Immunohistochemistry of pulmonary biomarkers a perspective from members of the pulmonary pathology society

Archives of Pathology and Laboratory Medicine

Volumn 142, Issue 3, 2018, Pages 408-419

  Thunnissen, Erik ^a   Allen, Timothy Craig ^b   Adam, Julien ^c   Aisner, Dara L ^d   Beasley, Mary Beth ^e   Borczuk, Alain C ^f   Cagle, Philip T ^g   Capelozzi, Vera Luiza ^h   Cooper, Wendy ⁱ   Hariri, Lida P ^j   Kern, Izidor ^k   Lantuejoul, Sylvie ^l   Miller, Ross ^g   Mino Kenudson, Mari ^j   Radonic, Teodora ^a   Raparia, Kirtee ^m   Rekhtman, Natasha ⁿ   Roy Chowdhuri, Sinchita ^o   Russell, Prudence ^c   Schneider, Frank ^p   Sholl, Lynette M ^q   Tsao, Ming Sound ^r   Vivero, Marina ^q   Yatabe, Yasushi ^s   more..

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b University of Texas Medical Branch School of Medicine   (United States)

^c Department of Pathology ^*  (Australia)

^d UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^e MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^f WEILL CORNELL MEDICAL CENTER   (United States)

^g HOUSTON METHODIST HOSPITAL   (United States)

^h UNIVERSITY OF SÃO PAULO   (Brazil)

ⁱ ROYAL PRINCE ALFRED HOSPITAL   (Australia)

^j MASSACHUSETTS GENERAL HOSPITAL   (United States)

^k UNIVERSITY CLINIC OF RESPIRATORY AND ALLERGIC DISEASES   (Slovenia)

^l INSERM   (France)

^m NORTHWESTERN UNIVERSITY   (United States)

ⁿ MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^o UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^p UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^q BRIGHAM AND WOMEN S HOSPITAL   (United States)

^r UNIVERSITY HEALTH NETWORK   (Canada)

^s AICHI CANCER CENTER HOSPITAL   (Japan)

more..

Author keywords

[No Author keywords available]

Indexed keywords

TUMOR MARKER;

HUMAN; IMMUNOHISTOCHEMISTRY; LUNG TUMOR; MEDICAL SOCIETY; PATHOLOGY; PROCEDURES; STANDARDS;

BIOMARKERS, TUMOR; HUMANS; IMMUNOHISTOCHEMISTRY; LUNG NEOPLASMS; PATHOLOGY, CLINICAL; SOCIETIES, MEDICAL;

EID: 85042635867     PISSN: 00039985     EISSN: 15432165     Source Type: Journal    
DOI: 10.5858/arpa.2017-0106-SA     Document Type: Review

References (129)

