Skip to main content
Top
Published in: Annals of Surgical Oncology 9/2012

01-09-2012 | Thoracic Oncology

The Significance of Visceral Pleural Surface Invasion in 321 Cases of Non-Small Cell Lung Cancers with Pleural Retraction

Authors: Yih-Leong Chang, MD, Mong-Wei Lin, MD, Jin-Yuan Shih, MD, PhD, Chen-Tu Wu, MD, Yung-Chie Lee, MD, PhD

Published in: Annals of Surgical Oncology | Issue 9/2012

Login to get access

Abstract

Background

In order to improve prognostic applications and treatment decisions, we report our experiences of visceral pleural surface invasion (VPSI) in non-small cell lung cancers (NSCLCs) with pleural retraction.

Methods

A total of 321 NSCLCs with pleural retraction were identified by carefully inspecting surgically resected specimens. The extent of pleural invasion, including the use of elastic stain, was evaluated. Patients with and without VPSI were compared for clinicopathologic parameters and survival.

Results

VPSI was identified in 170 (53.0 %) of the stage I–III cases and 98 (43.4 %) of the patients with stage I disease. VPSI was associated with a higher frequency of tumor size greater than 3 cm, moderate/poor differentiation, vascular invasion, mediastinal lymph node metastasis, extranodal involvement, and higher TNM stages. Multivariate analysis revealed VPSI to be a significant independent predictor of unfavorable prognosis. The 5-year survival of patients with and without VPSI was 57.9 and 83.0 %, respectively (P = 0.001), and was 74.3 and 88.5 % (P = 0.005) in stages I–III and stage I disease, respectively.

