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Pulmonary enteric adenocarcinoma: an overview

Published online by Cambridge University Press:  28 April 2020

Raffaele Palmirotta*
Affiliation:
Department of Biomedical Sciences and Human Oncology, University of Bari ‘Aldo Moro’, P.zza G. Cesare, 11 – 70124Bari, Italy
Domenica Lovero
Affiliation:
Department of Biomedical Sciences and Human Oncology, University of Bari ‘Aldo Moro’, P.zza G. Cesare, 11 – 70124Bari, Italy
Stella D'Oronzo
Affiliation:
Department of Biomedical Sciences and Human Oncology, University of Bari ‘Aldo Moro’, P.zza G. Cesare, 11 – 70124Bari, Italy IRCCS-Istituto Tumori ‘Giovanni Paolo II’, Viale Orazio Flacco, 65, 70124Bari, Italy
Annalisa Todisco
Affiliation:
Department of Biomedical Sciences and Human Oncology, University of Bari ‘Aldo Moro’, P.zza G. Cesare, 11 – 70124Bari, Italy
Valeria Internò
Affiliation:
Department of Biomedical Sciences and Human Oncology, University of Bari ‘Aldo Moro’, P.zza G. Cesare, 11 – 70124Bari, Italy
Fabio Mele
Affiliation:
IRCCS-Istituto Tumori ‘Giovanni Paolo II’, Viale Orazio Flacco, 65, 70124Bari, Italy
Luigia Stefania Stucci
Affiliation:
Department of Biomedical Sciences and Human Oncology, University of Bari ‘Aldo Moro’, P.zza G. Cesare, 11 – 70124Bari, Italy
Franco Silvestris
Affiliation:
Department of Biomedical Sciences and Human Oncology, University of Bari ‘Aldo Moro’, P.zza G. Cesare, 11 – 70124Bari, Italy
*
Author for correspondence: Raffaele Palmirotta, E-mail: [email protected]

Abstract

Most commonly described as sporadic, pulmonary adenocarcinoma with enteric differentiation (PAED) is a rare variant of invasive lung cancer recently established and recognised by the World Health Organization. This tumour is highly heterogeneous and shares several morphological features with pulmonary and colorectal adenocarcinomas. Our objective is to summarise current research on PAED, focusing on its immunohistochemical and molecular features as potential tools for differential diagnosis from colorectal cancer, as well as prognosis definition and therapeutic choice. PAED exhibits an ‘entero-like’ pathological morphology in more than half cases, expressing at least one of the typical immunohistochemical markers of enteric differentiation, namely CDX2, CK20 or MUC2. For this reason, this malignancy appears often indistinguishable from a colorectal cancer metastasis, making the differential diagnosis laborious. Although standard diagnostic criteria have not been established yet, in the past few years, a number of approaches have been addressed, aimed at defining specific immunohistochemical and molecular signatures. Based on previously published literature, we have collected and analysed molecular and immunohistochemical data on this rare neoplasm, and have described the state of the art on diagnostic criteria as well as major clinical and therapeutic implications.

The analysis of data from 295 patients from 58 published articles allowed us to identify the most represented immunohistochemical and molecular markers, as well as major differences between Asian PAEDs and those diagnosed in European/North American countries. The innovative molecular approaches, exploring driver mutations or new gene alterations, could help to identify rare prognostic factors and guide future tailored therapeutic approaches to this rare neoplasm.