1. Dietel M, Bubendorf L, Dingemans A-MC, et al. Diagnostic procedures for non-small-cell lung cancer (NSCLC): recommendations of the European Expert Group. Thorax. 2016;71(2):177-184. doi:10.1136/thoraxjnl-2014-206677.
2. Travis WD, Brambilla E, Nicholson AG, et al. The 2015 World Health Organization Classification of Lung Tumors: impact of genetic, clinical and radiologic advances since the 2004 classification. J Thorac Oncol. 2015;10(9): 1243-1260. doi:10.1097/JTO.0000000000000630.
3. Tsao MS, Hirsch FR, Yatabe Y, eds. IASLC Atlas of ALK and ROS1 Testing in Lung Cancer. 2nd ed. North Forth Myers, FL: Editorial Rx Press; 2016.
4. Bubendorf L, Büttner R, Al-Dayel F, et al. Testing for ROS1 in non-small cell lung cancer: a review with recommendations. Virchows Arch. 2016;469(5):489-503. doi:10.1007/s00428-016-2000-3.
5. Zhou F, Moreira AL. Lung carcinoma predictive biomarker testing by immunoperoxidase stains in cytology and small biopsy specimens: advantages and limitations. Arch Pathol Lab Med. 2016;140(12):1331-1337. doi:10.5858/arpa.2016-0157-RA.
6. Savic S, Bode B, Diebold J, et al. Detection of ALK-positive non-small-cell lung cancers on cytological specimens: high accuracy of immunocytochemistry with the 5A4 clone. J Thorac Oncol. 2013;8(8):1004-1011. doi:10.1097/JTO.0b013e3182936ca9.
7. Bass BP, Engel KB, Greytak SR, Moore HM. A review of preanalytical factors affecting molecular, protein, and morphological analysis of formalinfixed, paraffin-embedded (FFPE) tissue: how well do you know your FFPE specimen? Arch Pathol Lab Med. 2014;138(11):1520-1530. doi:10.5858/arpa. 2013-0691-RA.
8. Pollard K, Lunny D, Holgate CS, Jackson P, Bird CC. Fixation, processing, and immunochemical reagent effects on preservation of T-lymphocyte surface membrane antigens in paraffin-embedded tissue. J Histochem Cytochem. 1987; 35(11):1329-1338.
9. Sauter JL, Grogg KL, Vrana JA, Law ME, Halvorson JL, Henry MR. Young investigator challenge: validation and optimization of immunohistochemistry protocols for use on cellient cell block specimens. Cancer Cytopathol. 2016; 124(2):89-100. doi:10.1002/cncy.21660.
10. Loftin I, Miller R, Thorne-Nuzzo P, et al. ALK IHC is highly sensitive to fixation parameters. J Thorac Oncol. 2017;12(S1):S265.
11. Kerr KM, Bubendorf L, Edelman MJ, et al. Second ESMO consensus conference on lung cancer: pathology and molecular biomarkers for non-smallcell lung cancer. Ann Oncol. 2014;25(9):1681-1690. doi:10.1093/annonc/mdu145.
12. Thunnissen E, Kerr KM, Herth FJ, et al. The challenge of NSCLC diagnosis and predictive analysis on small samples: practical approach of a working group. Lung Cancer. 2012;76(1):1-18. doi:10.1016/j.lungcan.2011.10.017.
13. Blind C, Koepenik A, Pacyna-Gengelbach M, et al. Antigenicity testing by immunohistochemistry after tissue oxidation. J Clin Pathol. 2008;61(1):79-83. doi:10.1136/jcp.2007.047340.
14. Schrijver WAME, van der Groep P, Hoefnagel LD, et al. Influence of decalcification procedures on immunohistochemistry and molecular pathology in breast cancer. Mod Pathol. 2016;29(12):1460-1470. doi:10.1038/modpathol. 2016.116.
15. Prinsen CFM, Klaassen CHW, Thunnissen FBJM. Microarray as a model for quantitative visualization chemistry. Appl Immunohistochem Mol Morphol. 2003;11(2):168-173.
16. Rüschoff J, Dietel M, Baretton G, et al. HER2 diagnostics in gastric cancerguideline validation and development of standardized immunohistochemical testing. Virchows Arch. 2010;457(3):299-307. doi:10.1007/s00428-010-0952-2.
17. Rüschoff J, Kerr K, Grote H, et al. The Reproducibility of immunohistochemical scoring for epidermal growth factor receptor expression in non-small cell lung cancer. Arch Pathol Lab Med. 2013;137(9):1255-1261.
18. Torlakovic EE, Francis G, Garratt J, et al. Standardization of negative controls in diagnostic immunohistochemistry: recommendations from the international ad hoc expert panel. Appl Immunohistochem Mol Morphol. 2014; 22(4):241-252. doi:10.1097/PAI.0000000000000069.
19. Torlakovic EE, Nielsen S, Francis G, et al. Standardization of positive controls in diagnostic immunohistochemistry: recommendations from the International Ad Hoc Expert Committee. Appl Immunohistochem Mol Morphol. 2015;23(1):1-18. doi:10.1097/PAI.0000000000000163.
