{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,25]],"date-time":"2026-09-25T23:55:01Z","timestamp":1790380501683,"version":"4.1.0"},"reference-count":37,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2017,5,8]],"date-time":"2017-05-08T00:00:00Z","timestamp":1494201600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2017,5,8]],"date-time":"2017-05-08T00:00:00Z","timestamp":1494201600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Visceral pleural invasion (VPI) has been known to be an adverse prognostic factor in non-small cell lung cancer (NSCLC). However, the prognostic significance of extent of VPI (PL0, PL1 and PL2) remains controversial. We conduct a meta-analysis to summarize available evidence on this topic. PubMed, EMBASE, OVID and The Cochrane Library were searched for published studies from inception to May 9, 2016. A total of 16 studies were included in meta-analysis. Our results showed that patients with PL1 or PL2 had poorer overall survival compared with PL0 (HR\u2009=\u20091.555, 95% CI 1.399, 1.730; HR\u2009=\u20092.447, 95% CI 1.913, 3.130) and patients with PL2 had even poorer overall survival than PL1 (HR\u2009=\u20091.287, 95% CI 1.114, 1.487). Patients with PL1 or PL2 had lower 5-year survival rate than PL0 patients (OR\u2009=\u20090.515, 95% CI 0.415, 0.640; OR\u2009=\u20090.441, 95% CI 0.336, 0.579) and patients with PL2 had even lower 5-year survival rate than PL1 (OR\u2009=\u20090.706, 95% CI 0.545, 0.915). In conclusion, extent of VPI impacts the prognosis of resected NSCLC and VPI should be categorized as PL1 and PL2 in the terms of clinical practice and trials.<\/jats:p>","DOI":"10.1038\/s41598-017-01845-7","type":"journal-article","created":{"date-parts":[[2017,5,2]],"date-time":"2017-05-02T09:54:11Z","timestamp":1493718851000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":23,"title":["Extent of Visceral Pleural Invasion Affects Prognosis of Resected Non-small Cell Lung Cancer: A meta-analysis"],"prefix":"10.1038","volume":"7","author":[{"given":"Ting","family":"Wang","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chengya","family":"Zhou","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qinghua","family":"Zhou","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2017,5,8]]},"reference":[{"key":"1845_CR1","doi-asserted-by":"publisher","first-page":"593","DOI":"10.1097\/JTO.0b013e31807a2f81","volume":"2","author":"R Rami-Porta","year":"2007","unstructured":"Rami-Porta, R. et al. The IASLC Lung Cancer Staging Project: proposals for the revision of the T descriptors in the forthcoming (seventh) edition of the TNM classification for lung cancer. J Thorac Oncol \n                           2, 593\u2013602, doi:10.1097\/JTO.0b013e31807a2f81 (2007).","journal-title":"J Thorac Oncol"},{"key":"1845_CR2","doi-asserted-by":"publisher","first-page":"1710","DOI":"10.1378\/chest.111.6.1710","volume":"111","author":"CF Mountain","year":"1997","unstructured":"Mountain, C. F. Revisions in the International System for Staging Lung Cancer. Chest \n                           111, 1710\u20131717, doi:10.1378\/chest.111.6.1710 (1997).","journal-title":"Chest"},{"key":"1845_CR3","doi-asserted-by":"publisher","first-page":"706","DOI":"10.1097\/JTO.0b013e31812f3c1a","volume":"2","author":"P Goldstraw","year":"2007","unstructured":"Goldstraw, P. et al. The IASLC Lung Cancer Staging Project: proposals for the revision of the TNM stage groupings in the forthcoming (seventh) edition of the TNM Classification of malignant tumours. J Thorac Oncol \n                           2, 706\u2013714, doi:10.1097\/JTO.0b013e31812f3c1a (2007).","journal-title":"J Thorac Oncol"},{"key":"1845_CR4","doi-asserted-by":"publisher","first-page":"1384","DOI":"10.1097\/JTO.0b013e31818e0d9f","volume":"3","author":"WD Travis","year":"2008","unstructured":"Travis, W. D. et al. 