Type
Review
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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References

Tsao, MS and Fraser, RS (1991) Primary pulmonary adenocarcinoma with enteric differentiation. Cancer 68, 17541757.3.0.CO;2-E>CrossRefGoogle ScholarPubMed
Weidner, N (1992) Pulmonary adenocarcinoma with intestinal-type differentiation. Ultrastructural Pathology 16, 710.CrossRefGoogle ScholarPubMed
Inamura, K et al. (2005) Pulmonary adenocarcinomas with enteric differentiation: histologic and immunohistochemical characteristics compared with metastatic colorectal cancers and usual pulmonary adenocarcinomas. American Journal of Surgical Pathology 29, 660665.CrossRefGoogle ScholarPubMed
Yousem, SA (2005) Pulmonary intestinal-type adenocarcinoma does not show enteric differentiation by immunohistochemical study. Modern Pathology 18, 816821.CrossRefGoogle Scholar
Satoh, Y et al. (2006) Cytology of pulmonary adenocarcinomas showing enteric differentiation. Acta Cytologica 50, 250256.CrossRefGoogle ScholarPubMed
Maeda, R et al. (2008) Pulmonary intestinal-type adenocarcinoma. Interactive Cardiovascular and Thoracic Surgery 7, 349351.CrossRefGoogle ScholarPubMed
Li, HC et al. (2009) Primary pulmonary adenocarcinoma with intestinal differentiation mimicking metastatic colorectal carcinoma: case report and review of literature. American Journal of Clinical Pathology 131, 129133.CrossRefGoogle ScholarPubMed
Canney, A et al. (2009) Synchronous lung tumours in a patient with metachronous colorectal carcinoma and a germline MSH2 mutation. Journal of Clinical Pathology 62, 471473.CrossRefGoogle Scholar
Wei, Q et al. (2010) Expression and significance of TTF-1, CK7, CK5/6, P63 and CK20 in mucin producing lung cancer. Chinese Journal of Difficult and Complicated Cases 11, 822–624.Google Scholar
Tominaga, S et al. (2006) A case of intratracheal metastasis of lung adenocarcinoma showing intestinal differentiation. Haigan 46, 173.Google Scholar
Bian, T et al. (2017) Combination of cadherin-17 and SATB homeobox 2 serves as potential optimal makers for the differential diagnosis of pulmonary enteric adenocarcinoma and metastatic colorectal adenocarcinoma. Oncotarget 8, 6344263452.CrossRefGoogle ScholarPubMed
Nottegar, A et al. (2018) Pulmonary adenocarcinoma with enteric differentiation: immunohistochemistry and molecular morphology. Applied Immunohistochemistry & Molecular Morphology 26, 383387.Google ScholarPubMed
Travis, WD et al. (2011) International association for the study of lung cancer/American thoracic society/European respiratory society international multidisciplinary classification of lung adenocarcinoma. Journal of Thoracic Oncology 6, 244285.CrossRefGoogle Scholar
Travis, WD et al. (2013) Diagnosis of lung adenocarcinoma in resected specimens: implications of the 2011 International Association for the Study of Lung Cancer/American Thoracic Society/European Respiratory Society classification. Archives of Pathology & Laboratory Medicine 137, 685705.CrossRefGoogle Scholar
Truini, A et al. (2015) Classification of different patterns of pulmonary adenocarcinomas. Expert Review of Respiratory Medicine 9, 571586.CrossRefGoogle ScholarPubMed
Wang, CX et al. (2014) Pulmonary enteric adenocarcinoma: a study of the clinicopathologic and molecular status of nine cases. International Journal of Clinical and Experimental Pathology 7, 12661274.Google ScholarPubMed
El Hammoumi, M-M, El Ochi, R and and Kabiri, EH (2016) Adenocarcinoma primario de pulmón con morfología entérica asociado a un adenocarcinoma primario de colon. Archivos de Bronconeumología 52, 221.CrossRefGoogle Scholar
