Diagnostic utility of BAP1 for malignant pleural mesothelioma in pleural fluid specimens with atypical morphology.


Journal

Cytopathology : official journal of the British Society for Clinical Cytology
ISSN: 1365-2303
Titre abrégé: Cytopathology
Pays: England
ID NLM: 9010345

Informations de publication

Date de publication:
01 2022
Historique:
revised: 07 05 2021
received: 16 02 2021
accepted: 14 05 2021
pubmed: 26 5 2021
medline: 5 4 2022
entrez: 25 5 2021
Statut: ppublish

Résumé

To assess the utility of BRCA1-associated protein 1 (BAP1) immunohistochemistry (IHC) for the diagnosis of malignant pleural mesothelioma (MPM) in fluid samples with atypical cytology. Pleural fluid samples with an atypical mesothelial proliferation (diagnostic categories: 'atypical' and 'suspicious') received between January 2015 and March 2018 at a tertiary referral centre were identified. Results of routine IHC testing were recorded for each case. BAP1 by IHC was performed and a final diagnosis sought from subsequent pathology specimens, medical records, or consensus clinical diagnosis. Of 50 cases identified, 41 were reported as atypical and 9 as suspicious. Seven (14%) demonstrated loss of BAP1 staining, 40 retained BAP1 staining, 1 had heterogeneous staining, and 2 had insufficient cells for analysis. All seven cases with BAP1 loss were diagnosed with MPM on follow-up. Of those with retained BAP1, 52.5% (21) were subsequently diagnosed with MPM, while 40% (16) had non-MPM diagnoses after a median follow-up of 24 months. Three cases were not further investigated based on patient and clinician decision. The case with heterogeneous staining was diagnosed as mesothelioma by clinical consensus. BAP1 IHC loss is highly specific for malignancy and has value as a rule-in test. Even in a tertiary centre with clinical interest in the cytological diagnosis of MPM this investigation was able to increase diagnostic accuracy beyond routine IHC studies. Cytological criteria remain valuable, as retained BAP1 in an atypical or suspicious mesothelial proliferation cannot exclude malignancy.

Identifiants

pubmed: 34033161
doi: 10.1111/cyt.13015
doi:

Substances chimiques

BAP1 protein, human 0
Biomarkers, Tumor 0
Tumor Suppressor Proteins 0
Ubiquitin Thiolesterase EC 3.4.19.12

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

84-92

Informations de copyright

© 2021 John Wiley & Sons Ltd.

