{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,15]],"date-time":"2026-01-15T23:17:19Z","timestamp":1768519039810,"version":"3.49.0"},"reference-count":26,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2024,1,1]],"date-time":"2024-01-01T00:00:00Z","timestamp":1704067200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2024,1,16]],"date-time":"2024-01-16T00:00:00Z","timestamp":1705363200000},"content-version":"vor","delay-in-days":15,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"name":"National Key Research Project of China","award":["2017YFC0113502"],"award-info":[{"award-number":["2017YFC0113502"]}]},{"name":"Key Research Project of Sichuan Province","award":["2020YFS0249"],"award-info":[{"award-number":["2020YFS0249"]}]},{"name":"1\u00b73\u00b75 project for disciplines of excellence\u2013Clinical Research Incubation Project, West China Hospital, Sichuan University","award":["2021HXFH056"],"award-info":[{"award-number":["2021HXFH056"]}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["J Cancer Res Clin Oncol"],"published-print":{"date-parts":[[2024,1]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:sec>\n                <jats:title>Objectives<\/jats:title>\n                <jats:p>Thymic carcinoma and thymic neuroendocrine tumor (NET) are rare and are more likely to develop second malignancies. The purpose of this study was to explore the incidence and lifetime risk of second malignancies in thymic carcinoma and thymic NET.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Methods<\/jats:title>\n                <jats:p>The standardized incidence ratio (SIR) and the age-adjusted cancer incidence of the thymic carcinoma and thymic NET patients with second malignancies were retrospectively calculated by using the Surveillance, Epidemiology, and End Results (SEER) database. Prognosis results were also determined by Kaplan\u2013Meier analysis and Cox regression.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Results<\/jats:title>\n                <jats:p>1130 patients with thymic carcinoma (73 patients had second malignancies) and 263 patients with thymic NET (19 patients had second malignancies) from 2000 to 2018 are included. Patients with thymic carcinoma (SIR: 1.36, 95% CI 1.08\u20131.69) and with thymic NET (SIR: 1.73, 95% CI 1.13\u20132.54) demonstrate an increased overall risk of developing second malignancies in various organ systems. The age-adjusted cancer incidence of second malignancies in patients with thymic carcinoma is 3058.48 per 100,000 persons (4178.46 per 100,000 persons in patients with thymic NET). Age at diagnosis is a significant risk factor for the development of second malignancies.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Conclusion<\/jats:title>\n                <jats:p>The incidence of second malignancies in patients with thymic carcinoma and thymic NET is significantly higher than the patients in the normal population. The occurrence of second malignancies is not related to the use of different treatments. It is important to extend the follow-up period and add other screening methods.<\/jats:p>\n              <\/jats:sec>","DOI":"10.1007\/s00432-023-05522-3","type":"journal-article","created":{"date-parts":[[2024,1,16]],"date-time":"2024-01-16T14:02:22Z","timestamp":1705413742000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":2,"title":["Incidence of second malignancies in patients with thymic carcinoma and thymic neuroendocrine tumor"],"prefix":"10.1007","volume":"150","author":[{"given":"Guanghao","family":"Qiu","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Fuqiang","family":"Wang","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yun","family":"Wang","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2024,1,16]]},"reference":[{"issue":"95\u2013100","key":"5522_CR1","doi-asserted-by":"publisher","first-page":"101.e1","DOI":"10.1016\/j.jtcvs.2014.09.124","volume":"149","author":"U Ahmad","year":"2015","unstructured":"Ahmad