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 \n                           3, 1384\u20131390, doi:10.1097\/JTO.0b013e31818e0d9f (2008).","journal-title":"J Thorac Oncol"},{"key":"1845_CR5","doi-asserted-by":"publisher","unstructured":"David, E. et al. Visceral pleural invasion is not predictive of survival in patients with lung cancer and smaller tumor size. Ann Thorac Surg \n                           95, 1872\u20131877, discussion 1877, doi:10.1016\/j.athoracsur.2013.03.085 (2013).","DOI":"10.1016\/j.athoracsur.2013.03.085"},{"key":"1845_CR6","doi-asserted-by":"publisher","first-page":"433","DOI":"10.1016\/j.athoracsur.2014.04.084","volume":"98","author":"A Hattori","year":"2014","unstructured":"Hattori, A., Suzuki, K., Matsunaga, T., Takamochi, K. & Oh, S. Visceral pleural invasion is not a significant prognostic factor in patients with a part-solid lung cancer. Ann Thorac Surg \n                           98, 433\u2013438, doi:10.1016\/j.athoracsur.2014.04.084 (2014).","journal-title":"Ann Thorac Surg"},{"key":"1845_CR7","doi-asserted-by":"publisher","first-page":"259","DOI":"10.1016\/j.lungcan.2012.09.010","volume":"78","author":"JJ Fibla","year":"2012","unstructured":"Fibla, J. J. et al. Re-evaluation of the prognostic value of visceral pleura invasion in Stage IB non-small cell lung cancer using the prospective multicenter ACOSOG Z0030 trial data set. Lung Cancer \n                           78, 259\u2013262, doi:10.1016\/j.lungcan.2012.09.010 (2012).","journal-title":"Lung Cancer"},{"key":"1845_CR8","doi-asserted-by":"publisher","first-page":"5905","DOI":"10.1007\/s13277-014-1781-8","volume":"35","author":"X Fan","year":"2014","unstructured":"Fan, X., Zhang, X., Wang, H. & Jin, B. Reevaluation of survival and prognostic factors in pathologic stage I lung adenocarcinoma by the new 2009 TNM classification. Tumour Biol \n                           35, 5905\u20135910, doi:10.1007\/s13277-014-1781-8 (2014).","journal-title":"Tumour Biol"},{"key":"1845_CR9","doi-asserted-by":"publisher","first-page":"206","DOI":"10.3779\/j.issn.1009-3419.2010.03.04","volume":"13","author":"Z Hu","year":"2010","unstructured":"Hu, Z., Shen-Tu, Y., Ding, Z., Tan, Q. & Zhou, Y. Study on the prognosis of the T1a non-small cell lung cancer. Zhongguo Fei Ai Za Zhi \n                           13, 206\u2013210, doi:10.3779\/j.issn.1009-3419.2010.03.04 (2010).","journal-title":"Zhongguo Fei Ai Za Zhi"},{"key":"1845_CR10","doi-asserted-by":"publisher","first-page":"808","DOI":"10.1097\/JTO.0b013e31814617c7","volume":"2","author":"N Kobayashi","year":"2007","unstructured":"Kobayashi, N. et al. Risk factors for recurrence and unfavorable prognosis in patients with stage I non-small cell lung cancer and a tumor diameter of 20\u2009mm or less. J Thorac Oncol \n                           2, 808\u2013812, doi:10.1097\/JTO.0b013e31814617c7 (2007).","journal-title":"J Thorac Oncol"},{"key":"1845_CR11","doi-asserted-by":"publisher","first-page":"3057","DOI":"10.1245\/s10434-012-2354-y","volume":"19","author":"YL Chang","year":"2012","unstructured":"Chang, Y. L., Lin, M. W., Shih, J. Y., Wu, C. T. & Lee, Y. C. The significance of visceral pleural surface invasion in 321 cases of non-small cell lung cancers with pleural retraction. Ann Surg Oncol \n                           19, 3057\u20133064, doi:10.1245\/s10434-012-2354-y (2012).","journal-title":"Ann Surg Oncol"},{"key":"1845_CR12","doi-asserted-by":"publisher","first-page":"141","DOI":"10.1378\/chest.11-2552","volume":"142","author":"JJ Hung","year":"2012","unstructured":"Hung, J. J. et al. Prognostic significance of the extent of visceral pleural invasion in completely resected node-negative non-small cell lung cancer. Chest \n                           142, 141\u2013150, doi:10.1378\/chest.11-2552 (2012).","journal-title":"Chest"},{"key":"1845_CR13","doi-asserted-by":"publisher","first-page":"606","DOI":"10.1097\/JTO.0b013e31828632b8","volume":"8","author":"A Kawase","year":"2013","unstructured":"Kawase, A. et al. Visceral pleural invasion classification in