Progress in diagnosis and treatment of thymic neuroendocrine tumors_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

ZHANG Jiaqi , CHEN Yeye , ZHOU Mengxin , HUANG Cheng , ZHANG Ye , GUO Chao ,  LI Shanqing

Department of Thoracic Surgery, Peking Union Medical College Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, 100730, P. R. China;

Corresponding author：

LI Shanqing, Email: lishanqing@pumch.cn

Keywords：

Thymus; neuroendocrine tumors; progress; review

DOI：

10.7507/1007-4848.202011013

Video：

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Abstract Full text Figures/Tables Video References Cited by

Thymic neuroendocrine tumors (TNETs) are a series of rare diseases with aggressive biology and poor prognosis. Clinical manifestations of TNETs are atypical, and ectopic secretion of adrenocorticotropic hormone can be found in some cases, resulting in associated endocrine symptoms. Due to the low morbidity and strong heterogeneity, it’s difficult to diagnose, treat and obtain new treatment regimen. Early complete surgical resection is an effective treatment. For advanced cancer, clinical trials of new drugs are expected to improve the survival of patients.

Citation： ZHANG Jiaqi, CHEN Yeye, ZHOU Mengxin, HUANG Cheng, ZHANG Ye, GUO Chao, LI Shanqing. Progress in diagnosis and treatment of thymic neuroendocrine tumors. Chinese Journal of Clinical Thoracic and Cardiovascular Surgery, 2022, 29(4): 488-496. doi: 10.7507/1007-4848.202011013 Copy