U, Yao X, Detterbeck F et al (2015) Thymic carcinoma outcomes and prognosis: results of an international analysis. J Thorac Cardiovasc Surg 149(95\u2013100):101.e1\u20132. https:\/\/doi.org\/10.1016\/j.jtcvs.2014.09.124","journal-title":"J Thorac Cardiovasc Surg"},{"key":"5522_CR2","doi-asserted-by":"publisher","first-page":"2472","DOI":"10.3390\/cancers13102472","volume":"13","author":"SS Badve","year":"2021","unstructured":"Badve SS, Dougherty R, Balatico M et al (2021) Thymic carcinomas and second malignancies: a single-center review. Cancers (basel) 13:2472. https:\/\/doi.org\/10.3390\/cancers13102472","journal-title":"Cancers (basel)"},{"key":"5522_CR3","doi-asserted-by":"publisher","first-page":"110","DOI":"10.1002\/ssu.2980060209","volume":"6","author":"MM Couture","year":"1990","unstructured":"Couture MM, Mountain CF (1990) Thymoma. Semin Surg Oncol 6:110\u2013114. https:\/\/doi.org\/10.1002\/ssu.2980060209","journal-title":"Semin Surg Oncol"},{"key":"5522_CR4","doi-asserted-by":"publisher","first-page":"123","DOI":"10.1016\/j.ejca.2007.11.004","volume":"44","author":"WK de Jong","year":"2008","unstructured":"de Jong WK, Blaauwgeers JLG, Schaapveld M et al (2008) Thymic epithelial tumours: a population-based study of the incidence, diagnostic procedures and therapy. Eur J Cancer 44:123\u2013130. https:\/\/doi.org\/10.1016\/j.ejca.2007.11.004","journal-title":"Eur J Cancer"},{"key":"5522_CR5","doi-asserted-by":"publisher","first-page":"S260","DOI":"10.1097\/JTO.0b013e3181f1f62d","volume":"5","author":"EA Engels","year":"2010","unstructured":"Engels EA (2010) Epidemiology of thymoma and associated malignancies. J Thorac Oncol 5:S260-265. https:\/\/doi.org\/10.1097\/JTO.0b013e3181f1f62d","journal-title":"J Thorac Oncol"},{"key":"5522_CR6","doi-asserted-by":"publisher","first-page":"692","DOI":"10.1093\/annonc\/mdh155","volume":"15","author":"A Evoli","year":"2004","unstructured":"Evoli A, Punzi C, Marsili F et al (2004) Extrathymic malignancies in patients with thymoma. Ann Oncol 15:692\u2013693. https:\/\/doi.org\/10.1093\/annonc\/mdh155","journal-title":"Ann Oncol"},{"key":"5522_CR7","doi-asserted-by":"publisher","first-page":"2603","DOI":"10.1210\/jc.2004-1155","volume":"90","author":"P Ferolla","year":"2005","unstructured":"Ferolla P, Falchetti A, Filosso P et al (2005) Thymic neuroendocrine carcinoma (carcinoid) in multiple endocrine neoplasia type 1 syndrome: the Italian series. J Clin Endocrinol Metab 90:2603\u20132609. https:\/\/doi.org\/10.1210\/jc.2004-1155","journal-title":"J Clin Endocrinol Metab"},{"key":"5522_CR8","doi-asserted-by":"publisher","first-page":"219","DOI":"10.1093\/ejcts\/ezs663","volume":"44","author":"PL Filosso","year":"2013","unstructured":"Filosso PL, Galassi C, Ruffini E et al (2013) Thymoma and the increased risk of developing extrathymic malignancies: a multicentre study. Eur J Cardiothorac Surg 44:219\u2013224. https:\/\/doi.org\/10.1093\/ejcts\/ezs663. (discussion 224)","journal-title":"Eur J Cardiothorac Surg"},{"key":"5522_CR9","doi-asserted-by":"publisher","first-page":"1117","DOI":"10.1097\/SLA.0b013e3181dd4ec4","volume":"251","author":"P Gaur","year":"2010","unstructured":"Gaur P, Leary C, Yao JC (2010) Thymic neuroendocrine tumors: a SEER database analysis of 160 patients. Ann Surg 251:1117\u20131121. https:\/\/doi.org\/10.1097\/SLA.0b013e3181dd4ec4","journal-title":"Ann Surg"},{"key":"5522_CR10","doi-asserted-by":"publisher","first-page":"235","DOI":"10.1097\/00000478-197906000-00006","volume":"3","author":"GF Gray","year":"1979","unstructured":"Gray GF, Gutowski WT (1979) Thymoma. A clinicopathologic study of 54 cases. Am J Surg Pathol 3:235\u2013249","journal-title":"Am J Surg Pathol"},{"key":"5522_CR11","doi-asserted-by":"publisher","first-page":"290","DOI":"10.1177\/0218492318765872","volume":"26","author":"M Hamaji","year":"2018","unstructured":"Hamaji M, Sozu T, Machida R et al (2018) Second malignancy versus recurrence after complete