Clinical feature of diagnostic challenging cases for pleural biopsy in patient with malignant pleural mesothelioma

Abstract

Objective

Pleural biopsy through video-assisted thoracic surgery (VATS pleural biopsy) is the most reliable diagnostic procedure for malignant pleural mesothelioma (MPM). However, definitive diagnosis of MPM is occasionally difficult to establish. This study aims to investigate clinicopathological features of MPM patients who failed diagnosis by the first VATS pleural biopsy.

Methods

Four hundred consecutive patients with suspected MPM who received VATS pleural biopsy between March 2004 and July 2017 were enrolled in this retrospective study. Patients, whose histological diagnoses were not definitive in the first VATS pleural biopsy, were followed up as atypical mesothelial proliferation (AMP) or non-specific pleuritis (NSP). Re-examination was performed in cases strongly suspected of having MPM.

Results

Of the 400 patients, 267 (66.8%) were pathologically diagnosed with MPM, 25 with metastatic carcinoma and 6 with benign pleural disease by the first VATS pleural biopsy. Of the remaining 102 patients diagnosed with AMP or NSP, 10 patients (9.8%) were subsequently diagnosed with MPM. Analysis of the clinical course revealed that only insufficient tissue for diagnosis was obtained via VATS pleural biopsy in all cases and that it was caused by very early stage without visible tumour in 4 patients, intrathoracic inflammation in 4 and desmoplastic MPM in 2.

Conclusions

In our review, 9.8% of patients diagnosed with AMP or NSP in first VATS pleural biopsy were subsequently diagnosed with MPM due to insufficient tissue for diagnosis. Definitive diagnosis via VATS pleural biopsy is sometimes challenging in following situation; very early stage, intrathoracic inflammation and desmoplastic MPM.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  1. 1.

    Rusch VW, Giroux D, Kennedy C, Ruffini E, Cangir AK, Rice D, et al. Initial analysis of the international association for the study of lung cancer mesothelioma database. J Thorac Oncol. 2012;7:1631–9.

    Article  Google Scholar 

  2. 2.

    Takuwa T, Hasegawa S. Current surgical strategies for malignant pleural mesothelioma. Surg Today. 2016;46:887–94.

    Article  Google Scholar 

  3. 3.

    Hasegawa S. Early mesothelioma revisited. Int J Clin Oncol. 2012;17:30–2.

    Article  Google Scholar 

  4. 4.

    Hasegawa S, Kondo N, Matsumoto S, Takuwa T, Hashimoto M, Orui H, et al. Practical approaches to diagnose and treat for T0 malignant pleural mesothelioma: a proposal for diagnostic total parietal pleurectomy. Int J Clin Oncol. 2012;17:33–9.

    Article  Google Scholar 

  5. 5.

    Husain AN, Colby TV, Ordonez NG, Allen TC, Attanoos RL, Beasley MB, 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.

    CAS  Article  Google Scholar 

  6. 6.

    Hjerpe A, Ascoli V, Bedrossian CW, Boon ME, Creaney J, Davidson B, et al. Guidelines for the cytopathologic diagnosis of epithelioid and mixed-type malignant mesothelioma. Complementary statement from the International Mesothelioma Interest Group, also endorsed by the International Academy of Cytology and the Papanicolaou Society of Cytopathology. Acta Cytol. 2015;59:2–16.

  7. 7.

    Husain AN, Colby T, Ordonez N, Krausz T, Attanoos R, Beasley MB, et al. Guidelines for pathologic diagnosis of malignant mesothelioma: 2012 update of the consensus statement from the International Mesothelioma Interest Group. Arch Pathol Lab Med. 2013;137:647–67.

    Article  Google Scholar 

  8. 8.

    Husain AN, Colby TV, Ordonez NG, Krausz T, Borczuk A, Cagle PT, et al. Guidelines for pathologic diagnosis of malignant mesothelioma: a consensus statement from the International Mesothelioma Interest Group. Arch Pathol Lab Med. 2009;133:1317–31.

    PubMed  Google Scholar 

  9. 9.

    Scherpereel A, Astoul P, Baas P, Berghmans T, Clayson H, de Vuyst P, et al. Guidelines of the European Respiratory Society and the European Society of Thoracic Surgeons for the management of malignant pleural mesothelioma. Eur Respir J. 2010;35:479–95.

    CAS  Article  Google Scholar 

  10. 10.

    Welker L, Muller M, Holz O, Vollmer E, Magnussen H, Jorres RA. Cytological diagnosis of malignant mesothelioma—improvement by additional analysis of hyaluronic acid in pleural effusions. Virchows Arch. 2007;450:455–61.

    CAS  Article  Google Scholar 

  11. 11.

    Boutin C, Rey F. Thoracoscopy in pleural malignant mesothelioma: a prospective study of 188 consecutive patients. Part 1: Diagnosis. Cancer. 1993;72:389–93.

  12. 12.

    Attanoos R, Gibbs A. The comparative accuracy of different pleural biopsy techniques in the diagnosis of malignant mesothelioma. Histopathology. 2008;53:340–4.

    CAS  Article  Google Scholar 

  13. 13.

    Heilo A, Stenwig AE, Solheim OP. Malignant pleural mesothelioma: US-guided histologic core-needle biopsy. Radiology. 1999;211:657–9.

    CAS  Article  Google Scholar 

  14. 14.

    Hansen M, Faurschou P, Clementsen P. Medical thoracoscopy, results and complications in 146 patients: a retrospective study. Respir Med. 1998;92:228–32.

    CAS  Article  Google Scholar 

  15. 15.