Conclusions

VPSI is an independent factor for poor prognosis in NSCLCs, regardless of lymph node status. Stage IB NSCLCs with PL1 pleural invasion are associated with a survival rate similar to that of stage IA NSCLCs and could be classified as T1 lesions. While surgical treatment is adequate in these patients, stage IB NSCLCs with VPSI have poor prognosis, and these patients should be considered for adjuvant chemotherapy.
Appendix
Available only for authorised users
Literature
1.
go back to reference Brewer LA, Bai AF, Little JN, Pardo GR. Carcinoma of the lung: practical classification of early diagnosis and survival treatment. JAMA. 1958;166:1149–54.CrossRef Brewer LA, Bai AF, Little JN, Pardo GR. Carcinoma of the lung: practical classification of early diagnosis and survival treatment. JAMA. 1958;166:1149–54.CrossRef
2.
go back to reference Mountain CF. Revisions in the International System for Staging Lung Cancer. Chest. 1997;111:1710–7.PubMedCrossRef Mountain CF. Revisions in the International System for Staging Lung Cancer. Chest. 1997;111:1710–7.PubMedCrossRef
3.
go back to reference Martini N, Flehinger BJ, Nagasaki F, Hart B. Prognostic significance of N1 disease in carcinoma of the lung. J Thorac Cardiovasc Surg. 1983;86:646–53.PubMed Martini N, Flehinger BJ, Nagasaki F, Hart B. Prognostic significance of N1 disease in carcinoma of the lung. J Thorac Cardiovasc Surg. 1983;86:646–53.PubMed
4.
go back to reference Ichinose Y, Yano T, Asoh H, Yokoyama H, Yoshino I, Katsuda Y. Prognostic factors obtained by a pathologic examination in completely resected non-small-cell lung cancer, an analysis in each pathologic stage. J Thorac Cardiovasc Surg. 1995;110:601–5.PubMedCrossRef Ichinose Y, Yano T, Asoh H, Yokoyama H, Yoshino I, Katsuda Y. Prognostic factors obtained by a pathologic examination in completely resected non-small-cell lung cancer, an analysis in each pathologic stage. J Thorac Cardiovasc Surg. 1995;110:601–5.PubMedCrossRef
5.
go back to reference Shimizu K, Yoshida J, Nagai K, Nishimura M, Ishii G, Morishita Y, et al. Visceral pleural invasion is an invasive and aggressive indicator of non-small cell lung cancer. J Thorac Cardiovasc Surg. 2005;130:160–5.PubMedCrossRef Shimizu K, Yoshida J, Nagai K, Nishimura M, Ishii G, Morishita Y, et al. Visceral pleural invasion is an invasive and aggressive indicator of non-small cell lung cancer. J Thorac Cardiovasc Surg. 2005;130:160–5.PubMedCrossRef
6.
go back to reference Manac’h D, Riquet M, Medioni J, Le Pimpec Barthes F, Dujon A, Danel C. Visceral pleura invasion by non-small cell lung cancer: an underrated bad prognostic factor. Ann Thorac Surg. 2001;71:1088–93.PubMedCrossRef Manac’h D, Riquet M, Medioni J, Le Pimpec Barthes F, Dujon A, Danel C. Visceral pleura invasion by non-small cell lung cancer: an underrated bad prognostic factor. Ann Thorac Surg. 2001;71:1088–93.PubMedCrossRef
8.
go back to reference Oken MM, Creech RH, Tormey DC, Horton J, Davis TE, McFadden ET, et al. Toxicity and response criteria of the Eastern Cooperative Oncology Group. Am J Clin Oncol. 1982;5:649–55.PubMedCrossRef Oken MM, Creech RH, Tormey DC, Horton J, Davis TE, McFadden ET, et al. Toxicity and response criteria of the Eastern Cooperative Oncology Group. Am J Clin Oncol. 1982;5:649–55.PubMedCrossRef
9.
go back to reference Travis WD, Brambilla E, Müller-Hermelink H, Harris CC. Pathology and Genetics of Tumours of the Lung, Pleura, Thymus and Heart. Lyon: IARC Press, 2004;10–1. Travis WD, Brambilla E, Müller-Hermelink H, Harris CC. Pathology and Genetics of Tumours of the Lung, Pleura, Thymus and Heart. Lyon: IARC Press, 2004;10–1.
10.
go back to reference Goldstraw P. Staging Manual in Thoracic Oncology. Denver: IASLC, 2009;85–9. Goldstraw P. Staging Manual in Thoracic Oncology. Denver: IASLC, 2009;85–9.