20. Fitzgibbons PL, Bradley LA, Fatheree LA, et al. Principles of analytic validation of immunohistochemical assays: Guideline From the College of American Pathologists Pathology and Laboratory Quality Center. Arch Pathol Lab Med. 2014;138(11):1432-1443. doi:10.5858/arpa.2013-0610-CP.
21. Shaw AT, Kim D-W, Nakagawa K, et al. Crizotinib versus chemotherapy in advanced ALK-positive lung cancer. N Engl J Med. 2013;368(25):2385-2394. doi:10.1056/NEJMoa1214886.
22. Solomon BJ, Mok T, Kim D-W, et al. First-line crizotinib versus chemotherapy in ALK-positive lung cancer. N Engl J Med. 2014;371(23):2167-2177. doi:10.1056/NEJMoa1408440.
23. Conklin CMJ, Craddock KJ, Have C, Laskin J, Couture C, Ionescu DN. Immunohistochemistry is a reliable screening tool for identification of ALK rearrangement in non-small-cell lung carcinoma and is antibody dependent. J Thorac Oncol. 2013;8(1):45-51. doi:10.1097/JTO.0b013e318274a83e.
24. Blackhall FH, Peters S, Bubendorf L, et al. Prevalence and clinical outcomes for patients with ALK-positive resected stage I to III adenocarcinoma: results from the European Thoracic Oncology Platform Lungscape Project. J Clin Oncol. 2014;32(25):2780-2787. doi:10.1200/JCO.2013.54.5921.
25. Gruber K, Kohlhäufl M, Friedel G, Ott G, Kalla C. A novel, highly sensitive ALK antibody 1A4 facilitates effective screening for ALK rearrangements in lung adenocarcinomas by standard immunohistochemistry. J Thorac Oncol. 2015;10(4):713-716. doi:10.1097/JTO.0000000000000427.
26. Wang Q, Zhao L, Yang X, et al. Antibody 1A4 with routine immunohistochemistry demonstrates high sensitivity for ALK rearrangement screening of Chinese lung adenocarcinoma patients: a single-center large-scale study. Lung Cancer. 2016;95:39-43. doi:10.1016/j.lungcan.2016.02.014.
27. Savic S, Diebold J, Zimmermann A-K, et al. Screening for ALK in nonsmall cell lung carcinomas: 5A4 and D5F3 antibodies perform equally well, but combined use with FISH is recommended. Lung Cancer. 2015;89(2):104-109. doi:10.1016/j.lungcan.2015.05.012.
28. Ibrahim M, Parry S, Wilkinson D, et al. ALK Immunohistochemistry in NSCLC: discordant staining can impact patient treatment regimen. J Thorac Oncol. 2016;11(12):2241-2247. doi:10.1016/j.jtho.2016.07.012.
29. VENTANA ALK Scoring Interpretation Guide for Non-Small Cell Lung Carcinoma (NSCLC). http://www.uclad.com/newsletters/ALK-LUNG-IHCINTERPRETATION-GUIDE.pdf. Published 2013. Accessed March 26, 2017.
30. Rodig SJ, Mino-Kenudson M, Dacic S, et al. Unique clinicopathologic features characterize ALK-rearranged lung adenocarcinoma in the western population. Clin Cancer Res. 2009;15(16):5216-5223. doi:10.1158/1078-0432. CCR-09-0802.
31. Yoshida A, Tsuta K, Watanabe S, et al. Frequent ALK rearrangement and TTF-1/p63 co-expression in lung adenocarcinoma with signet-ring cell component. Lung Cancer. 2011;72(3):309-315. doi:10.1016/j.lungcan.2010.09.013.
32. Popat S, Gonzalez D, Min T, et al. ALK translocation is associated with ALK immunoreactivity and extensive signet-ring morphology in primary lung adenocarcinoma. Lung Cancer. 2012;75(3):300-305. doi:10.1016/j.lungcan. 2011.07.017.
33. Murakami Y, Mitsudomi T, Yatabe Y. A screening method for the ALK fusion gene in NSCLC. Front Oncol. 2012;2(March):24. doi:10.3389/fonc.2012. 00024.
34. Nakamura H, Tsuta K, Yoshida A, et al. Aberrant anaplastic lymphoma kinase expression in high-grade pulmonary neuroendocrine carcinoma. J Clin Pathol. 2013;66(8):705-707. doi:10.1136/jclinpath-2012-201329.
35. Takeuchi K, Choi YL, Togashi Y, et al. KIF5B-ALK, a novel fusion oncokinase identified by an immunohistochemistry-based diagnostic system for ALK-positive lung cancer. Clin Cancer Res. 2009;15(9):3143-3149. doi:10.1158/1078-0432.CCR-08-3248.
36. Mino-Kenudson M, Chirieac LR, Law K, et al. A novel, highly sensitive antibody allows for the routine detection of ALK-rearranged lung adenocarcinomas by standard immunohistochemistry. Clin Cancer Res. 2010;16(5):1561-1571. doi:10.1158/1078-0432.CCR-09-2845.