Travis, WD et al. (2015) The 2015 World Health Organization classification of lung tumors: impact of genetic, clinical and radiologic advances since the 2004 classification. Journal of Thoracic Oncology 10, 12431260.CrossRefGoogle ScholarPubMed
Zhao, L et al. (2017) Clinicopathological, radiographic, and oncogenic features of primary pulmonary enteric adenocarcinoma in comparison with invasive adenocarcinoma in resection specimens. Medicine (Baltimore) 96, e8153.Google ScholarPubMed
Chen, M et al. (2018) Distinctive features of immunostaining and mutational load in primary pulmonary enteric adenocarcinoma: implications for differential diagnosis and immunotherapy. Journal of Translational Medicine 16, 81.CrossRefGoogle ScholarPubMed
Stojsic, J et al. (2014) Intestinal type of lung adenocarcinoma in younger adults. Case Reports in Pulmonology 2014, 282196.CrossRefGoogle ScholarPubMed
Todisco, A et al. (2019) Cutaneous metastasis as a primary presentation of a pulmonary enteric adenocarcinoma. International Journal of Biological Markers 34, 421426.CrossRefGoogle ScholarPubMed
Lin, L et al. (2017) Genetic mutations in lung enteric adenocarcinoma identified using next-generation sequencing. International Journal of Clinical and Experimental Pathology 10, 95839590.Google ScholarPubMed
Feng, C et al. (2018) Clinicopathologic significance of intestinal-type molecules’ expression and different EGFR gene status in pulmonary adenocarcinoma. Applied Immunohistochemistry & Molecular Morphology 27, 364372.CrossRefGoogle Scholar
Zhang, J et al. (2019) Differential diagnosis of pulmonary enteric adenocarcinoma and metastatic colorectal carcinoma with the assistance of next-generation sequencing and immunohistochemistry. Journal of Cancer Research and Clinical Oncology 145, 269279.CrossRefGoogle ScholarPubMed
Jurmeister, P et al. (2019) DNA methylation profiling reliably distinguishes pulmonary enteric adenocarcinoma from metastatic colorectal cancer. Modern Pathology 32, 855865.CrossRefGoogle ScholarPubMed
Falagas, ME et al. (2008) Comparison of PubMed, Scopus, Web of Science, and Google Scholar: strengths and weaknesses. FASEB Journal 22, 338342.CrossRefGoogle ScholarPubMed
Kuhn, E et al. (2018) Adenocarcinoma classification: patterns and prognosis. Pathologica 110, 511.Google ScholarPubMed
Handa, Y et al. (2016) Pulmonary enteric adenocarcinoma. General Thoracic and Cardiovascular Surgery 64, 749751.CrossRefGoogle ScholarPubMed
Garajova, I et al. (2015) MicroRNA profiling of primary pulmonary enteric adenocarcinoma in members from the same family reveals some similarities to pancreatic adenocarcinoma-a step towards personalized therapy. Clinical Epigenetics 7, 129.CrossRefGoogle ScholarPubMed
de Castria, TB and de Azevedo Souza, MCL (2016) Pulmonary adenocarcinoma with enteric differentiation: a distinctive histologic subtype. Journal of Reports and Images in Oncology 2, 2327.Google Scholar
Lin, LI et al. (2016) Clinicopathological observation of primary lung enteric adenocarcinoma and its response to chemotherapy: a case report and review of the literature. Experimental and Therapeutic Medicine 11, 201207.CrossRefGoogle ScholarPubMed
Jurmeister, P et al. (2019) Next generation sequencing of lung adenocarcinoma subtypes with intestinal differentiation reveals distinct molecular signatures associated with histomorphology and therapeutic options. Lung Cancer (Amsterdam, Netherlands) 138, 4351.CrossRefGoogle ScholarPubMed
Hatanaka, K et al. (2011) Primary pulmonary adenocarcinoma with enteric differentiation resembling metastatic colorectal carcinoma: a report of the second case negative for cytokeratin 7. Pathology Research and Practice 207, 188191.CrossRefGoogle ScholarPubMed