1.	Modlin IM, Shapiro MD, Kidd M. Siegfried oberndorfer: Origins and perspectives of carcinoid tumors. Hum Pathol, 2004, 35(12): 1440-1451.
2.	Klöppel G. Oberndorfer and his successors: From carcinoid to neuroendocrine carcinoma. Endocr Pathol, 2007, 18(3): 141-144.
3.	Uccella S, La Rosa S, Volante M, et al. Immunohistochemical biomarkers of gastrointestinal, pancreatic, pulmonary, and thymic neuroendocrine neoplasms. Endocr Pathol, 2018, 29(2): 150-168.
4.	Rosai J, Higa E. Mediastinal endocrine neoplasm, of probable thymic origin, related to carcinoid tumor. Clinicopathologic study of 8 cases. Cancer, 1972, 29(4): 1061-1074.
5.	Yao JC, Hassan M, Phan A, et al. One hundred years after "carcinoid": Epidemiology of and prognostic factors for neuroendocrine tumors in 35, 825 cases in the United States. J Clin Oncol, 2008, 26(18): 3063-3072.
6.	Phan AT, Oberg K, Choi J, et al. NANETS consensus guideline for the diagnosis and management of neuroendocrine tumors: Well-differentiated neuroendocrine tumors of the thorax (includes lung and thymus). Pancreas, 2010, 39(6): 784-798.
7.	Hsu C, Chan J K, Yin C, et al. Trends in the incidence of thymoma, thymic carcinoma, and thymic neuroendocrine tumor in the United States. PLoS One, 2019, 14(12): e227197.
8.	Filosso PL, Ruffini E, Solidoro P, et al. Neuroendocrine tumors of the thymus. J Thorac Dis, 2017, 9(Suppl 15): S1484-S1490.
9.	Gaur P, Leary C, Yao JC. Thymic neuroendocrine tumors: A SEER database analysis of 160 patients. Ann Surg, 2010, 251(6): 1117-1121.
10.	Chen YY, Li SQ, Liu HS, et al. Ectopic adrenocorticotropic hormone syndrome caused by neuroendocrine tumors of the thymus: 30-year experience with 16 patients at a single institute in the People's Republic of China. Onco Targets Ther, 2016, 9: 2193-2201.
11.	Neary NM, Lopez-Chavez A, Abel BS, et al. Neuroendocrine ACTH-producing tumor of the thymus—Experience with 12 patients over 25 years. J Clin Endocrinol Metab, 2012, 97(7): 2223-2230.
12.	Christakis I, Qiu W, Silva Figueroa AM, et al. Clinical features, treatments, and outcomes of patients with thymic carcinoids and multiple endocrine neoplasia type 1 syndrome at MD Anderson Cancer Center. Horm Cancer, 2016, 7(4): 279-287.
13.	Teh BT. Thymic carcinoids in multiple endocrine neoplasia type 1. J Intern Med, 1998, 243(6): 501-504.
14.	Filosso PL, Yao X, Ahmad U, et al. Outcome of primary neuroendocrine tumors of the thymus: A joint analysis of the International Thymic Malignancy Interest Group and the European Society of Thoracic Surgeons databases. J Thorac Cardiovasc Surg, 2015, 149(1): 103-109.
15.	Wu MH, Tseng YL, Cheng FF, et al. Thymic carcinoid combined with myasthenia gravis. J Thorac Cardiovasc Surg, 2004, 127(2): 584-585.
16.	Nakajima J, Okumura M, Yano M, et al. Myasthenia gravis with thymic epithelial tumour: A retrospective analysis of a Japanese database. Eur J Cardiothorac Surg, 2016, 49(5): 1510-1515.
17.	Bordin-Wosk T, Patel SP, Horman SF. GABAB R-mediated paraneoplastic limbic encephalitis due to thymic small cell carcinoma. J Gen Intern Med, 2019, 34(8): 1658-1661.
18.	Kamp K, Alwani RA, Korpershoek E, et al. Prevalence and clinical features of the ectopic ACTH syndrome in patients with gastroenteropancreatic and thoracic neuroendocrine tumors. Eur J Endocrinol, 2016, 174(3): 271-280.
19.	Alexandraki KI, Grossman AB. The ectopic ACTH syndrome. Rev Endocr Metab Disord, 2010, 11(2): 117-126.
20.	Araki T, Sholl LM, Hatabu H, et al. Radiological features and metastatic patterns of thymic neuroendocrine tumours. Clin Radiol, 2018, 73(5): 479-484.
21.	Zhao Y, Gu H, Fan L, et al. Comparison of clinical features and survival between thymic carcinoma and thymic carcinoid patients. Eur J Cardiothorac Surg, 2017, 52(1): 33-38.