37. Martinez P, Hernández-Losa J, Montero MA, et al. Fluorescence in situ hybridization and immunohistochemistry as diagnostic methods for ALK positive non-small cell lung cancer patients. PLoS One. 2013;8(1):e52261. doi:10.1371/journal.pone.0052261.
38. Minca EC, Portier BP, Wang Z, et al. ALK status testing in non-small cell lung carcinoma: correlation between ultrasensitive IHC and FISH. J Mol Diagn. 2013;15(3):341-346. doi:10.1016/j.jmoldx.2013.01.004.
39. Ying J, Guo L, Qiu T, et al. Diagnostic value of a novel fully automated immunochemistry assay for detection of ALK rearrangement in primary lung adenocarcinoma. Ann Oncol. 2013;24(10):2589-2593. doi:10.1093/annonc/mdt295.
40. Wu Y-C, Chang I-C, Wang C-L, et al. Comparison of IHC, FISH and RTPCR methods for detection of ALK rearrangements in 312 non-small cell lung cancer patients in Taiwan. PLoS One. 2013;8(8):e70839. doi:10.1371/journal. pone.0070839.
41. Tantraworasin A, Lertprasertsuke N, Kongkarnka S, Euathrongchit J, Wannasopha Y, Saeteng S. Retrospective study of ALK rearrangement and clinicopathological implications in completely resected non- small cell lung cancer patients in Northern Thailand: role of screening with D5F3 antibodies. Asian Pac J Cancer Prev. 2014;15(7):3057-3063.
42. Wang J, Cai Y, Dong Y, et al. Clinical characteristics and outcomes of patients with primary lung adenocarcinoma harboring ALK rearrangements detected by FISH, IHC, and RT-PCR. PLoS One. 2014;9(7):e101551. doi:10.1371/journal.pone.0101551.
43. Zhou J, Zhao J, Sun K, et al. Accurate and economical detection of ALK positive lung adenocarcinoma with semiquantitative immunohistochemical screening. PLoS One. 2014;9(3):e92828. doi:10.1371/journal.pone.0092828.
44. Shan L, Lian F, Guo L, Yang X, Ying J, Lin D. Combination of conventional immunohistochemistry and qRT-PCR to detect ALK rearrangement. Diagn Pathol. 2014;9(1):3. doi:10.1186/1746-1596-9-3.
45. Alì G, Proietti A, Pelliccioni S, et al. ALK rearrangement in a large series of consecutive non-small cell lung cancers: comparison between a new immunohistochemical approach and fluorescence in situ hybridization for the screening of patients eligible for crizotinib treatment. Arch Pathol Lab Med. 2014;138(11): 1449-1458. doi:10.5858/arpa.2013-0388-OA.
46. Ilie MI, Bence C, Hofman V, et al. Discrepancies between FISH and immunohistochemistry for assessment of the ALK status are associated with ALK "borderline"-positive rearrangements or a high copy number: a potential major issue for anti-ALK therapeutic strategies. Ann Oncol. 2015;26(1):238-244. doi: 10.1093/annonc/mdu484.
47. Wynes MW, Sholl LM, Dietel M, et al. An international interpretation study using the ALK IHC antibody D5F3 and a sensitive detection kit demonstrates high concordance between ALK IHC and ALK FISH and between evaluators. J Thorac Oncol. 2014;9(5):631-638. doi:10.1097/JTO.0000000000000115.
48. Paik JH, Choe G, Kim H, et al. 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. doi:10.1097/JTO.0b013e31820b82e8.
49. Jokoji R, Yamasaki T, Minami S, et al. Combination of morphological feature analysis and immunohistochemistry is useful for screening of EML4-ALKpositive lung adenocarcinoma. J Clin Pathol. 2010;63(12):1066-1070. doi:10. 1136/jcp.2010.081166.
50. Kim H, Yoo S-B, Choe J-Y, et al. Detection of ALK gene rearrangement in non-small cell lung cancer: a comparison of fluorescence in situ hybridization and chromogenic in situ hybridization with correlation of ALK protein expression. J Thorac Oncol. 2011;6(8):1359-1366. doi:10.1097/JTO.0b013e31821cfc73.
51. McLeer-Florin A, Moro-Sibilot D, Melis A, et al. Dual IHC and FISH testing for ALK gene rearrangement in lung adenocarcinomas in a routine practice: a French study. J Thorac Oncol. 2012;7(2):348-354. doi:10.1097/JTO.0b013e3182381535.
52. Lopes L, Bacchi C. Anaplastic lymphoma kinase gene rearrangement in non-small-cell lung cancer in a Brazilian population. Clinics. 2012;67(7):845-847. doi:10.6061/clinics/2012(07)23.
53. Park HS, Lee JK, Kim D-W, et al. Immunohistochemical screening for anaplastic lymphoma kinase (ALK) rearrangement in advanced non-small cell lung cancer patients. Lung Cancer. 2012;77(2):288-292. doi:10.1016/j.lungcan. 2012.03.004.
