Cribriform adenocarcinoma of the lung: Clinicopathologic, immunohistochemical, and molecular analysis of 15 cases of a distinctive morphologic subtype of lung adenocarcinoma

Modern Pathology

Volumn 27, Issue 8, 2014, Pages 1063-1072

  Mackinnon, Alexander C ^a   Luevano, Arturo ^a,b   De Araujo, Lisley C ^a,c   Rao, Nagarjun ^a   Le, Min ^a   Suster, Saul ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

^b Christus Mugerza Del Parque Hospital   (Mexico)

^c HOSPITAL UNIVERSITÁRIO DE BRASÍLIA   (Brazil)

Author keywords

ALK1; cribriform adenocarcinoma; KRAS; lung adenocarcinoma; metastases to the lungs; molecular diagnostics; ROS1

Indexed keywords

ACTIVIN RECEPTOR LIKE KINASE 1; EPIDERMAL GROWTH FACTOR RECEPTOR; PROTEIN RET; ACTIVIN RECEPTOR 2; ACVRL1 PROTEIN, HUMAN; EGFR PROTEIN, HUMAN; KRAS PROTEIN, HUMAN; ONCOPROTEIN; PROTEIN TYROSINE KINASE; RAS PROTEIN; ROS1 PROTEIN, HUMAN; TUMOR MARKER; C ROS ONCOGENE 1 RECEPTOR TYROSINE KINASE 1; UNCLASSIFIED DRUG;

ADULT; AGED; ARTICLE; BREAST; CANCER GROWTH; CANCER SURGERY; CHROMATIN; CLINICAL ARTICLE; CLINICAL FEATURE; COLON; COLORECTAL CARCINOMA; CYSTADENOCARCINOMA; CYTOARCHITECTURE; DIFFERENTIAL DIAGNOSIS; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; GENE; GENE FREQUENCY; GENE MUTATION; GENE REARRANGEMENT; GENE SEQUENCE; GOBLET CELL; GROWTH CURVE; HETEROZYGOTE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOHISTOLOGY; INTESTINE NECROSIS; LIVER BIOPSY; LUNG ADENOCARCINOMA; LUNG METASTASIS; LYMPH NODE METASTASIS; MALE; MEDIASTINUM LYMPH NODE; MIDDLE AGED; MOLECULAR BIOLOGY; OVARY; PANCREAS; PHENOTYPE; PRIORITY JOURNAL; PROSTATE; PSAMMOMA BODY; RETROSPECTIVE STUDY; ROS1 GENE; SMOKING; THYROID GLAND; TUMOR CELL; TUMOR LOCALIZATION; TUMOR VOLUME; UTERUS; VERY ELDERLY; ADENOCARCINOMA; CHEMISTRY; CLASSIFICATION; GENETIC PREDISPOSITION; GENETICS; LUNG NEOPLASMS; MUTATION; NUCLEOTIDE SEQUENCE; PATHOLOGY; PREDICTIVE VALUE; BREAST CANCER; CANCER MORPHOLOGY; COLON CANCER; HISTOLOGY; LUNG CANCER; MEDICAL HISTORY; METASTASIS; MOLECULAR DYNAMICS; OVARY CANCER; PANCREAS CANCER; PROSTATE CANCER; THYROID CANCER; UTERUS CANCER;

ACTIVIN RECEPTORS, TYPE II; ADENOCARCINOMA; ADULT; AGED; AGED, 80 AND OVER; DIAGNOSIS, DIFFERENTIAL; DNA MUTATIONAL ANALYSIS; FEMALE; GENE REARRANGEMENT; GENETIC PREDISPOSITION TO DISEASE; HUMANS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION, FLUORESCENCE; LUNG NEOPLASMS; MALE; MIDDLE AGED; MUTATION; PHENOTYPE; PREDICTIVE VALUE OF TESTS; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS; RAS PROTEINS; RECEPTOR, EPIDERMAL GROWTH FACTOR; RETROSPECTIVE STUDIES; TUMOR MARKERS, BIOLOGICAL;

EID: 84905442619     PISSN: 08933952     EISSN: 15300285     Source Type: Journal    
DOI: 10.1038/modpathol.2013.227     Document Type: Article

References (47)

