification of ALK positive lung carcinoma patients: novel FDA-cleared automated fluorescence in situ hybridization scanning system and ultrasensitive immunohistochemistry. PLoS One, 9, 2014, e107200.
32. [32] Savic, S., Diebold, J., Zimmermann, A.K., Jochum, W., Baschiera, B., Grieshaber, S., Tornillo, L., Bisig, B., Kerr, K., Bubendorf, L., Screening for ALK in non-small cell lung carcinomas: 5A4 and D5F3 antibodies perform equally well but combined use with FISH is recommended. Lung Cancer 89 (2015), 104–109.
33. [33] Lantuejoul, S., Rouquette, I., Blons, H., Le Stang, N., Ilie, M., Begueret, H., Gregoire, V., Hofman, P., Gros, A., Garcia, S., Monhoven, N., Devouassoux-Shisheboran, M., Mansuet-Lupo, A., Thivolet, F., Antoine, M., Vignaud, J.M., Penault-Llorca, F., Galateau-Salle, F., McLeer-Florin, A., French multicentric validation of ALK rearrangement diagnostic in 547 lung adenocarcinomas. Eur. Respir. J. 46 (2015), 207–218.
34. [34] Santelmo, C., Ravaioli, A., Barzotti, E., Papi, M., Poggi, B., Drudi, F., Mangianti, M., Salvi, M., Crino, L., Coexistence of EGFR mutation and ALK translocation in NSCLC: literature review and case report of response to gefitinib. Lung Cancer 81 (2013), 294–296.
35. [35] Chiari, R., Duranti, S., Ludovini, V., Bellezza, G., Pireddu, A., Minotti, V., Bennati, C., Crino, L., Long-term response to gefitinib and crizotinib in lung adenocarcinoma harboring both epidermal growth factor receptor mutation and EML4-ALK fusion gene. J. Clin. Oncol. 32 (2014), e30–e32.
36. [36] Cabillic, F., Gros, A., Dugay, F., Begueret, H., Mesturoux, L., Chiforeanu, D.C., Dufrenot, L., Jauffret, V., Dachary, D., Corre, R., Lespagnol, A., Soler, G., Dagher, J., Catros, V., Le Calve, M., Merlio, J.P., Belaud-Rotureau, M.A., Parallel FISH and immunohistochemical studies of ALK status in 3244 non-small-cell lung cancers reveal major discordances. J. Thorac. Oncol. 9 (2014), 295–306.
37. [37] Yang, J.J., Zhang, X.C., Su, J., Xu, C.R., Zhou, Q., Tian, H.X., Xie, Z., Chen, H.J., Huang, Y.S., Jiang, B.Y., Wang, Z., Wang, B.C., Yang, X.N., Zhong, W.Z., Nie, Q., Liao, R.Q., Mok, T.S., Wu, Y.L., Lung cancers with concomitant EGFR mutations and ALK rearrangements: diverse responses to EGFR-TKI and crizotinib in relation to diverse receptors phosphorylation. Clin. Cancer Res. 20 (2014), 1383–1392.
38. [38] Sholl, L.M., Sun, H., Butaney, M., Zhang, C., Lee, C., Janne, P.A., Rodig, S.J., ROS1 immunohistochemistry for detection of ROS1-rearranged lung adenocarcinomas. Am. J. Surg. Pathol. 37 (2013), 1441–1449.
39. [39] Cha, Y.J., Lee, J.S., Kim, H.R., Lim, S.M., Cho, B.C., Lee, C.Y., Shim, H.S., Screening of ROS1 rearrangements in lung adenocarcinoma by immunohistochemistry and comparison with ALK rearrangements. PLoS One, 9, 2014, e103333.
40. [40] Yoshida, A., Tsuta, K., Wakai, S., Arai, Y., Asamura, H., Shibata, T., Furuta, K., Kohno, T., Kushima, R., Immunohistochemical detection of ROS1 is useful for identifying ROS1 rearrangements in lung cancers. Mod. Pathol. 27 (2014), 711–720.
41. [41] Rogers, T.M., Russell, P.A., Wright, G., Wainer, Z., Pang, J.M., Henricksen, L.A., Singh, S., Stanislaw, S., Grille, J., Roberts, E., Solomon, B., Fox, S.B., Comparison of methods in the detection of ALK and ROS1 rearrangements in lung cancer. J. Thorac. Oncol. 10 (2015), 611–618.
42. [42] Warth, A., Muley, T., Dienemann, H., Goeppert, B., Stenzinger, A., Schnabel, P.A., Schirmacher, P., Penzel, R., Weichert, W., ROS1 expression and translocations in non-small-cell lung cancer: clinicopathological analysis of 1478 cases. Histopathology 65 (2014), 187–194.