resection of thymoma. Asian Cardiovasc Thorac Ann 26:290\u2013295. https:\/\/doi.org\/10.1177\/0218492318765872","journal-title":"Asian Cardiovasc Thorac Ann"},{"key":"5522_CR12","doi-asserted-by":"publisher","first-page":"375","DOI":"10.1093\/icvts\/ivy260","volume":"28","author":"M Hamaji","year":"2019","unstructured":"Hamaji M, Kawaguchi A, Omasa M et al (2019a) Low incidence of and mortality from a second malignancy after resection of thymic carcinoma\u2020. Interact Cardiovasc Thorac Surg 28:375\u2013379. https:\/\/doi.org\/10.1093\/icvts\/ivy260","journal-title":"Interact Cardiovasc Thorac Surg"},{"key":"5522_CR13","doi-asserted-by":"publisher","first-page":"729","DOI":"10.1093\/icvts\/ivz177","volume":"29","author":"M Hamaji","year":"2019","unstructured":"Hamaji M, Sozu T, Machida R et al (2019b) Mortality from extrathymic malignancy after thymic tumour resections: incidences and risk factors. Interact Cardiovasc Thorac Surg 29:729\u2013736. https:\/\/doi.org\/10.1093\/icvts\/ivz177","journal-title":"Interact Cardiovasc Thorac Surg"},{"key":"5522_CR14","doi-asserted-by":"publisher","first-page":"576","DOI":"10.1093\/icvts\/ivw354","volume":"24","author":"T Kamata","year":"2017","unstructured":"Kamata T, Yoshida S, Wada H et al (2017) Extrathymic malignancies associated with thymoma: a forty-year experience at a single institution. Interact Cardiovasc Thorac Surg 24:576\u2013581. https:\/\/doi.org\/10.1093\/icvts\/ivw354","journal-title":"Interact Cardiovasc Thorac Surg"},{"key":"5522_CR15","doi-asserted-by":"publisher","first-page":"406","DOI":"10.1056\/NEJMoa2302892","volume":"389","author":"KA Kooshesh","year":"2023","unstructured":"Kooshesh KA, Foy BH, Sykes DB et al (2023) Health consequences of thymus removal in adults. N Engl J Med 389:406\u2013417. https:\/\/doi.org\/10.1056\/NEJMoa2302892","journal-title":"N Engl J Med"},{"key":"5522_CR16","doi-asserted-by":"publisher","first-page":"2142","DOI":"10.1002\/1097-0142(197705)39:5<2142::aid-cncr2820390531>3.0.co;2-q","volume":"39","author":"DP LeGolvan","year":"1977","unstructured":"LeGolvan DP, Abell MR (1977) Thymomas. Cancer 39:2142\u20132157. https:\/\/doi.org\/10.1002\/1097-0142(197705)39:5%3c2142::aid-cncr2820390531%3e3.0.co;2-q","journal-title":"Cancer"},{"key":"5522_CR17","doi-asserted-by":"publisher","first-page":"2727","DOI":"10.1002\/1097-0142(19871201)60:11<2727::aid-cncr2820601125>3.0.co;2-d","volume":"60","author":"JE Lewis","year":"1987","unstructured":"Lewis JE, Wick MR, Scheithauer BW et al (1987) Thymoma. A clinicopathologic review. Cancer 60:2727\u20132743. https:\/\/doi.org\/10.1002\/1097-0142(19871201)60:11%3c2727::aid-cncr2820601125%3e3.0.co;2-d","journal-title":"Cancer"},{"key":"5522_CR18","unstructured":"Oncology NCPGi (2017) Thymomas and thymic carcinomas"},{"key":"5522_CR19","doi-asserted-by":"publisher","first-page":"66","DOI":"10.1016\/j.jns.2009.11.006","volume":"290","author":"JF Owe","year":"2010","unstructured":"Owe JF, Cvancarova M, Romi F, Gilhus NE (2010) Extrathymic malignancies in thymoma patients with and without myasthenia gravis. J Neurol Sci 290:66\u201369. https:\/\/doi.org\/10.1016\/j.jns.2009.11.006","journal-title":"J Neurol Sci"},{"key":"5522_CR20","doi-asserted-by":"publisher","first-page":"2406","DOI":"10.1002\/1097-0142(20011101)92:9<2406::aid-cncr1589>3.0.co;2-7","volume":"92","author":"CC Pan","year":"2001","unstructured":"Pan CC, Chen PC, Wang LS et al (2001) Thymoma is associated with an increased risk of second malignancy. Cancer 92:2406\u20132411. https:\/\/doi.org\/10.1002\/1097-0142(20011101)92:9%3c2406::aid-cncr1589%3e3.0.co;2-7","journal-title":"Cancer"},{"key":"5522_CR21","doi-asserted-by":"publisher","first-page":"949","DOI":"10.1016\/j.ejca.2012.02.047","volume":"48","author":"S Siesling","year":"2012","unstructured":"Siesling S, van der Zwan JM, Izarzugaza I et al (2012) Rare thoracic cancers, including peritoneum mesothelioma. Eur J Cancer 