54. Sholl LM, Weremowicz S, Gray SW, et al. Combined use of ALK immunohistochemistry and FISH for optimal detection of ALK-rearranged lung adenocarcinomas. J Thorac Oncol. 2013;8(3):322-328. doi:10.1097/JTO.0b013e31827db604.
55. To K-F, Tong JH, Yeung KS, et al. Detection of ALK rearrangement by immunohistochemistry in lung adenocarcinoma and the identification of a novel EML4-ALK variant. J Thorac Oncol. 2013;8:883-891. doi:10.1097/JTO.0b013e3182904e22.
56. Cabillic F, Gros A, Dugay F, et al. Parallel FISH and immunohistochemical studies of ALK status in 3244 non-small-cell lung cancers reveal major discordances. J Thorac Oncol. 2014;9(3):295-306. doi:10.1097/JTO.0000000000000072.
57. Jiang L, Yang H, He P, et al. Improving selection criteria for ALK inhibitor therapy in non-small cell lung cancer: a pooled-data analysis on diagnostic operating characteristics of immunohistochemistry. Am J Surg Pathol. 2016;40(5): 697-703. doi:10.1097/PAS.0000000000000604.
58. Conde E, Suárez-Gauthier A, Benito A, et al. Accurate identification of ALK positive lung carcinoma patients: novel FDA-cleared automated fluorescence in situ hybridization scanning system and ultrasensitive immunohistochemistry. PLoS One. 2014;9(9):e107200. doi:10.1371/journal.pone.0107200.
59. Marchetti A, Di Lorito A, Pace MV, et al. 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. 2016;11(4):487-495. doi:10.1016/j.jtho.2015.12.111.
60. Zwaenepoel K, Van Dongen A, Lambin S, Weyn C, Pauwels P. Detection of ALK expression in non-small-cell lung cancer with ALK gene rearrangements-comparison of multiple immunohistochemical methods. Histopathology. 2014; 65(4):539-548. doi:10.1111/his.12414.
61. Lantuejoul S, Rouquette I, Blons H, et al. French multicentric validation of ALK rearrangement diagnostic in 547 lung adenocarcinomas. Eur Respir J. 2015; 46(1):207-218. doi:10.1183/09031936.00119914.
62. Jurmeister P, Lenze D, Berg E, et al. Parallel screening for ALK, MET and ROS1 alterations in non-small cell lung cancer with implications for daily routine testing. Lung Cancer. 2015;87(2):122-129. doi:10.1016/j.lungcan.2014.11.018.
63. Gao X, Sholl LM, Nishino M, Heng JC, Jänne PA, Oxnard GR. Clinical implications of variant ALK FISH rearrangement patterns. J Thorac Oncol. 2015; 10(11):1648-1652. doi:10.1097/JTO.0000000000000665.
64. Pekar-Zlotin M, Hirsch FR, Soussan-Gutman L, et al. Fluorescence in situ hybridization, immunohistochemistry, and next-generation sequencing for detection of EML4-ALK rearrangement in lung cancer. Oncologist. 2015;20(3): 316-322. doi:10.1634/theoncologist.2014-0389.
65. von Laffert M, Stenzinger A, Hummel M, et al. ALK-FISH borderline cases in non-small cell lung cancer: implications for diagnostics and clinical decision making. Lung Cancer. 2015;90:465-471. doi:10.1016/j.lungcan.2015.09.022.
66. Selinger CI, Rogers T-M, Russell PA, et al. Testing for ALK rearrangement in lung adenocarcinoma: a multicenter comparison of immunohistochemistry and fluorescent in situ hybridization. Mod Pathol. 2013;26(12):1545-1553. doi: 10.1038/modpathol.2013.87.
67. Kim H, Xu X, Yoo S-B, et al. Discordance between anaplastic lymphoma kinase status in primary non-small-cell lung cancers and their corresponding metastases. Histopathology. 2013;62(2):305-314. doi:10.1111/j.1365-2559. 2012.04356.x.
68. Salido M, Pijuan L, Martínez-Avil és L, et al. Increased ALK gene copy number and amplification are frequent in non-small cell lung cancer. J Thorac Oncol. 2011;6(1):21-27. doi:10.1097/JTO.0b013e3181fb7cd6.
69. Wiesner T, Lee W, Obenauf AC, et al. Alternative transcription initiation leads to expression of a novel ALK isoform in cancer. Nature. 2015;526(7573): 453-457. doi:10.1038/nature15258.
70. Rosoux A, Pauwels P, Duplaquet F, et al. Effectiveness of crizotinib in a patient with ALK IHC-positive/FISH-negative metastatic lung adenocarcinoma. Lung Cancer. 2016;98:118-121. doi:10.1016/j.lungcan.2016.06.001.
71. Bergethon K, Shaw AT, Ou S-HI, et al. ROS1 rearrangements define a unique molecular class of lung cancers. J Clin Oncol. 2012;30(8):863-870. doi: 10.1200/JCO.2011.35.6345.