22.	Li B, Xin YK, Xiao G, et al. Predicting pathological subtypes and stages of thymic epithelial tumors using DWI: Value of combining ADC and texture parameters. Eur Radiol, 2019, 29(10): 5330-5340.
23.	Weissferdt A, Moran CA. Neuroendocrine differentiation in thymic carcinomas: A diagnostic pitfall: An immunohistochemical analysis of 27 cases. Am J Clin Pathol, 2016, 145(3): 393-400.
24.	Marx A, Chan JKC, Chalabreysse L, et al. The 2021 WHO Classification of Tumors of the Thymus and Mediastinum: What Is New in Thymic Epithelial, Germ Cell, and Mesenchymal Tumors? J Thorac Oncol, 2022, 17(2): 200-213.
25.	Marx A, Chan JKC, Chalabreysse L, et al. The 2021 WHO classification of tumors of the thymus and mediastinum: What is new in thymic rpithelial, germ cell, and mesenchymal tumors? J Thorac Oncol, 2022, 17(2): 200-213.
26.	Cardillo G, Rea F, Lucchi M, et al. Primary neuroendocrine tumors of the thymus: A multicenter experience of 35 patients. Ann Thorac Surg, 2012, 94(1): 241-245.
27.	Masaoka A, Monden Y, Nakahara K, et al. Follow-up study of thymomas with special reference to their clinical stages. Cancer, 1981, 48(11): 2485-2492.
28.	Koga K, Matsuno Y, Noguchi M, et al. A review of 79 thymomas: Modification of staging system and reappraisal of conventional division into invasive and non-invasive thymoma. Pathol Int, 1994, 44(5): 359-367.
29.	Detterbeck FC, Nicholson AG, Kondo K, et al. The Masaoka-Koga stage classification for thymic malignancies: Clarification and definition of terms. J Thorac Oncol, 2011, 6(7 Suppl 3): S1710-1716.
30.	Detterbeck FC, Stratton K, Giroux D, et al. The IASLC/ITMIG Thymic Epithelial Tumors Staging Project: Proposal for an evidence-based stage classification system for the forthcoming (8th) edition of the TNM classification of malignant tumors. J Thorac Oncol, 2014, 9(9 Suppl 2): S65-S72.
31.	Meurgey A, Girard N, Merveilleux du Vignaux C, et al. Assessment of the ITMIG statement on the WHO histological classification and of the eighth TNM staging of thymic epithelial tumors of a series of 188 thymic epithelial tumors. J Thorac Oncol, 2017, 12(10): 1571-1581.
32.	Zhao Y, Shi J, Fan L, et al. Evaluation of the proposed International Association for the Study of Lung Cancer (IASLC)/International Thymic Malignancies Interest Group (ITMIG) staging revisions in thymic well-differentiated neuroendocrine carcinoma patients. Eur J Cardiothorac Surg, 2016, 49(2): 569-573.
33.	Dinter H, Bohnenberger H, Beck J, et al. Molecular classification of neuroendocrine tumors of the thymus. J Thorac Oncol, 2019, 14(8): 1472-1483.
34.	NCCN Clinical Practice Guidelines in Oncology (NCCN Guidelines®). Neuroendocrine and Adrenal Tumors, Version4.2021.https://www.nccn.org/guidelines/guidelines-detail?category=1&id=1448.Accessed on [2022-02-10].
35.	Bertolaccini L, Prisciandaro E, Galetta D, et al. Outcomes and safety analysis in superior vena cava resection for extended thymic epithelial tumors. Ann Thorac Surg, 2021, 112(1): 271-277.
36.	Mendogni P, Toker A, Moser B, et al. Surgical resection of Masaoka stage Ⅲ thymic epithelial tumours with great vessels involvement: A retrospective multicentric analysis from the European Society of Thoracic Surgeons thymic database. Eur J Cardiothorac Surg, 2022.
37.	Weksler B, Holden A, Sullivan JL. Impact of positive nodal metastases in patients with thymic carcinoma and thymic neuroendocrine tumors. J Thorac Oncol, 2015, 10(11): 1642-1647.
38.	Cheufou DH, Valdivia D, Puhlvers S, et al. Lymph node involvement and the surgical treatment of thymic epithelial and neuroendocrine carcinoma. Ann Thorac Surg, 2019, 107(6): 1632-1638.