11.
go back to reference Hammar SP. Common Tumors. In: Dail DH, Hammar SP, eds. Pulmonary Pathology, 2nd ed. New York: Springer-Verlag, 1994:1123–278. Hammar SP. Common Tumors. In: Dail DH, Hammar SP, eds. Pulmonary Pathology, 2nd ed. New York: Springer-Verlag, 1994:1123–278.
12.
go back to reference Travis WD, Brambilla E, Rami-Porta R, Vallières E, Tsuboi M, Rusch V, et al. International Staging Committee. Visceral pleural invasion: pathologic criteria and use of elastic stains: proposal for the 7th edition of the TNM classification for lung cancer. J Thorac Oncol. 2008;3:1384–90.PubMedCrossRef Travis WD, Brambilla E, Rami-Porta R, Vallières E, Tsuboi M, Rusch V, et al. International Staging Committee. Visceral pleural invasion: pathologic criteria and use of elastic stains: proposal for the 7th edition of the TNM classification for lung cancer. J Thorac Oncol. 2008;3:1384–90.PubMedCrossRef
13.
go back to reference Takizawa T, Terashima M, Koiki T, Watanabe T, Kurita Y, Yokoyama A, et al. Lymph node metastasis in small peripheral adenocarcinoma of the lung. J Thorac Cardiovasc Surg. 1998;116:276–80.PubMedCrossRef Takizawa T, Terashima M, Koiki T, Watanabe T, Kurita Y, Yokoyama A, et al. Lymph node metastasis in small peripheral adenocarcinoma of the lung. J Thorac Cardiovasc Surg. 1998;116:276–80.PubMedCrossRef
14.
go back to reference Hsu CP, Hsia JY, Chang GC, Chuang CY, Shai SE, Yang SS, et al. Surgical-pathologic factors affect long-term outcomes in stage IB (pT2N0M0) non-small cell lung cancer: A heterogeneous disease. J Thorac Cardiovasc Surg. 2009;138:426–33.PubMedCrossRef Hsu CP, Hsia JY, Chang GC, Chuang CY, Shai SE, Yang SS, et al. Surgical-pathologic factors affect long-term outcomes in stage IB (pT2N0M0) non-small cell lung cancer: A heterogeneous disease. J Thorac Cardiovasc Surg. 2009;138:426–33.PubMedCrossRef
15.
go back to reference Suzuki K, Nagai K, Yoshida J, Nishimura M, Nishiwaki Y. Predictors of lymph node and intrapulmonary metastasis in clinical stage IA non-small cell lung carcinoma. Ann Thorac Surg. 2001;72:352–6.PubMedCrossRef Suzuki K, Nagai K, Yoshida J, Nishimura M, Nishiwaki Y. Predictors of lymph node and intrapulmonary metastasis in clinical stage IA non-small cell lung carcinoma. Ann Thorac Surg. 2001;72:352–6.PubMedCrossRef
16.
go back to reference Maeda R, Yoshida J, Ishii G, Hishida T, Nishimura M, Nagai K. Risk factors for tumor recurrence in patients with early-stage (stage I and II) non-small cell lung cancer: Patient selection criteria for adjuvant chemotherapy according to the 7th edition TNM classification. Chest. 2011;140:1494–502.PubMedCrossRef Maeda R, Yoshida J, Ishii G, Hishida T, Nishimura M, Nagai K. Risk factors for tumor recurrence in patients with early-stage (stage I and II) non-small cell lung cancer: Patient selection criteria for adjuvant chemotherapy according to the 7th edition TNM classification. Chest. 2011;140:1494–502.PubMedCrossRef
17.
go back to reference Asamura H, Goya T, Yoshimura H, Sohara Y, Eguchi K, Mori M, et al. A Japanese Lung Cancer Registry Study: prognosis of 13,010 resected lung cancers. J Thorac Oncol. 2008;3:46–52.PubMedCrossRef Asamura H, Goya T, Yoshimura H, Sohara Y, Eguchi K, Mori M, et al. A Japanese Lung Cancer Registry Study: prognosis of 13,010 resected lung cancers. J Thorac Oncol. 2008;3:46–52.PubMedCrossRef
18.
go back to reference Mizuno T, Ishii G, Nagai K, Yoshida J, Nishimura M, Mochizuki T, et al. Identification of a low risk subgroup of stage IB lung adenocarcinoma patients. Lung Cancer. 2008;62:302–8.PubMedCrossRef Mizuno T, Ishii G, Nagai K, Yoshida J, Nishimura M, Mochizuki T, et al. Identification of a low risk subgroup of stage IB lung adenocarcinoma patients. Lung Cancer. 2008;62:302–8.PubMedCrossRef
19.