72. Li S, Choi Y-L, Gong Z, et al. Comprehensive characterization of oncogenic drivers in Asian lung adenocarcinoma. J Thorac Oncol. 2016;11(12): 2129-2140. doi:10.1016/j.jtho.2016.08.142.
73. Govindan R, Ding L, Griffith M, et al. Genomic landscape of non-small cell lung cancer in smokers and never-smokers. Cell. 2013;150(6):1121-1134. doi:10.1016/j.cell.2012.08.024.GENOMIC.
74. Rimkunas VM, Crosby KE, Li D, et al. Analysis of receptor tyrosine kinase ROS1-positive tumors in non-small cell lung cancer: identification of a FIG-ROS1 fusion. Clin Cancer Res. 2012;18(16):4449-4457. doi:10.1158/1078-0432.CCR-11-3351.
75. Seo J-S, Ju YS, Lee W-C, et al. The transcriptional landscape and mutational profile of lung adenocarcinoma. Genome Res. 2012;22(11):2109-2119.
76. Takeuchi K, Soda M, Togashi Y, et al. RET, ROS1 and ALK fusions in lung cancer. Nat Med. 2012;18(3):378-381. doi:10.1038/nm.2658.
77. Yoshida A, Kohno T, Tsuta K, et al. ROS1-rearranged lung cancer: a clinicopathologic and molecular study of 15 surgical cases. Am J Surg Pathol. 2013;37(4):554-562.
78. FDA expands use of Xalkori to treat rare form of advanced non-small cell lung cancer. www.fda.gov/newsevents/newsroom/pressannouncements/ucm490329.htm. Accessed March 26, 2017.
79. Boyle TA, Masago K, Ellison KE, Yatabe Y, Hirsch FR. ROS1 immunohistochemistry among major genotypes of non-small-cell lung cancer. Clin Lung Cancer. 2015;16(2):106-111. doi:10.1016/j.cllc.2014.10.003.
80. Yoshida A, Tsuta K, Wakai S, et al. Immunohistochemical detection of ROS1 is useful for identifying ROS1 rearrangements in lung cancers. Mod Pathol. 2014;27(5):711-720. doi:10.1038/modpathol.2013.192.
81. Sholl LM, Sun H, Butaney M, et al. ROS1 immunohistochemistry for detection of lung adenocarcinomas. Am J Surg Pathol. 2013;37(9):1441-1449.
82. Mescam-Mancini L, Lantuéjoul S, Moro-Sibilot D, et al. On the relevance of a testing algorithm for the detection of ROS1-rearranged lung adenocarcinomas. Lung Cancer. 2014;83(2):168-173. doi:10.1016/j.lungcan.2013.11.019.
83. Sholl LM, Aisner DL, Allen TC, et al. Programmed death ligand 1 immunohistochemistry- A new challenge for pathologists: a perspective from members of the Pulmonary Pathology Society. Arch Pathol Lab Med. 2016;140(4): 341-344. doi:10.5858/arpa.2015-0506-SA.
84. Weber JS, Kudchadkar RR, Yu B, et al. Safety, efficacy, and biomarkers of nivolumab with vaccine in ipilimumab-refractory or -naive melanoma. J Clin Oncol. 2013;31(34):4311-4318. doi:10.1200/JCO.2013.51.4802.
85. Tumeh PC, Harview CL, Yearley JH, et al. PD-1 blockade induces responses by inhibiting adaptive immune resistance. Nature. 2014;515(7528): 568-571. doi:10.1038/nature13954.
86. Planchard D, Yokoi T, McCleod MJ, et al. A phase III study of durvalumab (MEDI4736) with or without tremelimumab for previously treated patients with advanced NSCLC: rationale and protocol design of the ARCTIC study. Clin Lung Cancer. 2016;17(3):232-236.e1. doi:10.1016/j.cllc.2016.03.003.
87. Kaufman HL, Russell J, Hamid O, et al. Avelumab in patients with chemotherapy-refractory metastatic Merkel cell carcinoma: a multicentre, singlegroup, open-label, phase 2 trial. Lancet Oncol. 2016;17(10):1374-1385. doi:10. 1016/S1470-2045(16)30364-3.
88. Gaule P, Smithy JW, Toki M, et al. A quantitative comparison of antibodies to programmed cell death 1 ligand 1. JAMA Oncol. 2017;3(2):256. doi:10.1001/jamaoncol.2016.3015.
89. McLaughlin J, Han G, Schalper KA, et al. Quantitative assessment of the heterogeneity of PD-L1 expression in non-small-cell lung cancer. JAMA Oncol. 2016;2(1):46-54. doi:10.1001/jamaoncol.2015.3638.
90. Cree IA, Booton R, Cane P, et al. PD-L1 testing for lung cancer in the UK: recognizing the challenges for implementation. Histopathology. 2016;69(2):177-186. doi:10.1111/his.12996.
91. Midha A. PD-L1 expression in advanced NSCLC: primary lesions versus metastatic sites and impact of sample age. Poster presented at: ASCO Chicago, IL; June 5, 2016. J Clin Oncol. 2016;34(suppl):abstract 3025.
92. Yu H, Boyle TA, Zhou C, Rimm DL, Hirsch FR. PD-L1 expression in lung cancer. J Thorac Oncol. 2016;11(7):964-975. doi:10.1016/j.jtho.2016.04.014.