non-small-cell lung cancer in the 7th edition of the tumor, node, metastasis classification for lung cancer: validation analysis based on a large-scale nationwide database. J Thorac Oncol \n                           8, 606\u2013611, doi:10.1097\/JTO.0b013e31828632b8 (2013).","journal-title":"J Thorac Oncol"},{"key":"1845_CR14","doi-asserted-by":"publisher","first-page":"153","DOI":"10.1016\/j.lungcan.2012.08.004","volume":"78","author":"Y Kudo","year":"2012","unstructured":"Kudo, Y. et al. Impact of visceral pleural invasion on the survival of patients with non-small cell lung cancer. Lung Cancer \n                           78, 153\u2013160, doi:10.1016\/j.lungcan.2012.08.004 (2012).","journal-title":"Lung Cancer"},{"key":"1845_CR15","doi-asserted-by":"publisher","first-page":"1084","DOI":"10.1016\/j.athoracsur.2008.04.117","volume":"86","author":"N Sakakura","year":"2008","unstructured":"Sakakura, N. et al. Subcategorization of lung cancer based on tumor size and degree of visceral pleural invasion. Ann Thorac Surg \n                           86, 1084\u20131090, doi:10.1016\/j.athoracsur.2008.04.117 (2008).","journal-title":"Ann Thorac Surg"},{"key":"1845_CR16","doi-asserted-by":"publisher","unstructured":"Adachi, H. et al. Influence of visceral pleural invasion on survival in completely resected non-small-cell lung cancer. Eur J Cardiothorac Surg \n                           48, 691\u2013697, discussion 697, doi:10.1093\/ejcts\/ezu515 (2015).","DOI":"10.1093\/ejcts\/ezu515"},{"key":"1845_CR17","doi-asserted-by":"publisher","first-page":"426","DOI":"10.1016\/j.jtcvs.2008.12.035","volume":"138","author":"CP Hsu","year":"2009","unstructured":"Hsu, C. P. et al. Surgical-pathologic factors affect long-term outcomes in stage IB (pT2 N0 M0) non-small cell lung cancer: a heterogeneous disease. J Thorac Cardiovasc Surg \n                           138, 426\u2013433, doi:10.1016\/j.jtcvs.2008.12.035 (2009).","journal-title":"J Thorac Cardiovasc Surg"},{"key":"1845_CR18","doi-asserted-by":"publisher","first-page":"1784","DOI":"10.1097\/JTO.0b013e3181eedd9c","volume":"5","author":"A Kawase","year":"2010","unstructured":"Kawase, A. et al. Visceral pleural invasion classification in non-small cell lung cancer. J Thorac Oncol \n                           5, 1784\u20131788, doi:10.1097\/JTO.0b013e3181eedd9c (2010).","journal-title":"J Thorac Oncol"},{"key":"1845_CR19","doi-asserted-by":"publisher","first-page":"1622","DOI":"10.1378\/chest.13-0394","volume":"144","author":"J Nitadori","year":"2013","unstructured":"Nitadori, J. et al. Visceral pleural invasion does not affect recurrence or overall survival among patients with lung adenocarcinoma <\/=2\u2009cm: a proposal to reclassify T1 lung adenocarcinoma. Chest \n                           144, 1622\u20131631, doi:10.1378\/chest.13-0394 (2013).","journal-title":"Chest"},{"key":"1845_CR20","doi-asserted-by":"publisher","unstructured":"Osaki, T., Nagashima, A., Yoshimatsu, T., Yamada, S. & Yasumoto, K. Visceral pleural involvement in nonsmall cell lung cancer: prognostic significance. Ann Thorac Surg \n                           77, 1769\u20131773, discussion 1773, doi:10.1016\/j.athoracsur.2003.10.058 (2004).","DOI":"10.1016\/j.athoracsur.2003.10.058"},{"key":"1845_CR21","doi-asserted-by":"publisher","first-page":"540","DOI":"10.1093\/jjco\/hyt039","volume":"43","author":"M Oyama","year":"2013","unstructured":"Oyama, M. et al. Prognostic impact of pleural invasion in 1488 patients with surgically resected non-small cell lung carcinoma. Jpn J Clin Oncol \n                           43, 540\u2013546, doi:10.1093\/jjco\/hyt039 (2013).","journal-title":"Jpn J Clin Oncol"},{"key":"1845_CR22","doi-asserted-by":"publisher","first-page":"161","DOI":"10.1016\/j.lungcan.2008.11.008","volume":"65","author":"HS Shim","year":"2009","unstructured":"Shim, H. S., Park, I. K., Lee, C. Y. & Chung, K. Y. Prognostic significance of visceral pleural invasion in the forthcoming (seventh) edition of TNM classification for lung cancer. Lung Cancer \n                           65, 161\u2013165, doi:10.1016\/j.lungcan.2008.11.008 (2009).","journal-title":"Lung Cancer"},{"key":"1845_CR23","doi-asserted-by":"publisher","first-page":"1574","DOI":"10.1016\/j.jtcvs.2003.11.017","volume":"127","author":"K Shimizu","year":"2004","unstructured":"Shimizu, K. et al. Visceral pleural invasion classification in non-small cell lung cancer: a proposal on the basis of outcome assessment. J Thorac Cardiovasc Surg \n                           127, 1574\u20131578, doi:10.1016\/j.jtcvs.2003.11.017 (2004).","journal-title":"J Thorac Cardiovasc Surg"},{"key":"1845_CR24","doi-asserted-by":"publisher","first-page":"664","DOI":"10.1016\/j.ejcts.2010.12.059","volume":"40","author":"A Yilmaz","year":"2011","unstructured":"Yilmaz, A. et al. Clinical impact of visceral pleural, lymphovascular and perineural invasion in completely resected non-small cell lung cancer. Eur J Cardiothorac Surg \n                           40, 664\u2013670, doi:10.1016\/j.ejcts.2010.12.059 (2011).","journal-title":"Eur J Cardiothorac Surg"},{"key":"1845_CR25","doi-asserted-by":"publisher","first-page":"1130","DOI":"10.1016\/j.athoracsur.2014.11.052","volume":"99","author":"H Huang","year":"2015","unstructured":"Huang, H., Wang, T., Hu, B. & Pan, C. Visceral pleural invasion remains a size-independent prognostic factor in stage I non-small cell lung cancer. Ann Thorac Surg \n                           99, 1130\u20131139, doi:10.1016\/j.athoracsur.2014.11.052 (2015).","journal-title":"Ann Thorac Surg"},{"key":"1845_CR26","doi-asserted-by":"publisher","first-page":"603","DOI":"10.1007\/s10654-010-9491-z","volume":"25","author":"A Stang","year":"2010","unstructured":"Stang, A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol \n                           25, 603\u2013605, doi:10.1007\/s10654-010-9491-z (2010).","journal-title":"Eur J Epidemiol"},{"key":"1845_CR27","doi-asserted-by":"publisher","first-page":"16","DOI":"10.1186\/1745-6215-8-16","volume":"8","author":"JF Tierney","year":"2007","unstructured":"Tierney, J. F., Stewart, L. A., Ghersi, D., Burdett, S. & Sydes, M. R. Practical methods for incorporating summary time-to-event data into meta-analysis. Trials \n                           8, 16, doi:10.1186\/1745-6215-8-16 (2007).","journal-title":"Trials"},{"key":"1845_CR28","doi-asserted-by":"publisher","first-page":"1539","DOI":"10.1002\/sim.1186","volume":"21","author":"JP Higgins","year":"2002","unstructured":"Higgins, J. P. & Thompson, S. G. Quantifying heterogeneity in a meta-analysis. Stat Med \n                           21, 1539\u20131558, doi:10.1002\/sim.1186 (2002).","journal-title":"Stat Med"},{"key":"1845_CR29","doi-asserted-by":"publisher","first-page":"177","DOI":"10.1016\/0197-2456(86)90046-2","volume":"7","author":"R DerSimonian","year":"1986","unstructured":"DerSimonian, R. & Laird, N. Meta-analysis in clinical trials. Control Clin Trials \n                           7, 177\u2013188, doi:10.1016\/0197-2456(86)90046-2 (1986).","journal-title":"Control Clin Trials"},{"key":"1845_CR30","doi-asserted-by":"publisher","first-page":"1088","DOI":"10.2307\/2533446","volume":"50","author":"CB Begg","year":"1994","unstructured":"Begg, C. B. & Mazumdar, M. Operating characteristics of a rank correlation test for publication bias. Biometrics \n                           50, 1088\u20131101, doi:10.2307\/2533446 (1994).","journal-title":"Biometrics"},{"key":"1845_CR31","doi-asserted-by":"publisher","first-page":"1079","DOI":"10.1097\/SLA.0b013e31828920c0","volume":"258","author":"JJ Hung","year":"2013","unstructured":"Hung, J. J. et al. Prognostic value of the new International Association for the Study of Lung Cancer\/American Thoracic Society\/European Respiratory Society lung adenocarcinoma classification on death and recurrence in completely resected stage I lung adenocarcinoma. Ann Surg \n                           