39.	Fang W, Wang Y, Pang L, et al. Lymph node metastasis in thymic malignancies: A Chinese multicenter prospective observational study. J Thorac Cardiovasc Surg, 2018, 156(2): 824-833.
40.	Bian D, Qi M, Hu J, et al. The comparison of predictive factors regarding prognoses and invasion of thymic neuroendocrine tumors preoperatively and postoperatively. J Thorac Dis, 2018, 10(3): 1657-1669.
41.	Corsini EM, Mitchell KG, Sceusi EL, et al. Multidisciplinary treatment of thymic neuroendocrine tumors: surgery remains a key component. J Thorac Dis, 2019, 11(8): 3391-3398.
42.	Wen J, Chen J, Chen D, et al. Evaluation of the prognostic value of surgery and postoperative radiotherapy for patients with thymic neuroendocrine tumors: A propensity-matched study based on the SEER database. Thorac Cancer, 2018, 9(12): 1603-1613.
43.	Wang H, Yang Y, Fan X, et al. Thymic neuroendocrine tumors: An analysis of 18 cases and a literature review. Transl Cancer Res, 2016, 5(6): 789-796.
44.	Miyata R, Hamaji M, Omasa M, et al. The treatment and survival of patients with postoperative recurrent thymic carcinoma and neuroendocrine carcinoma: A multicenter retrospective study. Surg Today, 2020, 51(4): 502-510.
45.	Davi' MV, Cosaro E, Piacentini S, et al. Prognostic factors in ectopic Cushing's syndrome due to neuroendocrine tumors: Multicenter study. Eur J Endocrinol, 2017, 176(4): 453-461.
46.	Cho J, Kim HS, Ku BM, et al. Pembrolizumab for patients with refractory or relapsed thymic epithelial tumor: An open-label Phase Ⅱ trial. J Clin Oncol, 2019, 37(24): 2162-2170.
47.	Giaccone G, Kim C, Thompson J, et al. Pembrolizumab in patients with thymic carcinoma: A single-arm, single-centre, phase 2 study. Lancet Oncol, 2018, 19(3): 347-355.
48.	Yokoyama S, Miyoshi H. Thymic tumors and immune checkpoint inhibitors. J Thorac Dis, 2018, 10(Suppl 13): S1509-S1515.1509-1515.
49.	Filosso PL, Yao X, Ruffini E, et al. Comparison of outcomes between neuroendocrine thymic tumours and other subtypes of thymic carcinomas: A joint analysis of the European Society of Thoracic Surgeons and the International Thymic Malignancy Interest Group. Eur J Cardiothorac Surg, 2016, 50(4): 766-771.
50.	Liu H, Gu Z, Qiu B, et al. A Recurrence predictive model for thymic tumors and its implication for postoperative management: A Chinese alliance for research in thymomas database study. J Thorac Oncol, 2020, 15(3): 448-456.
51.	Song Q, Zhang LL, Qi Y, et al. Effect of clinicopathologic features on survival of patients with thymic carcinomas and thymic neuroendocrine tumors: A population-based analysis. Curr Probl Cancer, 2019, 43(5): 411-420.
52.	Ose N, Maeda H, Inoue M, et al. Results of treatment for thymic neuroendocrine tumours: Multicentre clinicopathological study. Interact Cardiovasc Thorac Surg, 2018, 26(1): 18-24.
53.	Hamaji M, Omasa M, Nakagawa T, et al. Survival outcomes of patients with high-grade and poorly differentiated thymic neuroendocrine carcinoma. Interact Cardiovasc Thorac Surg, 2020, 31(1): 98-101.
54.	Ma K, Liu Y, Xue Z, et al. Treatment, prognostic markers, and survival in thymic neuroendocrine tumors. Medicine (Baltimore), 2017, 96(43): e7842.
55.	Ströbel P, Zettl A, Shilo K, et al. Tumor genetics and survival of thymic neuroendocrine neoplasms: A multi-institutional clinicopathologic study. Genes Chromosomes Cancer, 2014, 53(9): 738-749.
56.	Ahn S, Lee JJ, Ha SY, et al. Clinicopathological analysis of 21 thymic neuroendocrine tumors. Korean J Pathol, 2012, 46(3): 221-225.
57.	Fang W, Filosso P L, Roden AC, et al. Clinicopathological features and current treatment outcomes of neuroendocrine thymic tumours. Eur J Cardio-Thorac Surg, 2021, 59(5): 1004-1013.