93. Velcheti V, Schalper KA, Carvajal DE, et al. Programmed death ligand-1 expression in non-small cell lung cancer. Lab Invest. 2013;94(1):107-116. doi: 10.1038/labinvest.2013.130.
94. Patel SP, Kurzrock R. PD-L1 expression as a predictive biomarker in cancer immunotherapy. Mol Cancer Ther. 2015;14(4):847-856. doi:10.1158/1535-7163.MCT-14-0983.
95. Sznol M, Chen L. Antagonist antibodies to PD-1 and B7-H1 (PD-L1) in the treatment of advanced human cancer. Clin Cancer Res. 2013;19(5):1021-1034. doi:10.1158/1078-0432.CCR-12-2063.
96. Kitazono S, Fujiwara Y, Tsuta K, et al. Reliability of small biopsy samples compared with resected specimens for the determination of programmed deathligand 1 expression in non-small-cell lung cancer. Clin Lung Cancer. 2015;16(5): 385-390. doi:10.1016/j.cllc.2015.03.008.
97. Ilie M, Long-Mira E, Bence C, et al. Comparative study of the PD-L1 status between surgically resected specimens and matched biopsies of NSCLC patients reveal major discordances: a potential issue for anti-PD-L1 therapeutic strategies. Ann Oncol. 2016;27(1):147-153. doi:10.1093/annonc/mdv489.
98. Borghaei H, Paz-Ares L, Horn L, et al. Nivolumab versus docetaxel in advanced nonsquamous non-small-cell lung cancer. N Engl J Med. 2015;373(17): 1627-1639. doi:10.1056/NEJMoa1507643.
99. Rittmeyer A, Barlesi F, Waterkamp D, et al. Atezolizumab versus docetaxel in patients with previously treated non-small-cell lung cancer (OAK): a phase 3, open-label, multicentre randomised controlled trial. Lancet. 2017; 389(10066):255-265. doi:10.1016/S0140-6736(16)32517-X.
100. Fischer AH, Schwartz MR, Moriarty AT, et al. Immunohistochemistry practices of cytopathology laboratories: a survey of participants in the College of American Pathologists Nongynecologic Cytopathology Education Program. Arch Pathol Lab Med. 2014;138(9):1167-1172. doi:10.5858/arpa.2013-0259-CP.
101. Skov BG, Skov T. Paired comparison of PD-L1 expression on cytologic and histologic specimens from malignancies in the lung assessed with PD-L1 IHC 28-8pharmDx and PD-L1 IHC 22C3pharmDx [published online ahead of print May 25, 2017]. Appl Immunohistochem Mol Morphol. doi:10.1097/PAI. 0000000000000540.
102. van Krieken JH, Normanno N, Blackhall F, et al. Guideline on the requirements of external quality assessment programs in molecular pathology. Virchows Arch. 2013;462(1):27-37. doi:10.1007/s00428-012-1354-4.
103. Hirsch FR, McElhinny A, Stanforth D, et al. PD-L1 Immunohistochemistry assays for lung cancer: results from phase 1 of the Blueprint PD-L1 IHC Assay Comparison Project. J Thorac Oncol. 2017;12(2):208-222. doi:10.1016/j.jtho. 2016.11.2228.
104. Scheel AH, Dietel M, Heukamp LC, et al. Harmonized PD-L1 immunohistochemistry for pulmonary squamous-cell and adenocarcinomas. Mod Pathol. 2016;29(10):1-8. doi:10.1038/modpathol.2016.117.
105. Cooper WA, Russell PA, Huot-Marhand P, et al. Intra- and interobserver reproducibility study of PD-L1 biomarker in NSCLC: The Dream Study. J Thorac Oncol. 2017;12(s1):424.
106. Rehman JA, Han G, Carvajal-Hausdorf DE, et al. Quantitative and pathologist-read comparison of the heterogeneity of programmed death-ligand 1 (PD-L1) expression in non-small cell lung cancer. Mod Pathol. 2017;30(3):340-349. doi:10.1038/modpathol.2016.186.
107. Ratcliffe MJ, Sharpe A, Midha A, et al. Agreement between programmed cell death ligand-1 diagnostic assays across multiple protein expression cut-offs in non-small cell lung cancer [published online ahead of print January 10, 2017]. Clin Cancer Res. doi:10.1158/1078-0432.CCR-16-2375.
108. Adam J, Rouquette I, Damotte D, et al. Multicentric French Harmonization study for PD-L1 testing in NSCLC. J Thorac Oncol. 2017;12(S1):S4-S5.
109. Li M. Statistical methods for clinical validation of follow-on companion diagnostic devices via an external concordance study. Stat Biopharm Res. 2016; 8(3):355-363. doi:10.1080/19466315.2016.1202859.
110. Brevet M, Arcila M, Ladanyi M. Assessment of EGFR mutation status in lung adenocarcinoma by immunohistochemistry using antibodies specific to the two major forms of mutant EGFR. J Mol Diagn. 2010;12(2):169-176. doi:10. 2353/jmoldx.2010.090140.