go back to reference Bréchot JM, Chevret S, Charpentier MC, Appere de Vecchi C, Capron F, Prudent J, et al. Blood vessel and lymphatic vessel invasion in resected non-small cell lung carcinoma. Cancer. 1996;78:2111–8.PubMedCrossRef Bréchot JM, Chevret S, Charpentier MC, Appere de Vecchi C, Capron F, Prudent J, et al. Blood vessel and lymphatic vessel invasion in resected non-small cell lung carcinoma. Cancer. 1996;78:2111–8.PubMedCrossRef
20.
go back to reference Chang YL, Wu CT, Lee YC. Surgical treatment of synchronous multiple primary lung cancers: Experience of 92 patients. J Thorac Cardiovasc Surg. 2007;134:630–7.PubMedCrossRef Chang YL, Wu CT, Lee YC. Surgical treatment of synchronous multiple primary lung cancers: Experience of 92 patients. J Thorac Cardiovasc Surg. 2007;134:630–7.PubMedCrossRef
21.
go back to reference Maeda R, Yoshida J, Ishii G, Hishida T, Nishimura M, Nagai K. Poor prognostic factors in patients with stage IB non-small cell lung cancer according to the seventh edition TNM classification. Chest. 2011;139:855–61.PubMedCrossRef Maeda R, Yoshida J, Ishii G, Hishida T, Nishimura M, Nagai K. Poor prognostic factors in patients with stage IB non-small cell lung cancer according to the seventh edition TNM classification. Chest. 2011;139:855–61.PubMedCrossRef
22.
go back to reference Johnson BE, Jänne PA. Epidermal growth factor receptor mutations in patients with non-small cell lung cancer. Cancer Res. 2005;65:7525–9.PubMed Johnson BE, Jänne PA. Epidermal growth factor receptor mutations in patients with non-small cell lung cancer. Cancer Res. 2005;65:7525–9.PubMed
23.
go back to reference Li M, Ito H, Wada H, Tanaka F. Pit-fall sign on computed tomography predicts pleural involvement and poor prognosis in non-small cell lung cancer. Lung Cancer. 2004;46:349–55.PubMedCrossRef Li M, Ito H, Wada H, Tanaka F. Pit-fall sign on computed tomography predicts pleural involvement and poor prognosis in non-small cell lung cancer. Lung Cancer. 2004;46:349–55.PubMedCrossRef
24.
go back to reference Inoue M, Minami M, Shiono H, Sawabata N, Ideguchi K, Okumura M. Clinicopathologic study of resected, peripheral, small-sized, non-small cell lung cancer tumors of 2 cm or less in diameter: Pleural invasion and increase of serum carcinoembryonic antigen level as predictors of nodal involvement. J Thorac Cardiovasc Surg. 2006;131:988–93.PubMedCrossRef Inoue M, Minami M, Shiono H, Sawabata N, Ideguchi K, Okumura M. Clinicopathologic study of resected, peripheral, small-sized, non-small cell lung cancer tumors of 2 cm or less in diameter: Pleural invasion and increase of serum carcinoembryonic antigen level as predictors of nodal involvement. J Thorac Cardiovasc Surg. 2006;131:988–93.PubMedCrossRef
25.
go back to reference Kawase A, Yoshida J, Ishii G, Hishida T, Nishimura M, Nagai K. Visceral pleural invasion classification in non-small cell lung cancer. J Thorac Oncol. 2010;5:1784–8.PubMedCrossRef Kawase A, Yoshida J, Ishii G, Hishida T, Nishimura M, Nagai K. Visceral pleural invasion classification in non-small cell lung cancer. J Thorac Oncol. 2010;5:1784–8.PubMedCrossRef
26.
go back to reference Riquet M, Assouad J, Foucault C, Danel C. Letter to the editor. Visceral pleura invasion and lung cancer: further clarifications. Eur J Cardiothorac Surg. 2004;25:471.PubMedCrossRef Riquet M, Assouad J, Foucault C, Danel C. Letter to the editor. Visceral pleura invasion and lung cancer: further clarifications. Eur J Cardiothorac Surg. 2004;25:471.PubMedCrossRef
27.
go back to reference Jones LW, Hornsby WE, Goetzinger A, Forbes LM, Sherrard EL, Quist M, et al. Prognostic significance of functional capacity and exercise behavior in patients with metastatic non-small cell lung cancer. Lung Cancer. doi:10.1016/j.lungcan.2011.10.009 [Epub ahead of print]. Jones LW, Hornsby WE, Goetzinger A, Forbes LM, Sherrard EL, Quist M, et al. Prognostic significance of functional capacity and exercise behavior in patients with metastatic non-small cell lung cancer. Lung Cancer. doi:10.​1016/​j.​lungcan.​2011.​10.​009 [Epub ahead of print].