1. Modlin IM, Shapiro MD, Kidd M. Siegfried oberndorfer: Origins and perspectives of carcinoid tumors. Hum Pathol, 2004, 35(12): 1440-1451.
2. Klöppel G. Oberndorfer and his successors: From carcinoid to neuroendocrine carcinoma. Endocr Pathol, 2007, 18(3): 141-144.
3. Uccella S, La Rosa S, Volante M, et al. Immunohistochemical biomarkers of gastrointestinal, pancreatic, pulmonary, and thymic neuroendocrine neoplasms. Endocr Pathol, 2018, 29(2): 150-168.
4. Rosai J, Higa E. Mediastinal endocrine neoplasm, of probable thymic origin, related to carcinoid tumor. Clinicopathologic study of 8 cases. Cancer, 1972, 29(4): 1061-1074.
5. Yao JC, Hassan M, Phan A, et al. One hundred years after "carcinoid": Epidemiology of and prognostic factors for neuroendocrine tumors in 35, 825 cases in the United States. J Clin Oncol, 2008, 26(18): 3063-3072.
6. Phan AT, Oberg K, Choi J, et al. NANETS consensus guideline for the diagnosis and management of neuroendocrine tumors: Well-differentiated neuroendocrine tumors of the thorax (includes lung and thymus). Pancreas, 2010, 39(6): 784-798.
7. Hsu C, Chan J K, Yin C, et al. Trends in the incidence of thymoma, thymic carcinoma, and thymic neuroendocrine tumor in the United States. PLoS One, 2019, 14(12): e227197.
8. Filosso PL, Ruffini E, Solidoro P, et al. Neuroendocrine tumors of the thymus. J Thorac Dis, 2017, 9(Suppl 15): S1484-S1490.
9. Gaur P, Leary C, Yao JC. Thymic neuroendocrine tumors: A SEER database analysis of 160 patients. Ann Surg, 2010, 251(6): 1117-1121.
10. Chen YY, Li SQ, Liu HS, et al. Ectopic adrenocorticotropic hormone syndrome caused by neuroendocrine tumors of the thymus: 30-year experience with 16 patients at a single institute in the People's Republic of China. Onco Targets Ther, 2016, 9: 2193-2201.
11. Neary NM, Lopez-Chavez A, Abel BS, et al. Neuroendocrine ACTH-producing tumor of the thymus—Experience with 12 patients over 25 years. J Clin Endocrinol Metab, 2012, 97(7): 2223-2230.
12. Christakis I, Qiu W, Silva Figueroa AM, et al. Clinical features, treatments, and outcomes of patients with thymic carcinoids and multiple endocrine neoplasia type 1 syndrome at MD Anderson Cancer Center. Horm Cancer, 2016, 7(4): 279-287.
13. Teh BT. Thymic carcinoids in multiple endocrine neoplasia type 1. J Intern Med, 1998, 243(6): 501-504.
14. Filosso PL, Yao X, Ahmad U, et al. Outcome of primary neuroendocrine tumors of the thymus: A joint analysis of the International Thymic Malignancy Interest Group and the European Society of Thoracic Surgeons databases. J Thorac Cardiovasc Surg, 2015, 149(1): 103-109.
15. Wu MH, Tseng YL, Cheng FF, et al. Thymic carcinoid combined with myasthenia gravis. J Thorac Cardiovasc Surg, 2004, 127(2): 584-585.
16. Nakajima J, Okumura M, Yano M, et al. Myasthenia gravis with thymic epithelial tumour: A retrospective analysis of a Japanese database. Eur J Cardiothorac Surg, 2016, 49(5): 1510-1515.
17. Bordin-Wosk T, Patel SP, Horman SF. GABAB R-mediated paraneoplastic limbic encephalitis due to thymic small cell carcinoma. J Gen Intern Med, 2019, 34(8): 1658-1661.
18. Kamp K, Alwani RA, Korpershoek E, et al. Prevalence and clinical features of the ectopic ACTH syndrome in patients with gastroenteropancreatic and thoracic neuroendocrine tumors. Eur J Endocrinol, 2016, 174(3): 271-280.
19. Alexandraki KI, Grossman AB. The ectopic ACTH syndrome. Rev Endocr Metab Disord, 2010, 11(2): 117-126.
20. Araki T, Sholl LM, Hatabu H, et al. Radiological features and metastatic patterns of thymic neuroendocrine tumours. Clin Radiol, 2018, 73(5): 479-484.
21. Zhao Y, Gu H, Fan L, et al. Comparison of clinical features and survival between thymic carcinoma and thymic carcinoid patients. Eur J Cardiothorac Surg, 2017, 52(1): 33-38.
