A Meta-Analysis of Induction Therapy for Advanced Thymic Epithelial Tumors
2015; Elsevier BV; Volume: 99; Issue: 5 Linguagem: Inglês
10.1016/j.athoracsur.2014.12.048
ISSN1552-6259
AutoresMasatsugu Hamaji, Syed Osman Ali, Bryan M. Burt,
Tópico(s)Meningioma and schwannoma management
ResumoThis meta-analysis was designed to determine the effect of induction therapy and surgical resection on overall survival in patients with advanced thymic epithelial tumors. PubMed and Scopus databases were queried, and 12 studies comprising 266 patients were analyzed. Meta-analysis using a random effect model revealed a pooled rate of response to induction therapy of 59%, a pooled rate of complete resection of 73%, and pooled 5-year and 10-year overall survival of 87% and 76% after induction therapy, respectively. Surgical resection after induction therapy for advanced thymic epithelial tumors can be undertaken with favorable outcomes. This meta-analysis was designed to determine the effect of induction therapy and surgical resection on overall survival in patients with advanced thymic epithelial tumors. PubMed and Scopus databases were queried, and 12 studies comprising 266 patients were analyzed. Meta-analysis using a random effect model revealed a pooled rate of response to induction therapy of 59%, a pooled rate of complete resection of 73%, and pooled 5-year and 10-year overall survival of 87% and 76% after induction therapy, respectively. Surgical resection after induction therapy for advanced thymic epithelial tumors can be undertaken with favorable outcomes. Thymic epithelial tumors (TETs) are the most frequent tumors of the anterior mediastinum in adults. Patients with TETs can present with locally advanced diseases (stage III or IVA), and completeness of resection has consistently been shown to be a critical factor for determining recurrence and overall survival [1Venuta F. Rendina E.A. Anile M. de Giacomo T. Vitolo D. Coloni G.F. Thymoma and thymic carcinoma.Gen Thorac Cardiovasc Surg. 2012; 60: 1-12Crossref PubMed Scopus (74) Google Scholar, 2Shapiro M. Korst R.J. Surgical approaches for stage IVA thymic epithelial tumors.Front Oncol. 2014; 3: 332Crossref PubMed Scopus (21) Google Scholar, 3Riely G.J. Huang J. Induction therapy for locally advanced thymoma.J Thorac Oncol. 2010; 5: S323-S326Crossref PubMed Scopus (38) Google Scholar]. In many patients, TETs may present as tumors that do not appear completely resectable. In these cases, induction therapy (chemotherapy or chemoradiotherapy) has been offered in an attempt to downstage the tumors and achieve complete resection. Cisplatin-based induction chemotherapy is generally well tolerated and was associated with good responses in several prospective clinical trials of advanced TETs [4Kunitoh H. Tamura T. Shibata T. et al.A phase II trial of dose-dense chemotherapy, followed by surgical resection and/or thoracic radiotherapy, in locally advanced thymoma: report of a Japan Clinical Oncology Group trial (JCOG 9606).Br J Cancer. 2010; 29: 6-11Crossref Scopus (66) Google Scholar, 5Berruti A. Borasio P. Gerbino A. et al.Primary chemotherapy with adriamycin, cisplatin, vincristine and cyclophosphamide in locally advanced thymomas: a single institution experience.Br J Cancer. 1999; 81: 841-845Crossref PubMed Scopus (74) Google Scholar, 6Kim E.S. Putnam J.B. Komaki R. et al.Phase II study of a multidisciplinary approach with induction chemotherapy, followed by surgical resection, radiation therapy, and consolidation chemotherapy for unresectable malignant thymomas: final report.Lung Cancer. 2004; 44: 369-379Abstract Full Text Full Text PDF PubMed Scopus (257) Google Scholar]. Radiotherapy has been added to induction chemotherapy regimens in an attempt to further enhance rates of response [7Korst R.J. Bezjak A. Blackmon S. et al.Neoadjuvant chemoradiotherapy for locally advanced thymic tumors: a phase II, multi-institutional clinical trial.J Thorac Cardiovasc Surg. 2014; 147: 36-44Abstract Full Text Full Text PDF PubMed Scopus (103) Google Scholar, 8Wright C.D. Choi N.C. Wain J.C. Mathisen D.J. Lynch T.J. Fidias P. Induction chemoradiotherapy followed by resection for locally advanced Masaoka stage III and IVA thymic tumors.Ann Thorac Surg. 2008; 85: 385-389Abstract Full Text Full Text PDF PubMed Scopus (125) Google Scholar, 9Wright C.D. Extended resections for thymic malignancies.J Thorac Oncol. 2010; 5: S344-S347Crossref PubMed Scopus (41) Google Scholar]. There is a paucity of published data on the management of advanced TETs, and there remains no standard guideline for management. Given the absence of high-quality evidence and the small numbers in relevant published cohorts, we set out to perform a quantitative meta-analysis to comprehensively characterize long-term survival outcomes in patients undergoing induction therapy and surgical resection for advanced (stage III to IVA) TETs. A search on August 17, 2014, of the PubMed (United States National Library of Medicine) and Scopus (by Elsevier) databases for original studies published in English and using the terms “thymoma,” “chemotherapy,” “surgery,” and “survival” resulted in 276 abstracts. The flow of selecting eligible articles was reported following the PRISMA (preferred reporting items for systematic reviews and meta-analysis) statement (Fig 1). Abstracts of these 276 articles were independently reviewed by a Japanese board-certified thoracic surgeon (M.H.) and thoracic surgeons certified by American Board of Thoracic Surgery (B.M.B. and S.O.A). Full manuscripts of 18 original studies describing cohorts of 10 patients or more with induction treatment, followed by surgical resection, for advanced (typically stage III or IVA) TETs were reviewed. Of these18 studies, 12 reported rates of response to induction treatment or 5-year or 10-year overall survival (OS), or both, by the Kaplan-Meier method and were selected for our review [4Kunitoh H. Tamura T. Shibata T. et al.A phase II trial of dose-dense chemotherapy, followed by surgical resection and/or thoracic radiotherapy, in locally advanced thymoma: report of a Japan Clinical Oncology Group trial (JCOG 9606).Br J Cancer. 2010; 29: 6-11Crossref Scopus (66) Google Scholar, 6Kim E.S. Putnam J.B. Komaki R. et al.Phase II study of a multidisciplinary approach with induction chemotherapy, followed by surgical resection, radiation therapy, and consolidation chemotherapy for unresectable malignant thymomas: final report.Lung Cancer. 2004; 44: 369-379Abstract Full Text Full Text PDF PubMed Scopus (257) Google Scholar, 7Korst R.J. Bezjak A. Blackmon S. et al.Neoadjuvant chemoradiotherapy for locally advanced thymic tumors: a phase II, multi-institutional clinical trial.J Thorac Cardiovasc Surg. 2014; 147: 36-44Abstract Full Text Full Text PDF PubMed Scopus (103) Google Scholar, 8Wright C.D. Choi N.C. Wain J.C. Mathisen D.J. Lynch T.J. Fidias P. Induction chemoradiotherapy followed by resection for locally advanced Masaoka stage III and IVA thymic tumors.Ann Thorac Surg. 2008; 85: 385-389Abstract Full Text Full Text PDF PubMed Scopus (125) Google Scholar, 10Huang J. Rizk N.P. Travis W.D. et al.Feasibility of multimodality therapy including extended resections in stage IVA thymoma.J Thorac Cardiovasc Surg. 2007; 134: 1477-1483Abstract Full Text Full Text PDF PubMed Scopus (90) Google Scholar, 11Park S. Ahn M.J. Ahn J.S. et al.A prospective phase II trial of induction chemotherapy with docetaxel/cisplatin for Masaoka stage III/IV thymic epithelial tumors.J Thorac Oncol. 2013; 8: 959-966Crossref PubMed Scopus (31) Google Scholar, 12Rena O. Mineo T.C. Casadio C. Multimodal treatment for stage IVA thymoma: a proposable strategy.Lung Cancer. 2012; 76: 89-92Abstract Full Text Full Text PDF PubMed Scopus (24) Google Scholar, 13Rea F. Marulli G. Di Chiara F. et al.Multidisciplinary approach for advanced stage thymic tumors: long-term outcome.Lung Cancer. 2011; 72: 68-72Abstract Full Text Full Text PDF PubMed Scopus (23) Google Scholar, 14Mineo T.C. Mineo D. Onorati I. Cufari M.E. Ambrogi V. New predictors of response to neoadjuvant chemotherapy and survival for invasive thymoma: a retrospective analysis.Ann Surg Oncol. 2010; 17: 3022-3029Crossref PubMed Scopus (14) Google Scholar, 15Cardillo G. Carleo F. Giunti R. et al.Predictors of survival in patients with locally advanced thymoma and thymic carcinoma (Masaoka stages III and IVa).Eur J Cardiothorac Surg. 2010; 37: 819-823Crossref PubMed Scopus (67) Google Scholar, 16Lucchi M. Melfi F. Dini P. et al.Neoadjuvant chemotherapy for stage III and IVA thymomas: a single-institution experience with a long follow-up.J Thorac Oncol. 2006; 1: 308-313Abstract Full Text Full Text PDF PubMed Scopus (36) Google Scholar, 17Venuta F. Rendina E.A. Longo F. et al.Long-term outcome after multimodality treatment for stage III thymic tumors.Ann Thorac Surg. 2003; 76: 1866-1872Abstract Full Text Full Text PDF PubMed Scopus (185) Google Scholar]. We excluded six studies: four secondary to missing OS data [18Marulli G. Lucchi M. Margaritora S. et al.Surgical treatment of stage III thymic tumors: a multi-institutional review from four Italian centers.Eur J Cardiothorac Surg. 2011; 39: e1-7Crossref PubMed Scopus (34) Google Scholar, 19Bretti S. Berruti A. Loddo C. et al.Multimodal management of stages III-IVa malignant thymoma.Lung Cancer. 2004; 44: 69-77Abstract Full Text Full Text PDF PubMed Scopus (99) Google Scholar, 20Okereke I.C. Kesler K.A. Morad M.H. et al.Prognostic indicators after surgery for thymoma.Ann Thorac Surg. 2010; 89: 1071-1077Abstract Full Text Full Text PDF PubMed Scopus (42) Google Scholar, 21Shin D.M. Walsh G.L. Komaki R. et al.A multidisciplinary approach to therapy for unresectable malignant thymoma.Ann Intern Med. 1998; 129: 100-104Crossref PubMed Scopus (129) Google Scholar] and two secondary to data overlap [22Lucchi M. Ambrogi M.C. Duranti L. et al.Advanced stage thymomas and thymic carcinomas: results of multimodality treatments.Ann Thorac Surg. 2005; 79: 1840-1844Abstract Full Text Full Text PDF PubMed Scopus (111) Google Scholar, 23Rea F. Sartori F. Loy M. et al.Chemotherapy and operation for invasive thymoma.J Thorac Cardiovasc Surg. 1993; 106: 543-549PubMed Google Scholar]. Rates of response to induction therapy, rates of complete resection, association of the response and complete resection, and 5-year and 10-year OS after induction therapy were extracted for a quantitative meta-analysis. Survival measures were calculated from the time of beginning induction therapy or from the time of surgical resection. For each study, the standard error (SE) of the 5-year or 10-year OS rate was calculated according to the formula [24Parmer M.K. Torri V. Stewart L. Extracting summary statistics to perform meta-analyses of the published literature for survival endpoints.Stat Med. 1998; 17: 2815-2834Crossref PubMed Scopus (3885) Google Scholar]:SE=a×(1−a)n,where a is the 5-year or 10-year overall survival rate and n is the sample size. Data were analyzed with Review Manager 2 software (Biostat Inc, Englewood, NJ). Meta-analysis was performed using random effect summaries. Potential publication bias was evaluated with funnel plots of precision using log standard errors. Q statistics were used to test for heterogeneity among the studies included in the meta-analyses. The proportion of total variability attributed to between-studies heterogeneity was assessed with the I2 statistic, a confirmatory test for heterogeneity [25Higgins J.P. Thompson S.G. Quantifying heterogeneity in a meta-analysis.Stat Med. 2002; 21: 1539-1558Crossref PubMed Scopus (23324) Google Scholar, 26Ioannidis J.P. Patsopoulos N.A. Evangelou E. Uncertainty in heterogeneity estimates in meta-analyses.Br Med J. 2007; 78: 375-376Google Scholar], with an I2 of less than 25, 25 to 50, and more than 50% representing low, moderate, and high degrees of heterogeneity, respectively. Some variables were extracted for reference but not included in the meta-analysis. These data included details of study design, eligibility criteria, age, sex, paraneoplastic syndromes, initial Masaoka stages, biopsy procedures, initial World Health Organization (WHO) histology, regimens of induction therapy, surgical approach, adjuvant therapy, follow-up period, and progression-free survival. No randomized trials on the management of advanced TETs were found. We identified 12 studies of 10 or more patients that reported the 5-year or 10-year OS of patients with advanced TETs from the time of induction therapy or from the time of surgical resection after induction therapy (Table 1). The cohort consisted of 266 patients. Six of the 12 studies were prospective studies that represented 127 patients (11 to 30 patients in each individual study), and the other six studies were retrospective case series that represented 139 patients (10 to 38 patients in each study). Each study met most of the criteria according to the checklists of STROBE (Strengthening the Reporting of Observational Studies in Epidemiology) statement.Table 1Characteristics of the Individual Studies Selected for a Quantitative Meta-AnalysisAuthorYearCountryStudy PeriodStudy DesignEligibility Stage CriteriaTotal (No.)AgeaData are shown as mean ± standard deviation or as mean or median (range). (y)Male (%)Paraneoplastic Syndrome (%)Korst 7Korst R.J. Bezjak A. Blackmon S. et al.Neoadjuvant chemoradiotherapy for locally advanced thymic tumors: a phase II, multi-institutional clinical trial.J Thorac Cardiovasc Surg. 2014; 147: 36-44Abstract Full Text Full Text PDF PubMed Scopus (103) Google Scholar2014USA2007–2012ProspectiveIII, IV, and I and II (only if >5 cm)22Median 51 (18–78)80MG: 24, RCA: 5Park 11Park S. Ahn M.J. Ahn J.S. et al.A prospective phase II trial of induction chemotherapy with docetaxel/cisplatin for Masaoka stage III/IV thymic epithelial tumors.J Thorac Oncol. 2013; 8: 959-966Crossref PubMed Scopus (31) Google Scholar2013Korea2007–2011ProspectiveIII and IV27Median 54 (15–68)59.3NIRena 12Rena O. Mineo T.C. Casadio C. Multimodal treatment for stage IVA thymoma: a proposable strategy.Lung Cancer. 2012; 76: 89-92Abstract Full Text Full Text PDF PubMed Scopus (24) Google Scholar2011Italy1998–2008RetrospectiveIVA with pleural implants18Mean 54.5 (29–68)55.6MG: 16.7, RCA: 5.6Rea 13Rea F. Marulli G. Di Chiara F. et al.Multidisciplinary approach for advanced stage thymic tumors: long-term outcome.Lung Cancer. 2011; 72: 68-72Abstract Full Text Full Text PDF PubMed Scopus (23) Google Scholar2011Italy1980–2008RetrospectiveUnresectable III, IVA and IVB38NININIMineo 14Mineo T.C. Mineo D. Onorati I. Cufari M.E. Ambrogi V. New predictors of response to neoadjuvant chemotherapy and survival for invasive thymoma: a retrospective analysis.Ann Surg Oncol. 2010; 17: 3022-3029Crossref PubMed Scopus (14) Google Scholar2010Italy1989–2008RetrospectiveUnresectable III3355.5 ± 7.360.6MG: 18.2Cardillo 15Cardillo G. Carleo F. Giunti R. et al.Predictors of survival in patients with locally advanced thymoma and thymic carcinoma (Masaoka stages III and IVa).Eur J Cardiothorac Surg. 2010; 37: 819-823Crossref PubMed Scopus (67) Google Scholar2010Italy1991–2007RetrospectiveUnresectable III and IVA3145.7 ± 12.577.4MG: 9.7Kunitoh 4Kunitoh H. Tamura T. Shibata T. et al.A phase II trial of dose-dense chemotherapy, followed by surgical resection and/or thoracic radiotherapy, in locally advanced thymoma: report of a Japan Clinical Oncology Group trial (JCOG 9606).Br J Cancer. 2010; 29: 6-11Crossref Scopus (66) Google Scholar2010Japan1997–2005ProspectiveUnresectable III11NININIWright 8Wright C.D. Choi N.C. Wain J.C. Mathisen D.J. Lynch T.J. Fidias P. Induction chemoradiotherapy followed by resection for locally advanced Masaoka stage III and IVA thymic tumors.Ann Thorac Surg. 2008; 85: 385-389Abstract Full Text Full Text PDF PubMed Scopus (125) Google Scholar2008U.S.A1997–2006RetrospectiveUnresectable III and IVA10Median 53.5 (34–66)30MG: 10Huang 10Huang J. Rizk N.P. Travis W.D. et al.Feasibility of multimodality therapy including extended resections in stage IVA thymoma.J Thorac Cardiovasc Surg. 2007; 134: 1477-1483Abstract Full Text Full Text PDF PubMed Scopus (90) Google Scholar2007U.S.A1996–2006RetrospectiveIVA18Median 43.5 (26–74)44.4NoneLucchi 22Lucchi M. Ambrogi M.C. Duranti L. et al.Advanced stage thymomas and thymic carcinomas: results of multimodality treatments.Ann Thorac Surg. 2005; 79: 1840-1844Abstract Full Text Full Text PDF PubMed Scopus (111) Google Scholar2006Italy1989–2004ProspectiveIII and IVA30Mean 53.7 (25–74)43.3MG: 40, RCA: 6.7Kim 6Kim E.S. Putnam J.B. Komaki R. et al.Phase II study of a multidisciplinary approach with induction chemotherapy, followed by surgical resection, radiation therapy, and consolidation chemotherapy for unresectable malignant thymomas: final report.Lung Cancer. 2004; 44: 369-379Abstract Full Text Full Text PDF PubMed Scopus (257) Google Scholar2004U.S.A1990–2000ProspectiveUnresectable III, IVA, and IVB22Median 47 (25–70)40.9NIVenuta 17Venuta F. Rendina E.A. Longo F. et al.Long-term outcome after multimodality treatment for stage III thymic tumors.Ann Thorac Surg. 2003; 76: 1866-1872Abstract Full Text Full Text PDF PubMed Scopus (185) Google Scholar2003Italy1989–2003ProspectiveUnresectable stage III15NININIMG = myasthenia gravis; NI = no information; RCA = red cell aplasia; USA = United States of America.a Data are shown as mean ± standard deviation or as mean or median (range). Open table in a new tab MG = myasthenia gravis; NI = no information; RCA = red cell aplasia; USA = United States of America. Masaoka stage and WHO histology are reported in Table 2. On average, stage III tumors were present in 57.4% of patients and stage IVA tumors in 36.6%. The WHO tumor histology types were A, AB, B1, B2, or B3 in 82.5% of patients and type C in 17.5%.Table 2Tumor Characteristics (Initial Masaoka Stages and World Health Organization Histology)AuthorInitial Masaoka Stage No. (%)Biopsy ProcedureInitial WHO HistologyNo. (%)Korst 7Korst R.J. Bezjak A. Blackmon S. et al.Neoadjuvant chemoradiotherapy for locally advanced thymic tumors: a phase II, multi-institutional clinical trial.J Thorac Cardiovasc Surg. 2014; 147: 36-44Abstract Full Text Full Text PDF PubMed Scopus (103) Google ScholarNINIA: 2 (10), AB: 1 (5), B1: 1 (5), B2: 3 (14), B3: 6 (29), C: 7 (33)Park 11Park S. Ahn M.J. Ahn J.S. et al.A prospective phase II trial of induction chemotherapy with docetaxel/cisplatin for Masaoka stage III/IV thymic epithelial tumors.J Thorac Oncol. 2013; 8: 959-966Crossref PubMed Scopus (31) Google ScholarIII: 8 (26.3), IVA: 17 (63.2), IVB: 2 (10.5)NIB2: 4 (14.8), B3: 3 (11.1), C: 18 (66.7), a mix of B subtypes: 2 (7.4)Rena 12Rena O. Mineo T.C. Casadio C. Multimodal treatment for stage IVA thymoma: a proposable strategy.Lung Cancer. 2012; 76: 89-92Abstract Full Text Full Text PDF PubMed Scopus (24) Google ScholarIVA: 18 (100)Anterior mediastinotomy: 16 (88.9), CT-guided percutaneous: 2 (11.1)AB: 1 (5.6), B1: 2 (11.1), B2: 4 (22.2), B3: 7 (38.9), a mixture of B subtypes: 4 (22.2)Rea 13Rea F. Marulli G. Di Chiara F. et al.Multidisciplinary approach for advanced stage thymic tumors: long-term outcome.Lung Cancer. 2011; 72: 68-72Abstract Full Text Full Text PDF PubMed Scopus (23) Google ScholarIII: 23 (60.5), IVA: 12 (31.6), IVB: 3 (7.9)NIA: 3 (7.9), AB: 5 (13.2), B1: 4 (10.5), B2: 12 (31.6), B3: 8 (21.1), C: 6 (15.8)Mineo 14Mineo T.C. Mineo D. Onorati I. Cufari M.E. Ambrogi V. New predictors of response to neoadjuvant chemotherapy and survival for invasive thymoma: a retrospective analysis.Ann Surg Oncol. 2010; 17: 3022-3029Crossref PubMed Scopus (14) Google ScholarIII: 33 (100)Anterior mediastinotomy: 12 (36.4), VATS: 21 (63.6)A: 5 (15.2), AB: 6 (18.2), B1: 5 (15.2), B2: 10 (33.3), B3: 7 (21.2)Cardillo 15Cardillo G. Carleo F. Giunti R. et al.Predictors of survival in patients with locally advanced thymoma and thymic carcinoma (Masaoka stages III and IVa).Eur J Cardiothorac Surg. 2010; 37: 819-823Crossref PubMed Scopus (67) Google ScholarIII: 18 (58.1), IVA: 13 (41.9)Anterior mediastinotomy: 31 (100)AB: 8 (25.8), B1: 3 (9.7), B2: 4 (12.9), B3: 6 (19.4), C: 10 (32.3)Kunitoh 4Kunitoh H. Tamura T. Shibata T. et al.A phase II trial of dose-dense chemotherapy, followed by surgical resection and/or thoracic radiotherapy, in locally advanced thymoma: report of a Japan Clinical Oncology Group trial (JCOG 9606).Br J Cancer. 2010; 29: 6-11Crossref Scopus (66) Google ScholarIII: 21 (100)NINIWright 8Wright C.D. Choi N.C. Wain J.C. Mathisen D.J. Lynch T.J. Fidias P. Induction chemoradiotherapy followed by resection for locally advanced Masaoka stage III and IVA thymic tumors.Ann Thorac Surg. 2008; 85: 385-389Abstract Full Text Full Text PDF PubMed Scopus (125) Google ScholarIII: 7 (70), IVA: 3 (30)NIA: 1 (10), B1: 1 (10), B3: 7 (70), C: 1 (10)Huang 10Huang J. Rizk N.P. Travis W.D. et al.Feasibility of multimodality therapy including extended resections in stage IVA thymoma.J Thorac Cardiovasc Surg. 2007; 134: 1477-1483Abstract Full Text Full Text PDF PubMed Scopus (90) Google ScholarIVA: 18 (100)NIAB: 1 (5.6), B1: 2 (11.1), B2: 3 (16.7), B3: 6 (33.3), a mixture of B subtypes: 6 (33.3)Lucchi 16Lucchi M. Melfi F. Dini P. et al.Neoadjuvant chemotherapy for stage III and IVA thymomas: a single-institution experience with a long follow-up.J Thorac Oncol. 2006; 1: 308-313Abstract Full Text Full Text PDF PubMed Scopus (36) Google ScholarIII: 20 (66.7), IV: 10 (33.3)Anterior mediastinotomy: 5 (16.7), VATS: 7 (23.3), needle biopsy: 4 (13.3), none: 14 (46.7)AB: 3 (10), B1: 5 (16.7), B2: 7 (23.3), B3: 15 (50)Kim 6Kim E.S. Putnam J.B. Komaki R. et al.Phase II study of a multidisciplinary approach with induction chemotherapy, followed by surgical resection, radiation therapy, and consolidation chemotherapy for unresectable malignant thymomas: final report.Lung Cancer. 2004; 44: 369-379Abstract Full Text Full Text PDF PubMed Scopus (257) Google ScholarIII: 11 (50), IVA: 10 (45.5), IVB: 1 (4.5)NINIVenuta 17Venuta F. Rendina E.A. Longo F. et al.Long-term outcome after multimodality treatment for stage III thymic tumors.Ann Thorac Surg. 2003; 76: 1866-1872Abstract Full Text Full Text PDF PubMed Scopus (185) Google ScholarIII: 15 (100)Anterior mediastinotomy: 7 (46.7), VATS: 8 (53.3)NICT = computed tomography; NI = no information; VATS = video-assisted thoracoscopic surgery; WHO = World Health Organization. Open table in a new tab CT = computed tomography; NI = no information; VATS = video-assisted thoracoscopic surgery; WHO = World Health Organization. Eight studies provided eligibility criteria for induction therapy [4Kunitoh H. Tamura T. Shibata T. et al.A phase II trial of dose-dense chemotherapy, followed by surgical resection and/or thoracic radiotherapy, in locally advanced thymoma: report of a Japan Clinical Oncology Group trial (JCOG 9606).Br J Cancer. 2010; 29: 6-11Crossref Scopus (66) Google Scholar, 6Kim E.S. Putnam J.B. Komaki R. et al.Phase II study of a multidisciplinary approach with induction chemotherapy, followed by surgical resection, radiation therapy, and consolidation chemotherapy for unresectable malignant thymomas: final report.Lung Cancer. 2004; 44: 369-379Abstract Full Text Full Text PDF PubMed Scopus (257) Google Scholar, 7Korst R.J. Bezjak A. Blackmon S. et al.Neoadjuvant chemoradiotherapy for locally advanced thymic tumors: a phase II, multi-institutional clinical trial.J Thorac Cardiovasc Surg. 2014; 147: 36-44Abstract Full Text Full Text PDF PubMed Scopus (103) Google Scholar, 8Wright C.D. Choi N.C. Wain J.C. Mathisen D.J. Lynch T.J. Fidias P. Induction chemoradiotherapy followed by resection for locally advanced Masaoka stage III and IVA thymic tumors.Ann Thorac Surg. 2008; 85: 385-389Abstract Full Text Full Text PDF PubMed Scopus (125) Google Scholar, 11Park S. Ahn M.J. Ahn J.S. et al.A prospective phase II trial of induction chemotherapy with docetaxel/cisplatin for Masaoka stage III/IV thymic epithelial tumors.J Thorac Oncol. 2013; 8: 959-966Crossref PubMed Scopus (31) Google Scholar, 12Rena O. Mineo T.C. Casadio C. Multimodal treatment for stage IVA thymoma: a proposable strategy.Lung Cancer. 2012; 76: 89-92Abstract Full Text Full Text PDF PubMed Scopus (24) Google Scholar, 15Cardillo G. Carleo F. Giunti R. et al.Predictors of survival in patients with locally advanced thymoma and thymic carcinoma (Masaoka stages III and IVa).Eur J Cardiothorac Surg. 2010; 37: 819-823Crossref PubMed Scopus (67) Google Scholar, 16Lucchi M. Melfi F. Dini P. et al.Neoadjuvant chemotherapy for stage III and IVA thymomas: a single-institution experience with a long follow-up.J Thorac Oncol. 2006; 1: 308-313Abstract Full Text Full Text PDF PubMed Scopus (36) Google Scholar]: bone marrow reserve (eight studies) [4Kunitoh H. Tamura T. Shibata T. et al.A phase II trial of dose-dense chemotherapy, followed by surgical resection and/or thoracic radiotherapy, in locally advanced thymoma: report of a Japan Clinical Oncology Group trial (JCOG 9606).Br J Cancer. 2010; 29: 6-11Crossref Scopus (66) Google Scholar, 6Kim E.S. Putnam J.B. Komaki R. et al.Phase II study of a multidisciplinary approach with induction chemotherapy, followed by surgical resection, radiation therapy, and consolidation chemotherapy for unresectable malignant thymomas: final report.Lung Cancer. 2004; 44: 369-379Abstract Full Text Full Text PDF PubMed Scopus (257) Google Scholar, 7Korst R.J. Bezjak A. Blackmon S. et al.Neoadjuvant chemoradiotherapy for locally advanced thymic tumors: a phase II, multi-institutional clinical trial.J Thorac Cardiovasc Surg. 2014; 147: 36-44Abstract Full Text Full Text PDF PubMed Scopus (103) Google Scholar, 8Wright C.D. Choi N.C. Wain J.C. Mathisen D.J. Lynch T.J. Fidias P. Induction chemoradiotherapy followed by resection for locally advanced Masaoka stage III and IVA thymic tumors.Ann Thorac Surg. 2008; 85: 385-389Abstract Full Text Full Text PDF PubMed Scopus (125) Google Scholar, 11Park S. Ahn M.J. Ahn J.S. et al.A prospective phase II trial of induction chemotherapy with docetaxel/cisplatin for Masaoka stage III/IV thymic epithelial tumors.J Thorac Oncol. 2013; 8: 959-966Crossref PubMed Scopus (31) Google Scholar, 12Rena O. Mineo T.C. Casadio C. Multimodal treatment for stage IVA thymoma: a proposable strategy.Lung Cancer. 2012; 76: 89-92Abstract Full Text Full Text PDF PubMed Scopus (24) Google Scholar, 15Cardillo G. Carleo F. Giunti R. et al.Predictors of survival in patients with locally advanced thymoma and thymic carcinoma (Masaoka stages III and IVa).Eur J Cardiothorac Surg. 2010; 37: 819-823Crossref PubMed Scopus (67) Google Scholar, 16Lucchi M. Melfi F. 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