111. Yu J, Kane S, Wu J, et al. Mutation-specific antibodies for the detection of EGFR mutations in non-small-cell lung cancer. Clin Cancer Res. 2009;15(9): 3023-3028. doi:10.1158/1078-0432.CCR-08-2739.
112. Simonetti S, Molina MA, Queralt C, et al. Detection of EGFR mutations with mutation-specific antibodies in stage IV non-small-cell lung cancer. J Transl Med. 2010;8:135. doi:10.1186/1479-5876-8-135.
113. Kawahara A, Yamamoto C, Nakashima K, et al. Molecular diagnosis of activating EGFR mutations in non-small cell lung cancer using mutation-specific antibodies for immunohistochemical analysis. Clin Cancer Res. 2010;16(12): 3163-3170. doi:10.1158/1078-0432.CCR-09-3239.
114. 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. 2010;16(13):3349-3355. doi:10.1158/1078-0432.CCR-10-0129.
115. Jiang G, Fan C, Zhang X, et al. Ascertaining an appropriate diagnostic algorithm using EGFR mutation-specific antibodies to detect EGFR status in nonsmall-cell lung cancer. PLoS One. 2013;8(3):e59183. doi:10.1371/journal.pone. 0059183.
116. Sasaki H, Shimizu S, Tani Y, et al. Usefulness of immunohistochemistry for the detection of the BRAF V600E mutation in Japanese lung adenocarcinoma. Lung Cancer. 2013;82(1):51-54. doi:10.1016/j.lungcan.2013.06.014.
117. Ilie M, Long E, Hofman V, et al. Diagnostic value of immunohistochemistry for the detection of the BRAFV600E mutation in primary lung adenocarcinoma Caucasian patients. Ann Oncol. 2013;24(3):742-748. doi:10.1093/annonc/mds534.
118. Cardarella S, Ogino A, Nishino M, et al. Clinical, pathologic, and biologic features associated with BRAF mutations in non-small cell lung cancer. Clin Cancer Res. 2013;19(16):4532-4540. doi:10.1158/1078-0432.CCR-13-0657.
119. Davies H, Bignell GR, Cox C, et al. Mutations of the BRAF gene in human cancer. Nature. 2002;417(6892):949-954. doi:10.1038/nature00766.
120. Marchetti A, Felicioni L, Malatesta S, et al. Clinical features and outcome of patients with non-small-cell lung cancer harboring BRAF mutations. J Clin Oncol. 2011;29(26):3574-3579. doi:10.1200/JCO.2011.35.9638.
121. Paik PK, Arcila ME, Fara M, et al. Clinical characteristics of patients with lung adenocarcinomas harboring BRAF mutations. J Clin Oncol. 2011;29(15): 2046-2051. doi:10.1200/JCO.2010.33.1280.
122. Rogers T-M, Russell PA, Wright G, et al. Comparison of methods in the detection of ALK and ROS1 rearrangements in lung cancer. J Thorac Oncol. 2015;10(4):611-618. doi:10.1097/JTO.0000000000000465.
123. Shan L, Lian F, Guo L, et al. Detection of ROS1 gene rearrangement in lung adenocarcinoma: comparison of IHC, FISH and real-time RT-PCR. PLoS One. 2015;10(3):e0120422. doi:10.1371/journal.pone.0120422.
124. Wu J, Lin Y, He X, et al. Comparison of detection methods and follow-up study on the tyrosine kinase inhibitors therapy in non-small cell lung cancer patients with ROS1 fusion rearrangement. BMC Cancer. 2016;16(1):599. doi:10. 1186/s12885-016-2582-9.
125. Cao B, Wei P, Liu Z, et al. Detection of lung adenocarcinoma with ROS1 rearrangement by IHC, FISH, and RT-PCR and analysis of its clinicopathologic features. Onco Targets Ther. 2015;9:131. doi:10.2147/OTT.S94997.
126. Selinger CI, Li BT, Pavlakis N, et al. Screening for ROS1 gene rearrangements in non-small-cell lung cancers using immunohistochemistry with FISH confirmation is an effective method to identify this rare target. Histopathology. 2017;70(3):402-411. doi:10.1111/his.13076.
127. Kao H-L, Yeh Y-C, Lin C-H, et al. 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. 2016;101:40-47. doi:10.1016/j.lungcan. 2016.09.007.
128. Wiesweg M, Eberhardt WEEE, Reis H, et al. High prevalence of concomitant oncogene mutations in prospectively identified patients with ROS1-positive metastatic lung cancer. J Thorac Oncol. 2017;12(1):54-64. doi: 10.1016/j.jtho.2016.08.137.
129. Scheel AH, Dietel M, Heukamp LC, et al. Predictive PD-L1 immunohistochemistry for non-small cell lung cancer : Current state of the art and experiences of the first German harmonization study. Pathologe. 2016;37(6):557-567.