Références

Robinson B, Lake R. Advances in malignant mesothelioma. N Engl J Med. 2005;353(13):1591-1603.
Australian Institute of Health and Welfare. Mesothelioma in Australia in 2019. Cat. no. CAN 134. Darlinghurst, NSW: AIHW; 2020.
Delgermaa V, Takahashi K, Park E, Le G, Hara T, Sorahan T. Global mesothelioma deaths reported to the World Health Organisation between 1994 and 2008. Bull World Health Organ. 2011;89:716-724.
Muruganandan S, Alfonso H, Franklin P, et al. Comparison of outcomes following a cytological or histological diagnosis of malignant mesothelioma. Br J Cancer. 2017;116(6):703-708.
Hjerpe A, Ascoli A, Bedrossian C, et al. Guidelines for the cytopathologic diagnosis of epithelioid and mixed-type malignant mesothelioma. Acta Cytol. 2015;59(1):2-16.
Segal A, Sterrett G, Frost F, et al. A diagnosis of malignant pleural mesothelioma can be made by effusion cytology: results of a 20 year audit. Pathology. 2013;45(1):44-48.
Monaco S, Mehrad M, Dacic S. Recent advances in the diagnosis of malignant mesothelioma: focus on approach in challenging cases and in limited tissue and cytologic samples. Adv Anat Pathol. 2018;25(1):24-30.
Louw A, Badiei A, Creaney J, Chai S, Lee Y. Advances in pathological diagnosis of mesothelioma: what pulmonologists should know. Curr Opin Pulm Med. 2019;25(4):354-361.
Husain A, Colby T, Ordonez N, et al. Guidelines for pathologic diagnosis of malignant mesothelioma: 2017 update of the consensus statement from the International Mesothelioma Interest Group. Arch Pathol Lab Med. 2018;142:89-108.
Travis W, Brambilia E, Burke A, Marx A, Nicholson A, eds. The World Health Organisation Classification of Tumours of the Lung, Pleura, Thymus and Heart, 4th edn. Lyon, France: IARC; 2015.
Whitaker D. The cytology of malignant mesothelioma. Cytopathology. 2000;11:139-151.
Stevens M, Leong A, Fazzalari N, Dowling K, Henderson D. Cytopathology of malignant mesothelioma: a stepwise logistic regression analysis. Diagn Cytopathol. 1992;8(4):333-341.
Churg A, Sheffield B, Galateau-Salle F. New markers for separating benign from malignant mesothelial proliferations. are we there yet? Arch Pathol Lab Med. 2016;140(4):318-321.
Hmeljak J, Sanchez-Vega F, Hoadley K, et al. Integrative molecular characterization of malignant pleural mesothelioma. Cancer Discov. 2018;8(12):1548-1565.
Sheffield B, Hwang H, Lee A, et al. BAP1 Immunohistochemistry and p16 FISH to separate benign from malignant mesothelial proliferations. Am J Clin Pathol. 2015;39(7):977-982.
Righi L, Duregon E, Vatrano S, et al. BRCA-1 Associated Protein 1 (BAP1) immunohistochemical expression as a diagnostic tool in malignancy pleural mesothelioma classification: a large retrospective study. J Thorac Oncol. 2016;11(11):2006-2017.
Wang X, Wang Z, Huang J, et al. Tissue-specific significance of BAP1 gene mutation in prognostic prediction and molecular taxonomy among different types of cancer. Tumour Biol. 2017;39(6):1-12.
Cigognetti M, Lonardi S, Fisogni S, et al. BAP1 (BRCA1-associated protein 1) is a highly specific marker for differentiating mesothelioma from reactive mesothelial proliferations. Mod Pathol. 2015;28(8):1043-1057.
McGregor S, McElherne J, Minor A, et al. BAP1 immunohistochemistry has limited prognostic utility as a complement of CDKN2A (p16) fluorescence in situ hybridization in malignant pleural mesothelioma. Hum Pathol. 2017;60:86-94.
Önder S, Özogul E, Koksal D, Sarinc Ulasli S, Firat P, Emri S. Diagnostic value of BRCA1-associated protein-1, glucose transporter-1 and desmin expression in the discrimination between reactive mesothelial proliferation and malignant mesothelioma in tissues and effusions. Cytopathology. 2019;30(6):592-600.
Cozzi I, Oprescu F, Rullo E, Ascoli A. Loss of BRCA-1 associated protein 1 (BAP1) expresion is useful in diagnostic cytopathology of malignant mesothelioma in effusions. Diagn Cytopathol. 2017;46:9-14.
Hwang H, Sheffield B, Rodriguez S, et al. Utility of BAP1 immunohistochemistry and p16 (CDKN2A) FISH in the diagnosis of malignant mesothelioma in effusion cytology specimens. Am J Clin Pathol. 2016;40(1):120-126.
College of American Pathologists Committee on Nomenclature and Classification of Disease. Systematized Nomenclature of Pathology. Chicago, IL: College of American Pathologists; 1965.
Chai S, Van Vliet C. Cytological diagnosis of malignant pleural mesothelioma. Curr Pulmonol Rep. 2017;6:1-8.
King J, Thatcher N, Pickering C, Hasleton P. Sensitivity and specificity of immunuhistochemical antibodies used to distinguish between benign and malignant pleural disease: a systematic review of published reports. Histopathology. 2006;49:561-568.
Minato H, Kurose N, Fukushima M, et al. Comparative immunohistochemical analysis of IMP3, GLUT1, EMA, CD146, and desmin for distinguishing malignant mesothelioma from reactive mesothelial cells. Am J Clin Pathol. 2014;141:85-93.
Ventii K, Devi N, Friedrich K, Chernova T, Tighiouart M, Van Meir E. BRCA1-associated protein-1 is a tumour suppressor that requires deubiquitinating activity and nuclear localisation. Can Res. 2008;68(17):6953-6962.
Bononi A, Giorgi C, Patergnani S, et al. BAP1 regulated IP3R3-mediated Ca2+ flux to mitochondria suppressing cell transformation. Nature. 2017;546(7659):549-553.
Yu H, Pak H, Hammond-Martel I, et al. Tumor suppressor and deubiquitinase BAP1 promotes DNA double-strand break repair. Proc Natl Acad Sci USA. 2014;111(1):285-290.
Ismail I, Davidson R, Gagne J, Xu Z, Poirier G, Hendzel M. Germline mutations in BAP1 impair its function in DNA double-strand break repair. Can Res. 2014;74(16):4282-4294.
Yoshikawa Y, Sato A, Tsujimura T, et al. Frequent inactivation of the BAP1 gene in epithelioid-type malignant mesothelioma. Cancer Sci. 2012;103(5):868-874.
Bott M, Brevet M, Taylor B, et al. The nuclear deubiquitinase BAP1 is commonly inactivated by somatic mutations and 3p21.1 losses in malignant pleural mesothelioma. Nat Genet. 2011;43:668-672.
Nasu M, Emi M, Pastorino S, et al. High incidence of somatic BAP1 alterations in sporadic malignant mesothelioma. J Thorac Oncol. 2015;10(4):565-576.
Farzin M, Toon C, Clarkson A, et al. Loss of expression of BAP1 predicts longer survival in mesothelioma. Pathology. 2015;47(4):302-307.
Wu D, Hiroshima K, Yusa T, et al. Usefulness of p16/CDKN2A fluorescence in situ hybridization and BAP1 immunohistochemistry for the diagnosis of biphasic mesothelioma. Ann Diagn Pathol. 2017;26:31-37.
Andrici J, Parkhill T, Jung J, t al. Loss of expression of BAP1 is very rare in non-small cell lung carcinoma. Pathology. 2016;48(4):336-340.
Owen D, Sheffield B, Ionescu D, Churg A. Loss of BRCA1-associated protein 1 (BAP1) expression is rare in non-small cell lung cancer. Hum Pathol. 2017;60:82-85.
Andrici J, Sheen A, Sioson L, et al. Loss of expression of BAP1 is a useful adjunct, which strongly supports the diagnosis of mesothlioma in effusion cytology. Mod Pathol. 2015;28:1360-1368.
Walts A, Hiroshima K, McGregor S, Wu D, Husain A, Marchevsky A. BAP1 immunostain and CDKN2A (p16) FISH analysis. Clinical applicability for the diagnosis of malignant mesothelioma in effusions. Diagn Cytopathol. 2016;44(7):599-606.
Pulford E, Huilgol K, Moffat D, Henderson D, Klebe S. Malignant mesothelioma, BAP1 immunohistochemistry, and VEGFA: does BAP1 have potential for early diagnosis and assessment of prognosis. Dis Markers. 2017;2017:e1310478.
Pillappa R, Maleszewski J, Sukov W, et al. Loss of BAP1 expression in atypical mesothelial proliferations helps to predict malignant mesothelioma. Am J Surg Pathol. 2018;42(2):256-263.
Hida T, Hamasaki M, Mastumoto S, et al. BAP1 Immunohistochemistry and p16 FISH results in combination provide higher confidence in malignant pleural mesothelioma diagnosis: ROC analysis of the two tests. Pathol Int. 2016;66(10):563-570.
Hida T, Hamasaki M, Mastumoto S, et al. Immunohistochemical detection of MTAP and BAP1 protein loss for mesothelioma diagnosis: comparison with 9p21 FISH and BAP1. Lung Cancer. 2017;104:98-105.
Hwang H, Pyott S, Rodriguez S, et al. BAP1 immunohistochemistry and p16 FISH in the diagnosis of sarcomatous and desmoplastic mesotheliomas. Am J Surg Pathol. 2016;40:714-718.
Chapel D, Schulte J, Berg K, et al. MTAP immunohistochemistry is an accurate and reproducible surrogate for CDKN2A fluorescence in situ hybridization in diagnosis of malignant pleural mesothelioma. Mod Pathol. 2020;33(2):245-254.
Kinoshita Y, Hida T, Hamasaki M, et al. A Combination of MTAP and BAP1 immunohistochemistry in pleural effusion cytology for the diagnosis of mesothelioma. Cancer Cytopathol. 2018;126:54-63.
Yoshimura M, Kinoshita Y, Hamasaki M, et al. Highly expressed EZH2 in combination with BAP1 and MTAP loss, as detected by immunohistochemistry, is useful for differentiating malignant pleural mesothelioma from reactive mesothelial hyperplasia. Lung Cancer. 2019;130:187-193.