22. Li B, Xin YK, Xiao G, et al. Predicting pathological subtypes and stages of thymic epithelial tumors using DWI: Value of combining ADC and texture parameters. Eur Radiol, 2019, 29(10): 5330-5340.
23. Weissferdt A, Moran CA. Neuroendocrine differentiation in thymic carcinomas: A diagnostic pitfall: An immunohistochemical analysis of 27 cases. Am J Clin Pathol, 2016, 145(3): 393-400.
24. Marx A, Chan JKC, Chalabreysse L, et al. The 2021 WHO Classification of Tumors of the Thymus and Mediastinum: What Is New in Thymic Epithelial, Germ Cell, and Mesenchymal Tumors? J Thorac Oncol, 2022, 17(2): 200-213.
25. Marx A, Chan JKC, Chalabreysse L, et al. The 2021 WHO classification of tumors of the thymus and mediastinum: What is new in thymic rpithelial, germ cell, and mesenchymal tumors? J Thorac Oncol, 2022, 17(2): 200-213.
26. Cardillo G, Rea F, Lucchi M, et al. Primary neuroendocrine tumors of the thymus: A multicenter experience of 35 patients. Ann Thorac Surg, 2012, 94(1): 241-245.
27. Masaoka A, Monden Y, Nakahara K, et al. Follow-up study of thymomas with special reference to their clinical stages. Cancer, 1981, 48(11): 2485-2492.
28. Koga K, Matsuno Y, Noguchi M, et al. A review of 79 thymomas: Modification of staging system and reappraisal of conventional division into invasive and non-invasive thymoma. Pathol Int, 1994, 44(5): 359-367.
29. Detterbeck FC, Nicholson AG, Kondo K, et al. The Masaoka-Koga stage classification for thymic malignancies: Clarification and definition of terms. J Thorac Oncol, 2011, 6(7 Suppl 3): S1710-1716.
30. Detterbeck FC, Stratton K, Giroux D, et al. The IASLC/ITMIG Thymic Epithelial Tumors Staging Project: Proposal for an evidence-based stage classification system for the forthcoming (8th) edition of the TNM classification of malignant tumors. J Thorac Oncol, 2014, 9(9 Suppl 2): S65-S72.
31. Meurgey A, Girard N, Merveilleux du Vignaux C, et al. Assessment of the ITMIG statement on the WHO histological classification and of the eighth TNM staging of thymic epithelial tumors of a series of 188 thymic epithelial tumors. J Thorac Oncol, 2017, 12(10): 1571-1581.
32. Zhao Y, Shi J, Fan L, et al. Evaluation of the proposed International Association for the Study of Lung Cancer (IASLC)/International Thymic Malignancies Interest Group (ITMIG) staging revisions in thymic well-differentiated neuroendocrine carcinoma patients. Eur J Cardiothorac Surg, 2016, 49(2): 569-573.
33. Dinter H, Bohnenberger H, Beck J, et al. Molecular classification of neuroendocrine tumors of the thymus. J Thorac Oncol, 2019, 14(8): 1472-1483.
34. NCCN Clinical Practice Guidelines in Oncology (NCCN Guidelines®). Neuroendocrine and Adrenal Tumors, Version4.2021.https://www.nccn.org/guidelines/guidelines-detail?category=1&id=1448.Accessed on [2022-02-10].
35. Bertolaccini L, Prisciandaro E, Galetta D, et al. Outcomes and safety analysis in superior vena cava resection for extended thymic epithelial tumors. Ann Thorac Surg, 2021, 112(1): 271-277.
36. Mendogni P, Toker A, Moser B, et al. Surgical resection of Masaoka stage Ⅲ thymic epithelial tumours with great vessels involvement: A retrospective multicentric analysis from the European Society of Thoracic Surgeons thymic database. Eur J Cardiothorac Surg, 2022.
37. Weksler B, Holden A, Sullivan JL. Impact of positive nodal metastases in patients with thymic carcinoma and thymic neuroendocrine tumors. J Thorac Oncol, 2015, 10(11): 1642-1647.
38. Cheufou DH, Valdivia D, Puhlvers S, et al. Lymph node involvement and the surgical treatment of thymic epithelial and neuroendocrine carcinoma. Ann Thorac Surg, 2019, 107(6): 1632-1638.
39. Fang W, Wang Y, Pang L, et al. Lymph node metastasis in thymic malignancies: A Chinese multicenter prospective observational study. J Thorac Cardiovasc Surg, 2018, 156(2): 824-833.