1. Cetin K, Ettinger DS, Hei YJ, et al. Survival by histologic subtype in stage IV nonsmall cell lung cancer based on data from the Surveillance, Epidemiology and End Results Program. Clin Epidemiol 2011;3:139-148.
2. Chilosi M, Murer B. Mixed adenocarcinomas of the lung: place in new proposals in classification, mandatory for target therapy. Arch Pathol Lab Med 2010;134: 55-65.
3. Travis WD, Brambilla E, Muller-Hermelink HK, et al. Pathology and Genetics of Tumours of the Lung, Pleura, Thymus, and Heart. IARC Press: France: Lyon 2004, pp 344.
4. Cooper WA, O'Toole S, Boyer M, et al. What's new in non-small cell lung cancer for pathologists: the importance of accurate subtyping, EGFR mutations and ALK rearrangements. Pathology 2011;43:103-115.
5. Kerr KM. Pulmonary adenocarcinomas: classification and reporting. Histopathology 2009;54:12-27.
6. Motoi N, Szoke J, Riely GJ, et al. Lung adenocarcinoma: modification of the 2004 WHO mixed subtype to include the major histologic subtype suggests correlations between papillary and micropapillary adenocarcinoma subtypes, EGFR mutations and gene expression analysis. Am J Surg Pathol 2008;32:810-827.
7. Travis WD, Brambilla E, Noguchi M, 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;6:244-285.
8. Russell PA, Wainer Z, Wright GM, et al. Does lung adenocarcinoma subtype predict patient survival?: A clinicopathologic study based on the new International Association for the Study of Lung Cancer/American Thoracic Society/European Respiratory Society international multidisciplinary lung adenocarcinoma classification. J Thorac Oncol 2011;6:1496-1504.
9. Yoshizawa A, Motoi N, Riely GJ, et al. Impact of proposed IASLC/ATS/ERS classification of lung adenocarcinoma: prognostic subgroups and implications for further revision of staging based on analysis of 514 stage I cases. Mod Pathol 2011;24:653-664.
10. Copeland JN, Amin MB, Humphrey PA, et al. The morphologic spectrum of metastatic prostatic adenocarcinoma to the lung: special emphasis on histologic features overlapping with other pulmonary neoplasms. Am J Clin Pathol 2002;117:552-557.
11. Herbst J, Jenders R, McKenna R, et al. Evidence-based criteria to help distinguish metastatic breast cancer from primary lung adenocarcinoma on thoracic frozen section. Am J Clin Pathol 2009;131:122-128.
12. Takeuchi K, Soda M, Togashi Y, et al. RET, ROS1 and ALK fusions in lung cancer. Nat Med 2012;18:378-381.
13. Keedy VL, Temin S, Somerfield MR, et al. American Society of Clinical Oncology provisional clinical opinion: epidermal growth factor receptor (EGFR) Mutation testing for patients with advanced nonsmall- cell lung cancer considering first-line EGFR tyrosine kinase inhibitor therapy. J Clin Oncol 2011;29: 2121-2127.
14. Mino-Kenudson M, Mark EJ. Reflex testing for epidermal growth factor receptor mutation and anaplastic lymphoma kinase fluorescence in situ hybridization in non-small cell lung cancer. Arch Pathol Lab Med 2011;135:655-664.
15. Pirker R, Herth FJ, Kerr KM, et al. Consensus for EGFR mutation testing in non-small cell lung cancer: results from a European workshop. J Thorac Oncol 2010;5: 1706-1713.
16. Lindeman NI, Cagle PT, Beasley MB, et al. 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. Arch Pathol Lab Med 2013;137:828-860.
17. Rikova K, Guo A, Zeng Q, et al. Global survey of phosphotyrosine signaling identifies oncogenic kinases in lung cancer. Cell 2007;131:1190-1203.
18. Ju YS, Lee WC, Shin JY, et al. A transforming KIF5B and RET gene fusion in lung adenocarcinoma revealed from whole-genome and transcriptome sequencing. Genome Res 2012;22:436-445.
19. Kohno T, Ichikawa H, Totoki Y, et al. KIF5B-RET fusions in lung adenocarcinoma. Nat Med 2012;18:375-377.
20. Lipson D, Capelletti M, Yelensky R, et al. Identification of new ALK and RET gene fusions from colorectal and lung cancer biopsies. Nat Med 2012;18:382-384.
21. Oxnard GR, Binder A, Janne PA. New targetable oncogenes in non-small-cell lung cancer. J Clinical Oncol 2013;31:1097-1104.
22. Drilon A, Wang L, Hasanovic A, et al. Response to Cabozantinib in patients with RET fusion-positive lung adenocarcinomas. Cancer Discov 2013;3:630-635.
23. Lindeman NI, Cagle PT, Beasley MB, et al. 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 Diag 2013;15:415-453.