258, 1079\u20131086, doi:10.1097\/SLA.0b013e31828920c0 (2013).","journal-title":"Ann Surg"},{"key":"1845_CR32","doi-asserted-by":"publisher","first-page":"1020","DOI":"10.1158\/1078-0432.CCR-13-1862","volume":"20","author":"SS Kachala","year":"2014","unstructured":"Kachala, S. S. et al. Mesothelin overexpression is a marker of tumor aggressiveness and is associated with reduced recurrence-free and overall survival in early-stage lung adenocarcinoma. Clin Cancer Res \n                           20, 1020\u20131028, doi:10.1158\/1078-0432.CCR-13-1862 (2014).","journal-title":"Clin Cancer Res"},{"key":"1845_CR33","doi-asserted-by":"publisher","first-page":"1149","DOI":"10.1001\/jama.1958.02990100037007","volume":"166","author":"LA Brewer","year":"1958","unstructured":"Brewer, L. A., Bai, A. F., Little, J. N. & Rabago, Y. P. G. Carcinoma of the lung; practical classification for early diagnosis and surgical treatment. J Am Med Assoc \n                           166, 1149\u20131155, doi:10.1001\/jama.1958.02990100037007 (1958).","journal-title":"J Am Med Assoc"},{"key":"1845_CR34","doi-asserted-by":"publisher","first-page":"903","DOI":"10.1378\/chest.14-2765","volume":"148","author":"L Jiang","year":"2015","unstructured":"Jiang, L. et al. The impact of visceral pleural invasion in node-negative non-small cell lung cancer: a systematic review and meta-analysis. Chest \n                           148, 903\u2013911, doi:10.1378\/chest.14-2765 (2015).","journal-title":"Chest"},{"key":"1845_CR35","doi-asserted-by":"publisher","first-page":"990","DOI":"10.1097\/JTO.0000000000000559","volume":"10","author":"R Rami-Porta","year":"2015","unstructured":"Rami-Porta, R. et al. The IASLC Lung Cancer Staging Project: Proposals for the Revisions of the T Descriptors in the Forthcoming Eighth Edition of the TNM Classification for Lung Cancer. J Thorac Oncol \n                           10, 990\u20131003, doi:10.1097\/JTO.0000000000000559 (2015).","journal-title":"J Thorac Oncol"},{"key":"1845_CR36","doi-asserted-by":"crossref","first-page":"1092","DOI":"10.1016\/S0022-5223(19)33983-2","volume":"106","author":"H Kondo","year":"1993","unstructured":"Kondo, H. et al. Prognostic significance of pleural lavage cytology immediately after thoracotomy in patients with lung cancer. J Thorac Cardiovasc Surg \n                           106, 1092\u20131097 (1993).","journal-title":"J Thorac Cardiovasc Surg"},{"key":"1845_CR37","doi-asserted-by":"publisher","first-page":"777","DOI":"10.1093\/ajcp\/112.6.777","volume":"112","author":"ML Bunker","year":"1999","unstructured":"Bunker, M. L., Raab, S. S., Landreneau, R. J. & Silverman, J. F. The diagnosis and significance of visceral pleural invasion in lung carcinoma. Histologic predictors and the role of elastic stains. Am J Clin Pathol \n                           112, 777\u2013783, doi:10.1093\/ajcp\/112.6.777 (1999).","journal-title":"Am J Clin Pathol"}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-017-01845-7.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-017-01845-7","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-017-01845-7.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,12,23]],"date-time":"2022-12-23T04:01:03Z","timestamp":1671768063000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-017-01845-7"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2017,5,8]]},"references-count":37,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2017,12]]}},"alternative-id":["1845"],"URL":"https:\/\/doi.org\/10.1038\/s41598-017-01845-7","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2017,5,8]]},"assertion":[{"value":"1 August 2016","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"4 April 2017","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"8 May 2017","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare that they have no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing Interests"}}],"article-number":"1527"}}