48:949\u2013960. https:\/\/doi.org\/10.1016\/j.ejca.2012.02.047","journal-title":"Eur J Cancer"},{"key":"5522_CR22","doi-asserted-by":"publisher","first-page":"13","DOI":"10.1016\/j.ejcts.2009.05.038","volume":"37","author":"F Venuta","year":"2010","unstructured":"Venuta F, Anile M, Diso D et al (2010) Thymoma and thymic carcinoma. Eur J Cardiothorac Surg 37:13\u201325. https:\/\/doi.org\/10.1016\/j.ejcts.2009.05.038","journal-title":"Eur J Cardiothorac Surg"},{"key":"5522_CR23","doi-asserted-by":"publisher","first-page":"884","DOI":"10.1016\/j.athoracsur.2011.05.089","volume":"93","author":"B Weksler","year":"2012","unstructured":"Weksler B, Nason KS, Mackey D et al (2012) Thymomas and extrathymic cancers. Ann Thorac Surg 93:884\u2013888. https:\/\/doi.org\/10.1016\/j.athoracsur.2011.05.089","journal-title":"Ann Thorac Surg"},{"key":"5522_CR24","doi-asserted-by":"publisher","first-page":"1142","DOI":"10.1001\/jama.283.9.1142","volume":"283","author":"JS Welsh","year":"2000","unstructured":"Welsh JS, Wilkins KB, Green R et al (2000) Association between thymoma and second neoplasms. JAMA 283:1142\u20131143. https:\/\/doi.org\/10.1001\/jama.283.9.1142","journal-title":"JAMA"},{"key":"5522_CR25","doi-asserted-by":"publisher","first-page":"562","DOI":"10.1097\/00000658-199910000-00012","volume":"230","author":"KB Wilkins","year":"1999","unstructured":"Wilkins KB, Sheikh E, Green R et al (1999) Clinical and pathologic predictors of survival in patients with thymoma. Ann Surg 230:562\u2013572. https:\/\/doi.org\/10.1097\/00000658-199910000-00012. (discussion 572-574)","journal-title":"Ann Surg"},{"key":"5522_CR26","doi-asserted-by":"publisher","first-page":"219","DOI":"10.1016\/j.athoracsur.2010.09.025","volume":"91","author":"Y-T Yen","year":"2011","unstructured":"Yen Y-T, Lai W-W, Wu M-H et al (2011) Thymic neuroendocrine carcinoma and thymoma are both associated with increased risk of extrathymic malignancy: a 20-year review of a single institution. Ann Thorac Surg 91:219\u2013225. https:\/\/doi.org\/10.1016\/j.athoracsur.2010.09.025","journal-title":"Ann Thorac Surg"}],"container-title":["Journal of Cancer Research and Clinical Oncology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s00432-023-05522-3.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1007\/s00432-023-05522-3\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s00432-023-05522-3.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,2,8]],"date-time":"2024-02-08T13:05:31Z","timestamp":1707397531000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1007\/s00432-023-05522-3"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,1]]},"references-count":26,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2024,1]]}},"alternative-id":["5522"],"URL":"https:\/\/doi.org\/10.1007\/s00432-023-05522-3","relation":{},"ISSN":["0171-5216","1432-1335"],"issn-type":[{"value":"0171-5216","type":"print"},{"value":"1432-1335","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,1]]},"assertion":[{"value":"8 October 2023","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"13 November 2023","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"16 January 2024","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"All authors report this study was supported by grants from the National Key Research Project of China (no. 2017YFC0113502), Key Research Project of Sichuan Province (no. 2020YFS0249) and 1\u00b73\u00b75 project for disciplines of excellence\u2013Clinical Research Incubation Project, West China Hospital, Sichuan University (2021HXFH056). The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Conflict of interest"}},{"value":"This study was approved by the Ethics Committee of West China Hospital (2021-385). Patient consent is not required because the data are sourced from the SEER database.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics statement"}},{"value":"Not applicable.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent to publish"}}],"article-number":"11"}}