24. Kakegawa S, Shimizu K, Sugano M, et al. Clinicopathological features of lung adenocarcinoma with KRAS mutations. Cancer 2011;117:4257-4266.
25. 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;37:554-562.
26. Yeh YC, Chou TY. Pulmonary adenocarcinoma with microcystic histology and intratumoral heterogeneity of EGFR gene polymorphism. Histopathology 2010;57: 112-120.
27. Sica G, Yoshizawa A, Sima CS, et al. A grading system of lung adenocarcinomas based on histologic pattern is predictive of disease recurrence in stage I tumors. Am J Surg Pathol 2010;34:1155-1162.
28. Shaw AT, Solomon B. Targeting anaplastic lymphoma kinase in lung cancer. Clin Cancer Res 2011;17: 2081-2086.
29. Tsao MS, Fraser RS. Primary pulmonary adenocarcinoma with enteric differentiation. Cancer 1991;68: 1754-1757.
30. Yousem SA. Pulmonary intestinal-type adenocarcinoma does not show enteric differentiation by immunohistochemical study. Mod Pathol 2005;18:816-821.
31. Inamura K, Satoh Y, Okumura S, et al. Pulmonary adenocarcinomas with enteric differentiation: histologic and immunohistochemical characteristics compared with metastatic colorectal cancers and usual pulmonary adenocarcinomas. Am J Surg Pathol 2005; 29:660-665.
32. Canney A, Sheahan K, Keegan D, et al. Synchronous lung tumours in a patient with metachronous colorectal carcinoma and a germline MSH2 mutation. J Clin Pathol 2009;62:471-473.
33. Albores-Saavedra J, Henson DE, Moran-Portela D, et al.Cribriform Carcinoma of the Gallbladder: A Clinicopathologic Study of 7 Cases. Am J Surg Pathol 2008;32: 1694-1698.
34. Cameselle-Teijeiro J, Menasce LP, Yap BK, et al. Cribriform-morular variant of papillary thyroid carcinoma: molecular characterization of a case with neuroendocrine differentiation and aggressive behavior. Am J Clin Pathol 2009;131:134-142.
35. Tamboli P, Mohsin SK, Hailemariam S, et al. Colonic adenocarcinoma metastatic to the urinary tract versus primary tumors of the urinary tract with glandular differentiation: a report of 7 cases and investigation using a limited immunohistochemical panel. Arch Pathol Lab Med 2002;126:1057-1063.
36. Meriden Z, Yemelyanova AV, Vang R, et al. Ovarian metastases of pancreaticobiliary tract adenocarcinomas: analysis of 35 cases, with emphasis on the ability of metastases to simulate primary ovarian mucinous tumors. Am J Surg Pathol 2011;35:276-288.
37. Skalova A, Sima R, Kaspirkova-Nemcova J, et al. Cribriform adenocarcinoma of minor salivary gland origin principally affecting the tongue: characterization of new entity. Am J Surg Pathol 2011;35:1168-1176.
38. Angeles-Angeles A, Chable-Montero F, Martinez-Benitez B, et al. Unusual metastases of papillary thyroid carcinoma: report of 2 cases. Ann Diag Pathol 2009;13:189-196.
39. DeCostanzo DC, Elias JM, Chumas JC. Necrosis in 84 ovarian carcinomas: a morphologic study of primary versus metastatic colonic carcinoma with a selective immunohistochemical analysis of cytokeratin subtypes and carcinoembryonic antigen. Int J Gynecol Pathol 1997;16:245-249.
40. Toker C. Tumors: An Atlas of Differential Diagnosis, 1st edn Lippincott Williams and Wilkins 1983, pp 216-217.
41. Nakatani Y, Masudo K, Miyagi Y, et al. Aberrant nuclear localization and gene mutation of beta-catenin in low-grade adenocarcinoma of fetal lung type: upregulation of the Wnt signaling pathway may be a common denominator for the development of tumors that form morules. Mod Pathol 2002;15:617-624.
42. Inamura K, Takeuchi K, Togashi Y, et al. EML4-ALK lung cancers are characterized by rare other mutations, a TTF-1 cell lineage, an acinar histology, and young onset. Mod Pathol 2009;22:508-515.
43. Inamura K, Takeuchi K, Togashi Y, et al. EML4-ALK fusion is linked to histological characteristics in a subset of lung cancers. J Thorac Oncol 2008;3:13-17.
44. 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;15:5216-5223.
45. Takahashi T, Sonobe M, Kobayashi M, et al. Clinicopathologic features of non-small-cell lung cancer with EML4-ALK fusion gene. Ann Surg Oncol 2010;17:889-897.
46. Yoshida A, Tsuta K, Nakamura H, et al. Comprehensive histologic analysis of ALK-rearranged lung carcinomas. Am J Surg Pathol 2011;35:1226-1234.
47. Wong DW, Leung EL, So KK, et al. The EML4-ALK fusion gene is involved in various histologic types of lung cancers from nonsmokers with wild-type EGFR and KRAS. Cancer 2009;115:1723-1733.