Matsushima, J et al. (2017) Clinicopathological, immunohistochemical, and mutational analyses of pulmonary enteric adenocarcinoma: usefulness of SATB2 and beta-catenin immunostaining for differentiation from metastatic colorectal carcinoma. Human Pathology 64, 179185.CrossRefGoogle ScholarPubMed
Qureshi, A and Furrukh, M (2013) Enteric adenocarcinoma lung: a rare presentation in an Omani woman. BMJ Case Reports 2013, 13.CrossRefGoogle Scholar
Laszlo, T et al. (2014) Pulmonary enteric adenocarcinoma indistinguishable morphologically and immunohistologically from metastatic colorectal carcinoma. Histopathology 65, 283287.CrossRefGoogle ScholarPubMed
Nottegar, A et al. (2017) Pulmonary adenocarcinoma with enteric differentiation: dissecting oncogenic genes alterations with DNA sequencing and FISH analysis. Experimental and Molecular Pathology 102, 276279.CrossRefGoogle ScholarPubMed
Planchard, D et al. . (2018) Metastatic non-small cell lung cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Annals of Oncology 29(supplement.4), iv192iv237.CrossRefGoogle ScholarPubMed
Savonarola, A et al. (2012) Pharmacogenetics and pharmacogenomics: role of mutational analysis in anti-cancer targeted therapy. Pharmacogenomics Journal 12, 277286.CrossRefGoogle ScholarPubMed
Fujita, A et al. (2011) A case of pulmonary adenocarcinoma with enteric differentiation. Haigan 51, 188192.CrossRefGoogle Scholar
Lin, D et al. (2013) Pulmonary enteric adenocarcinoma with villin brush border immunoreactivity: a case report and literature review. Journal of Thoracic Disease 5, E17E20.Google ScholarPubMed
Ishida, H et al. (2015) [A rare case of lymphangitis carcinomatosa of the lung due to primary pulmonary adenocarcinoma with intestinal differentiation successfully treated with chemotherapy]. Gan To Kagaku Ryoho 42, 371374.Google Scholar
Metro, G et al. (2015) Enteric-type adenocarcinoma of the lung harbouring a novel KRAS Q22 K mutation with concomitant KRAS polysomy: a case report. Ecancermedicalscience 9, 559.CrossRefGoogle Scholar
Shina, T., et al. (2016) A case of pulmonary enteric adenocarcinoma followed up as metastatic colorectal cancer. The Journal of the Japanese Association for Chest Surgery 30, 696702.CrossRefGoogle Scholar
Fujiwara, A, Iwashiro, N and Kimura, N (2017) A resected case of pulmonary enteric adenocarcinoma. Haigan 57, 758762.CrossRefGoogle Scholar
Gomez-Hernandez, MT et al. (2017) Enteric adenocarcinoma arising from a bronchogenic cyst. Archivos de Bronconeumologia 53, 523524.CrossRefGoogle ScholarPubMed
Matsubara, D et al. (2017) Inactivating mutations and hypermethylation of the NKX2–1/TTF-1 gene in non-terminal respiratory unit-type lung adenocarcinomas. Cancer Science 108, 18881896.CrossRefGoogle ScholarPubMed
Prakobkit, R et al. (2017) Pulmonary adenocarcinoma with enteric differentiation presenting with bronchorrhea. Journal of Thoracic Oncology 12, e120ee23.CrossRefGoogle ScholarPubMed
Shomura, S et al. (2017) [Surgical case of pulmonary enteric adenocarcinoma]. Kyobu Geka 70, 779781.Google Scholar
Sun, WW et al. (2017) Pulmonary enteric adenocarcinoma with pancreatic metastasis: a case report. Oncology Letters 13, 46514656.CrossRefGoogle ScholarPubMed
Hayama, M et al. (2018) A case of primary pulmonary enteric adenocarcinoma mimicking lung metastasis from colorectal cancer. Journal of the Japan Society for Respiratory Endoscopy 40, 584589.Google Scholar
Miura, K and Sakamoto, T (2018) [Pulmonary enteric adenocarcinoma; report of a case]. Kyobu Geka 71, 476479.Google Scholar
Miyaoka, M et al. (2018) CK7/CK20 double-negative pulmonary enteric adenocarcinoma with histopathological evaluation of transformation zone between enteric adenocarcinoma and conventional pulmonary adenocarcinoma. International Journal of Surgical Pathology 26, 464468.CrossRefGoogle ScholarPubMed