40. Bian D, Qi M, Hu J, et al. The comparison of predictive factors regarding prognoses and invasion of thymic neuroendocrine tumors preoperatively and postoperatively. J Thorac Dis, 2018, 10(3): 1657-1669.
41. Corsini EM, Mitchell KG, Sceusi EL, et al. Multidisciplinary treatment of thymic neuroendocrine tumors: surgery remains a key component. J Thorac Dis, 2019, 11(8): 3391-3398.
42. Wen J, Chen J, Chen D, et al. Evaluation of the prognostic value of surgery and postoperative radiotherapy for patients with thymic neuroendocrine tumors: A propensity-matched study based on the SEER database. Thorac Cancer, 2018, 9(12): 1603-1613.
43. Wang H, Yang Y, Fan X, et al. Thymic neuroendocrine tumors: An analysis of 18 cases and a literature review. Transl Cancer Res, 2016, 5(6): 789-796.
44. Miyata R, Hamaji M, Omasa M, et al. The treatment and survival of patients with postoperative recurrent thymic carcinoma and neuroendocrine carcinoma: A multicenter retrospective study. Surg Today, 2020, 51(4): 502-510.
45. Davi' MV, Cosaro E, Piacentini S, et al. Prognostic factors in ectopic Cushing's syndrome due to neuroendocrine tumors: Multicenter study. Eur J Endocrinol, 2017, 176(4): 453-461.
46. Cho J, Kim HS, Ku BM, et al. Pembrolizumab for patients with refractory or relapsed thymic epithelial tumor: An open-label Phase Ⅱ trial. J Clin Oncol, 2019, 37(24): 2162-2170.
47. Giaccone G, Kim C, Thompson J, et al. Pembrolizumab in patients with thymic carcinoma: A single-arm, single-centre, phase 2 study. Lancet Oncol, 2018, 19(3): 347-355.
48. Yokoyama S, Miyoshi H. Thymic tumors and immune checkpoint inhibitors. J Thorac Dis, 2018, 10(Suppl 13): S1509-S1515.1509-1515.
49. Filosso PL, Yao X, Ruffini E, et al. Comparison of outcomes between neuroendocrine thymic tumours and other subtypes of thymic carcinomas: A joint analysis of the European Society of Thoracic Surgeons and the International Thymic Malignancy Interest Group. Eur J Cardiothorac Surg, 2016, 50(4): 766-771.
50. Liu H, Gu Z, Qiu B, et al. A Recurrence predictive model for thymic tumors and its implication for postoperative management: A Chinese alliance for research in thymomas database study. J Thorac Oncol, 2020, 15(3): 448-456.
51. Song Q, Zhang LL, Qi Y, et al. Effect of clinicopathologic features on survival of patients with thymic carcinomas and thymic neuroendocrine tumors: A population-based analysis. Curr Probl Cancer, 2019, 43(5): 411-420.
52. Ose N, Maeda H, Inoue M, et al. Results of treatment for thymic neuroendocrine tumours: Multicentre clinicopathological study. Interact Cardiovasc Thorac Surg, 2018, 26(1): 18-24.
53. Hamaji M, Omasa M, Nakagawa T, et al. Survival outcomes of patients with high-grade and poorly differentiated thymic neuroendocrine carcinoma. Interact Cardiovasc Thorac Surg, 2020, 31(1): 98-101.
54. Ma K, Liu Y, Xue Z, et al. Treatment, prognostic markers, and survival in thymic neuroendocrine tumors. Medicine (Baltimore), 2017, 96(43): e7842.
55. Ströbel P, Zettl A, Shilo K, et al. Tumor genetics and survival of thymic neuroendocrine neoplasms: A multi-institutional clinicopathologic study. Genes Chromosomes Cancer, 2014, 53(9): 738-749.
56. Ahn S, Lee JJ, Ha SY, et al. Clinicopathological analysis of 21 thymic neuroendocrine tumors. Korean J Pathol, 2012, 46(3): 221-225.
57. Fang W, Filosso P L, Roden AC, et al. Clinicopathological features and current treatment outcomes of neuroendocrine thymic tumours. Eur J Cardio-Thorac Surg, 2021, 59(5): 1004-1013.

Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Progress in diagnosis and treatment of thymic neuroendocrine tumors

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