    Bueno R, Reblando J, Glickman J, Jaklitsch MT, Lukanich JM, Sugarbaker DJ. Pleural biopsy: a reliable method for determining the diagnosis but not subtype in mesothelioma. Ann Thorac Surg. 2004;78:1774–6.

    Article  Google Scholar 

  16. 16.

    Willendrup F, Bodtger U, Colella S, Rasmussen D, Clementsen PF. Diagnostic accuracy and safety of semirigid thoracoscopy in exudative pleural effusions in Denmark. J Bronchol Interv Pulmonol. 2014;21:215–9.

    Article  Google Scholar 

  17. 17.

    Miyoshi S, Sasada S, Izumo T, Matsumoto Y, Tsuchida T. Diagnostic utility of pleural fluid cell block versus pleural biopsy collected by flex-rigid pleuroscopy for malignant pleural disease: a single center retrospective analysis. PLoS ONE. 2016;11:e0167186.

    Article  Google Scholar 

  18. 18.

    Henderson DW, Reid G, Kao SC, van Zandwijk N, Klebe S. Challenges and controversies in the diagnosis of mesothelioma: part 1. Cytology-only diagnosis, biopsies, immunohistochemistry, discrimination between mesothelioma and reactive mesothelial hyperplasia, and biomarkers. J Clin Pathol. 2013;66:847–53.

  19. 19.

    Sheffield BS, Hwang HC, Lee AF, Thompson K, Rodriguez S, Tse CH, et al. BAP1 immunohistochemistry and p16 FISH to separate benign from malignant mesothelial proliferations. Am J Surg Pathol. 2015;39:977–82.

    Article  Google Scholar 

  20. 20.

    Hwang HC, Sheffield BS, Rodriguez S, Thompson K, Tse CH, Gown AM, et al. Utility of BAP1 immunohistochemistry and p16 (CDKN2A) FISH in the diagnosis of malignant mesothelioma in effusion cytology specimens. Am J Surg Pathol. 2016;40:120–6.

    Article  Google Scholar 

  21. 21.

    Hida T, Hamasaki M, Matsumoto S, Sato A, Tsujimura T, Kawahara K, 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;66:563–70.

    CAS  Article  Google Scholar 

  22. 22.

    Churg A, Hwang H, Tan L, Qing G, Taher A, Tong A, et al. Malignant mesothelioma in situ. Histopathology. 2018;72:1033–8.

    Article  Google Scholar 

  23. 23.

    Kinoshita Y, Hida T, Hamasaki M, Matsumoto S, Sato A, Tsujimura T, et al. A combination of MTAP and BAP1 immunohistochemistry in pleural effusion cytology for the diagnosis of mesothelioma. Cancer Cytopathol. 2018;126:54–63.

    CAS  Article  Google Scholar 

  24. 24.

    Hegmans JP, Hemmes A, Hammad H, Boon L, Hoogsteden HC, Lambrecht BN. Mesothelioma environment comprises cytokines and T-regulatory cells that suppress immune responses. Eur Respir J. 2006;27:1086–95.

    CAS  Article  Google Scholar 

  25. 25.

    Travis WD, Brambilla E, Burke AP, Marx A, Nicholson AG. Introduction to the 2015 World Health Organization classification of tumors of the lung, pleura, thymus, and heart. J Thorac Oncol. 2015;10:1240–2.

    Article  Google Scholar 

  26. 26.

    DePew ZS, Verma A, Wigle D, Mullon JJ, Nichols FC, Maldonado F. Nonspecific pleuritis: optimal duration of follow-up. Ann Thorac Surg. 2014;97:1867–71.

    Article  Google Scholar 

  27. 27.

    Wu D, Hiroshima K, Yusa T, Ozaki D, Koh E, Sekine Y, et al. Usefulness of p16/CDKN2A fluorescence in situ hybridization and BAP1 immunohistochemistry for the diagnosis of biphasic mesothelioma. Ann Diagn Pathol. 2017;26:31–7.

    Article  Google Scholar 

  28. 28.

    Metintas M, Ak G, Cadirci O, Yildirim H, Dundar E, Metintas S. Outcome of patients diagnosed with fibrinous pleuritis after medical thoracoscopy. Respir Med. 2012;106:1177–83.

    Article  Google Scholar 

  29. 29.

    Davies HE, Nicholson JE, Rahman NM, Wilkinson EM, Davies RJ, Lee YCG. Outcome of patients with nonspecific pleuritis/fibrosis on thoracoscopic pleural biopsies. Eur J Cardiothorac Surg. 2010;38:472–7.

    Article  Google Scholar 

  30. 30.

    Janssen JP, Ramlal S, Mravunac M. The long-term follow up of exudative pleural effusion after nondiagnostic thoracoscopy. J Bronchol Interv Pulmonol. 2004;11:169–74.

    Google Scholar 

Download references

Acknowledgements

We thank Miss Risa Murata for her secretarial skills. The authors thank Enago (https://www.enago.jp) for the English language review.

Funding

This study was funded by the Department of Thoracic Surgery, Hyogo College of Medicine.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Masaki Hashimoto.

Ethics declarations

Conflict of interest

All authors have nothing to disclose with regard to commercial support.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Hashimoto, M., Sato, A., Kuroda, A. et al. Clinical feature of diagnostic challenging cases for pleural biopsy in patient with malignant pleural mesothelioma. Gen Thorac Cardiovasc Surg 68, 820–827 (2020). https://doi.org/10.1007/s11748-020-01295-5

Download citation

Keywords

  • Malignant pleural mesothelioma
  • Pleural biopsy
  • Non-specific pleuritis