Suzuki, M et al. (2018) Pulmonary adenocarcinoma with high-grade fetal adenocarcinoma component has a poor prognosis, comparable to that of micropapillary adenocarcinoma. Modern Pathology 31, 14041417.CrossRefGoogle Scholar
Kimura, D et al. (2012) A surgical case of lung-intestinal type adenocarcinoma. Haigan 52, 743.Google Scholar
Toyazaki, T, Yamamoto, Y and Shinji, K (2015) Transverse colon cancer and intestinal lung gland. One case of duplicate cancer. Haigan 55, 558.Google Scholar
Mizoguchi, M et al. (2015) A resected case of intestinal lung adenocarcinoma. Haigan 55, 558.Google Scholar
Nojima, Y et al. (2015) One resected case of intestinal lung adenocarcinoma. Haigan 55, 558.Google Scholar
Saito, K et al. (2015) Intestinal lung adenocarcinoma with relatively long-term follow up. Haigan 55, 624.Google Scholar
Ogihara, A et al. (2018) A case of pulmonary enteric adenocarcinoma requiring differentiation from metastatic colorectal cancer. Haigan 58, 5556.CrossRefGoogle Scholar
Lee, JG, Kim, S and Shim, HS (2012) Napsin A is an independent prognostic factor in surgically resected adenocarcinoma of the lung. Lung Cancer (Amsterdam, The Netherlands) 77, 156161.CrossRefGoogle ScholarPubMed
Suzuki, M et al. (2015) High-grade fetal adenocarcinoma of the lung is a tumour with a fetal phenotype that shows diverse differentiation, including high-grade neuroendocrine carcinoma: a clinicopathological, immunohistochemical and mutational study of 20 cases. Histopathology 67, 806816.CrossRefGoogle ScholarPubMed
Calio, A et al. (2017) Increased frequency of bronchiolar histotypes in lung carcinomas associated with idiopathic pulmonary fibrosis. Histopathology 71, 725735.CrossRefGoogle ScholarPubMed
Yang, L et al. (2016) Detection of ALK translocation in non-small cell lung carcinoma (NSCLC) and its clinicopathological significance using the Ventana immunohistochemical staining method: a single-center large-scale investigation of 1, 504 Chinese Han patients. Chinese Journal of Cancer Research = Chung-kuo Yen Cheng Yen Chiu 28, 495502.CrossRefGoogle ScholarPubMed
Yaeger, R et al. (2018) Clinical sequencing defines the genomic landscape of metastatic colorectal cancer. Cancer Cell 33, 125136, e3.CrossRefGoogle ScholarPubMed
Gao, J et al. (2013) Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Science Signaling 6, l1.CrossRefGoogle ScholarPubMed
Schabath, MB, Cress, D and Munoz-Antonia, T (2016) Racial and ethnic differences in the epidemiology and genomics of lung cancer. Cancer Control: Journal of the Moffitt Cancer Center 23, 338346.CrossRefGoogle ScholarPubMed
Araujo, LH and Carbone, DP (2017) Non-small cell lung cancer genomics around the globe: focus on ethnicity. Journal of Thoracic Disease 9, E392EE94.CrossRefGoogle ScholarPubMed
Heath, EI et al. (2018) Racial disparities in the molecular landscape of cancer. Anticancer Research 38, 22352240.Google ScholarPubMed
Soh, J et al. (2015) Ethnicity affects EGFR and KRAS gene alterations of lung adenocarcinoma. Oncology Letters 10, 17751782.CrossRefGoogle ScholarPubMed
Graham, RP et al. (2018) Worldwide frequency of commonly detected EGFR mutations. Archives of Pathology & Laboratory Medicine 142, 163167.CrossRefGoogle ScholarPubMed
Dearden, S et al. (2013) Mutation incidence and coincidence in non small-cell lung cancer: meta-analyses by ethnicity and histology (mutMap). Annals of Oncology 24, 23712376.CrossRefGoogle Scholar
Garrido-Castro, AC and Felip, E (2013) HER2 driven non-small cell lung cancer (NSCLC): potential therapeutic approaches. Translational Lung Cancer Research 2, 122127.Google ScholarPubMed
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