Auteurs

Amber Louw (A)

Department of Anatomical Pathology, PathWest Laboratory Medicine, QEII Medical Centre, Nedlands, WA, Australia.
School of Medical and Health Sciences, Edith Cowan University, Perth, WA, Australia.
National Centre for Asbestos Related Diseases, University of Western Australia, Nedlands, WA, Australia.
Institute for Respiratory Health, Nedlands, WA, Australia.

Y C Gary Lee (YCG)

Institute for Respiratory Health, Nedlands, WA, Australia.
Department of Respiratory Medicine, Sir Charles Gairdner Hospital, Nedlands, WA, Australia.
School of Medicine, University of Western Australia, Nedlands, WA, Australia.

Nathan Acott (N)

Department of Anatomical Pathology, PathWest Laboratory Medicine, QEII Medical Centre, Nedlands, WA, Australia.

Jenette Creaney (J)

National Centre for Asbestos Related Diseases, University of Western Australia, Nedlands, WA, Australia.
Institute for Respiratory Health, Nedlands, WA, Australia.
Department of Respiratory Medicine, Sir Charles Gairdner Hospital, Nedlands, WA, Australia.

Chris van Vliet (C)

Department of Anatomical Pathology, PathWest Laboratory Medicine, QEII Medical Centre, Nedlands, WA, Australia.

Siaw Ming Chai (SM)

Department of Anatomical Pathology, PathWest Laboratory Medicine, QEII Medical Centre, Nedlands, WA, Australia.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH