Annals of Oncology Advance Access published February 2, 2011
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1 Advance Access published February 2, 2011 original article doi: /annonc/mdq696 Comparison of RECIST and Choi criteria for computed tomographic response evaluation in patients with advanced gastrointestinal stromal tumor treated with sunitinib O. Dudeck 1,2 *, M. Zeile 1,2, P. Reichardt 3,4 & D. Pink 3,4 1 Department of Radiology, HELIOS Clinic Berlin-Buch, Berlin; 2 Department of Radiology and Nuclear Medicine, University of Magdeburg, Magdeburg; 3 Department of Hematology, Oncology and Palliative Care, HELIOS Clinic Bad Saarow, Bad Saarow; 4 Sarcoma Center Berlin-Brandenburg, Berlin, Germany Received 10 August 2010; revised 28 October 2010; accepted 28 October 2010 Background: Controversies exist about computed tomography (CT) response evaluation criteria for patients with gastrointestinal stromal tumor (GIST). Patients and methods: Fifty-one patients with advanced GIST treated second line with sunitinib were evaluated with contrast-enhanced CT every 3 months. Response was rated according to RECIST and Choi criteria. Progression-free survival (PFS) and overall survival (OS) were estimated by Kaplan Meier analysis. Results: According to RECIST, patients were categorized as complete response (CR; n = 0; 0%), partial remission (PR; n = 1; 2.0%), stable disease (SD; n = 37; 72.5%), and progressive disease (PD; n = 13; 25.5%) at 3 months. When Choi criteria were applied responses were CR (n = 0; 0%), PR (n = 16; 31.4%), SD (n = 21; 41.1%), and PD (n = 14; 27.5%). Despite these discrepancies, patients rated as SD with RECIST and PR as well as SD according to Choi criteria displayed similar PFS (41.3, 40.7, and 41.3 weeks, respectively) and OS (100.4, 91.6, and weeks, respectively). Patients with PD had significantly shorter PFS (10.1 weeks for both criteria) and OS (29.1 weeks for RECIST; 28.9 weeks for Choi) regardless of the response classification applied. Conclusion: In contrast to absence of progression, discrimination of PR from SD with Choi criteria was of no predictive value. Key words: Choi criteria, gastrointestinal stromal tumor, GIST, RECIST, sunitinib introduction Imatinib mesylate (GlivecÒ; Novartis Pharma, Basel, Switzerland), a selective tyrosine kinase inhibitor, is currently the standard-of-care first-line treatment of unresectable or metastatic gastrointestinal stromal tumor (GIST), the most common sarcoma of the gastrointestinal tract. Up to 90% of patients with GIST respond to imatinib or achieve durable stabilization of disease [1 3]. Nevertheless, primary and secondary (acquired) resistance to imatinib is a substantial problem in routine clinical practice [4]. Recently, excellent anticancer effects have been reported for the broad-spectrum receptor tyrosine kinase inhibitor sunitinib malate (SutentÒ; Pfizer, New York, NY) in patients with advanced GIST, who were resistant to or intolerant of previous treatment with imatinib [5 7]. Since the introduction of such molecularly targeted drugs, there has been increasing concern about the use of traditional *Correspondence to: Dr O. Dudeck, Department of Radiology and Nuclear Medicine, University of Magdeburg, Leipziger Strasse 44, Magdeburg, Germany. Tel: ; Fax: ; oliver.dudeck@med.ovgu.de tumor response criteria [8 11]. The patterns of drug-induced radiologic changes are heterogeneous, and the classification into formal response categories according to RECIST is often ambiguous and complex. In fact, these targeted therapies induce changes not only in lesion size but also in lesion structure, often resulting in a decrease in tumor density, enhancement of intratumoral nodules, and tumor vessels with no further decrease in size [11 13]. Positron emission tomography (PET) using 2-[fluorine-18]fluoro-2-deoxy-D-glucose (18FDG) has been shown to be highly sensitive in detecting early response in patients with metastatic GIST [14]. Nevertheless, a considerable fraction of GIST lesions may not demonstrate appreciable glucose uptake on pretreatment 18FDG PET [11]. Furthermore, access to PET technology is still limited for GIST patients because of scanner availability and cost constraints. Therefore, the widely accessible computed tomography (CT) currently resembles the imaging modality of choice in monitoring GIST patients treated with tyrosine kinase inhibitors during the course of treatment and surveillance. The recently reported Choi criteria aimed to combine morphologic original article ª The Author Published by Oxford University Press on behalf of the European Society for Medical Oncology. All rights reserved. For permissions, please journals.permissions@oup.com
2 original article tumor volume response and biologic response [10]. These CT criteria take a treatment-related decrease of tumor density into account and were found to correlate closely with early PET results [10, 15]. Nevertheless, a recent exploratory analysis found the much simpler RECIST sufficient to identify patients with a survival benefit just by the absence of progression [16]. In result, the prognostic value of Choi criteria remains unclear. Besides, available data on radiologic response evaluation are limited to GIST patients treated with imatinib. Therefore, the objective of this retrospective analysis was to evaluate the impact of the method of response evaluation, using both RECIST and Choi criteria in patients with advanced GIST treated with sunitinib. patients and methods patient population and study design A total of 54 patients (30 men and 24 women, age range years) treated at our institute from May 2005 to January 2010 were included in this retrospective analysis as they presented with histologically proven malignant GIST that was not amenable to surgery, radiation, or a combination of different approaches with curative intent, and confirmed objective failure of previous imatinib therapy. A part of the patients were treated within an international treatment-use study, supported by Pfizer Inc. This study was approved by the institutional review board and written informed consent was obtained from each patient. Other patients were treated according to the institutional standards. Criteria for inclusion were evidence of disease that was unidimensionally measurable with CT or magnetic resonance imaging; failure of treatment with imatinib based either on progression of disease according to RECIST [17] or on unacceptably severe toxic effects during imatinib therapy that precluded further treatment; imatinib last administered at least 2 weeks before inclusion; resolution of all toxic effects of imatinib or other therapy to grade 1 or less; adequate hepatic, renal, and cardiac function; absolute neutrophil count of at least 1500/ll; platelet count of at least /ll; and hemoglobin concentration of 90 g/l. Sunitinib was given at a starting daily dose of 50 mg. Dose reduction was carried out in the case of clinically relevant grade 3 or 4 toxic effects (to 37.5 mg/day and, if additional reduction was warranted, to 25 mg/day), so that all efforts were made to prevent drug discontinuation. imaging techniques CT was carried out with a Hi-Speed Advantage helical scanner (GE Medical Systems, Milwaukee, WI) using a monophasic scanning technique. Abdominopelvic scan was carried out from the level of the diaphragm to the pubic symphysis with 5.0 mm collimation, a pitch of 2, and 5 mm reconstruction interval; 100 ml of nonionic contrast agent (Ultravist 300; Schering, Berlin, Germany) was administered through an antecubital vein at a rate of 2 ml/s. Bolus tracking was used with a region of interest (ROI) placed in the descending thoracic aorta, which provided an automatic initiation of the scan 40 s after a contrast threshold of 120 Hounsfield units (HU) was reached, in order to ensure uniformity of parenchymal contrast enhancement. evaluation of response Contrast-enhanced helical CT was carried out every 3 months until patients experienced clinical or objective progressive disease (PD). Tumor size was measured in the longest cross-sectional dimension for each lesion at each time point using a MagicView workstation (Siemens, Erlangen, Germany). For each patient, the sum of all target lesion measurements was computed, and the absolute and percent changes from the pretreatment evaluation to the follow-up evaluation were calculated. In addition, the CT attenuation coefficient (density) of the tumor in HU was assessed by drawing a ROI circumscribing the margin of each lesion. The tumor density measurements of all lesions in a patient were combined, and an average HU was computed for each patient. Then, the absolute and percent changes in CT density from the pretreatment evaluation to the follow-up evaluation were computed for each patient. tumor response categorization Results of the measurements were classified according to RECIST as well as Choi criteria [10, 17]. We want to highlight that for RECIST, a decrease in the sum of lesion diameters of 30% was necessary for categorization as partial remission (PR), while a decrease of lesion diameters of 10% was sufficient according to Choi criteria. In addition, patients were rated as PR, when a decrease in the sum of the lesion densities (HU) of 15% was found, regardless of changes in tumor size. statistical analysis Progression-free survival (PFS) was measured from the date of pretreatment CT to the time point of death or objective PD as assessed with standard RECIST. Overall survival (OS) was measured from the date of pretreatment CT to the date of death. Patients alive and progression free at the last follow-up were censored. Both end points were estimated by the Kaplan Meier method. The log-rank test was used for comparison tests. A P value of 0.05 was set to be the level of statistical significance. results A total of 54 patients were included in the analysis with a median follow-up of 21 months (range 1 50 months). Mean duration of treatment with imatinib was weeks (range weeks) with a mean maximum dose of 800 mg (range mg). All patients had measurable disease at entry. A total of 176 lesions (mean lesion number per patient: 3.3; 109 liver lesions, 67 peritoneal lesions) with a mean tumor burden of mm (range mm) were evaluated. An overview of all patient data is given in Table 1. Fifty-one patients were assessable for tumor size changes at 3 months and 43 patients at 6 months. Overall, sunitinib dosing for the period reported resulted in acceptable tolerability. Adverse events rarely led to treatment discontinuation and were generally easily managed and reversible through dose reduction, dose interruption, or standard supportive medical treatment. In total, mean maximum sunitinib dose was 50 mg (range mg). Total PFS was 38.7 weeks [95% confidence interval (CI) ] as assessed with RECIST; total OS was 72.6 weeks (95% CI ). According to RECIST, no patient had complete response (CR), while only one patient (2.0%) was characterized as having achieved PR at 3-months follow-up. This patient had a PFS of 68.0 weeks and was still alive at the time of data cut-off (50 months after starting sunitinib). In contrast, stable disease (SD) was the most common tumor response found in 72.5% (n = 37) of patients. Median PFS of these patients was 41.3 weeks (95% CI ) with no difference found when compared with patients categorized either as PR (P = 0.684) or SD (P = 0.690) according to Choi criteria (compare Figure 1, Table 2). Similarly, median OS of patients rated as SD according to RECIST was weeks (95% CI ), 2 Dudeck et al.
3 Table 1. Patient characteristics Characteristics Total (N = 54) Age (years) Median 58 Range Sex, n (%) Male 30 (55.6) Female 24 (44.4) ECOG status, n (%) a ECOG 0 16 (29.6) ECOG 1 28 (51.9) ECOG 2 7 (13.0) ECOG 3+ 3 (5.5) Tumor burden at baseline (mm) Median 213 Range Maximum dose of imatinib therapy (mg) Median 800 Range Duration of imatinib therapy (weeks) Median Range Imatinib therapy outcome, n (%) Progression within 6 5 (9.4) months Progression after >6 46 (88.7) months Intolerance 1 (1.9) Best response to imatinib, n (%) Complete response 5 (9.3) Partial response 16 (29.6) Stable disease 22 (40.7) Progressive disease 5 (9.3) Not applicable or missing 6 (11.1) a ECOG status is graded on a scale from 0 to 5, with 0 denoting fully active and 5 death. A score of 3 indicates that the patient is capable of limited self-care but is confined to a bed or chair for >50% of his or her waking hours. ECOG, Eastern Cooperative Oncology Group. which again was not different as compared with patients categorized either as PR (P = 0.683) or SD (P = 0.607) according to Choi criteria (compare Figure 2, Table 2). In contrast, 25.5% (n = 13) of patients were categorized as PD according to RECIST, who had a median PFS of 10.1 weeks (95% CI ) and a median OS of 29.1 