28.
go back to reference Doning JS, Le QT, Wakelee HA. Lung cancer in women: Exploring sex differences in susceptibility, biology, and therapeutic response. Clin Lung Cancer. 2006;8:22–9.CrossRef Doning JS, Le QT, Wakelee HA. Lung cancer in women: Exploring sex differences in susceptibility, biology, and therapeutic response. Clin Lung Cancer. 2006;8:22–9.CrossRef
29.
go back to reference Wang NS. The preformed stomas connecting the pleural cavity and the lymphatics in the parietal pleura. Am Rev Respir Dis. 1975;111:12–20.PubMed Wang NS. The preformed stomas connecting the pleural cavity and the lymphatics in the parietal pleura. Am Rev Respir Dis. 1975;111:12–20.PubMed
30.
go back to reference Fujimoto T, Cassivi SD, Yang P, Barnes SA, Nichols FC, Deschamps C, et al. Completely resected N1 non-small cell lung cancer: Factors affecting recurrence and long-term survival. J Thorac Cardiovasc Surg. 2003;132:499–506.CrossRef Fujimoto T, Cassivi SD, Yang P, Barnes SA, Nichols FC, Deschamps C, et al. Completely resected N1 non-small cell lung cancer: Factors affecting recurrence and long-term survival. J Thorac Cardiovasc Surg. 2003;132:499–506.CrossRef
31.
go back to reference Osaki T, Nagashima A, Yoshimatsu T, Yamada S, Yasumoto K. Visceral pleural involvement in nonsmall cell lung cancer: prognostic significance. Ann Thorac Surg. 2004;77:1769–73.PubMedCrossRef Osaki T, Nagashima A, Yoshimatsu T, Yamada S, Yasumoto K. Visceral pleural involvement in nonsmall cell lung cancer: prognostic significance. Ann Thorac Surg. 2004;77:1769–73.PubMedCrossRef
32.
go back to reference Shimizu K, Yoshida J, Nagai K, Nishimura M, Yokose T, Ishii G, et al. Visceral pleural invasion classification in non-small cell lung cancer: a proposal on the basis of outcome assessment. J Thorac Cardiovasc Surg. 2004;127:1574–8.PubMedCrossRef Shimizu K, Yoshida J, Nagai K, Nishimura M, Yokose T, Ishii G, et al. Visceral pleural invasion classification in non-small cell lung cancer: a proposal on the basis of outcome assessment. J Thorac Cardiovasc Surg. 2004;127:1574–8.PubMedCrossRef
33.
go back to reference Sakakura N, Mori S, Okuda K, Fukui T, Hatooka S, Shinoda M, et al. Subcategorization of lung cancer based on tumor size and degree of visceral pleural invasion. Ann Thorac Surg. 2008;86:1084–91.PubMedCrossRef Sakakura N, Mori S, Okuda K, Fukui T, Hatooka S, Shinoda M, et al. Subcategorization of lung cancer based on tumor size and degree of visceral pleural invasion. Ann Thorac Surg. 2008;86:1084–91.PubMedCrossRef
34.
go back to reference Rami-Porta R, Wittekind C, Goldstraw P; International Association for the Study of Lung Cancer (IASLC) Staging Committee. Complete resection in lung cancer surgery: proposed definition. Lung Cancer. 2005;49:25–33.PubMedCrossRef Rami-Porta R, Wittekind C, Goldstraw P; International Association for the Study of Lung Cancer (IASLC) Staging Committee. Complete resection in lung cancer surgery: proposed definition. Lung Cancer. 2005;49:25–33.PubMedCrossRef
Metadata
Title
The Significance of Visceral Pleural Surface Invasion in 321 Cases of Non-Small Cell Lung Cancers with Pleural Retraction
Authors
Yih-Leong Chang, MD
Mong-Wei Lin, MD
Jin-Yuan Shih, MD, PhD
Chen-Tu Wu, MD
Yung-Chie Lee, MD, PhD
Publication date
01-09-2012
Publisher
Springer-Verlag
Published in
Annals of Surgical Oncology / Issue 9/2012
Print ISSN: 1068-9265
Electronic ISSN: 1534-4681
DOI
https://doi.org/10.1245/s10434-012-2354-y

Other articles of this Issue 9/2012

Annals of Surgical Oncology 9/2012 Go to the issue