weeks (95% CI ; compare Figures 1 and 2). Both parameters were significantly shorter as compared with patients rated as SD according to RECIST (P < each). When Choi criteria were applied on 3-months follow-up, no patient qualified for CR, 31.4% (n = 16) of patients were categorized as PR, 41.1% (n = 21) as SD, and 27.5% (n = 14) as PD. In the group of patients with PR, median PFS was 40.7 weeks (95% CI ) and median OS 91.6 weeks (95% CI ). Surprisingly, patients categorized as SD had an almost similar median PFS of 41.3 weeks (95% CI ) as compared with patients rated as PR (compare Figure 1). Consequently, no statistical difference was found when both groups were compared using the log-rank test (P = 0.901). original article Furthermore, median OS of patients categorized as SD was weeks (95% CI ), which was even somewhat longer as compared with patients rated as PR (compare Figure 2). Nevertheless, again no statistical difference was found (P = 0.577). In contrast, patients with PD had a median PFS of 10.1 weeks (95% CI ), which was significantly shorter as compared with patients with either PR or SD (P < each; compare Figure 1). Similarly, median OS was with 28.9 weeks (95% CI ) also significantly shorter as compared with patients categorized as PR (P < 0.001) and SD (P < ; compare Figure 2). No differences in PFS and OS were found for patients with disease progression according to RECIST and Choi criteria (P = for PFS and P = for OS). At 6 months, again no patient had CR, 30.2% (n = 13) of patients were categorized as PR, 37.2% (n = 16) as SD, and 32.6% (n = 14) as PD according to Choi criteria. Two patients priorly categorized as PR as well as four patients categorized as SD were now rated as PD. When RECIST were used for response assessment, the same single patient was still characterized as having PR. The vast majority of patients (74.4%, n = 32) were classified as SD, while 23.3% (n = 10) were rated as PD. Three patients priorly categorized as SD were now rated as PD. Median PFS of patients rated PR and SD according to Choi criteria was 43.4 and 40.7 weeks, respectively, as well as 40.4 weeks for patients rated SD according to RECIST. Furthermore, median OS was 101.3, 114.6, and weeks, respectively. In total, very similar values of median PFS and OS were found for the response assessment with RECIST and Choi criteria at 6 months as compared with 3-months results. An overview of median PFS and OS according to response categorization with RECIST and Choi criteria at 3 and 6 months is given in Table 2. With Choi criteria, there was a strong trend to evaluate treatment response higher as compared with RECIST. At 3-months follow-up, 37 patients were rated as SD according to RECIST. When Choi criteria were applied to these patients, 15 were assigned to a higher response category (PR), while 2 patients were rated worse (PD). Higher categorization with Choi criteria (n = 14; 37.8%) was due to a decrease in tumor density 15% in six patients, a decrease in tumor size 10% but <30% in six patients, and due to both in two patients. Cystic transformation of 15% was observed in a total of 62.5% (n = 10) of our patients with PR according to Choi criteria. In two of these patients, there was a discrepancy between a decrease in tumor density (236% and 230%, respectively) and an increase in tumor size of (25% and 13%, respectively), so that they were rated as PD as well as SD according to RECIST. Interestingly, both patients experienced PD assessed with RECIST and Choi criteria on subsequent follow-up. All patients assessed as SD according to Choi criteria (n = 21; 41.1%) were also ranked as SD with RECIST. Discrepancies in PD categorization were found in three patients. One patient, already described above, was rated PR despite an increase of tumor size of 25% due to a simultaneous decrease in tumor density of 236%. In addition, two patients who were rated as PD with Choi criteria had an increase in tumor size of only 11% and 16%, which did not fulfill the RECIST for PD and thus were categorized as SD. doi: /annonc/mdq696 3
4 original article Figure 1. Progression-free survival of patients with advanced gastrointestinal stromal tumor according to response evaluation with RECIST and Choi criteria at 3 months of treatment with sunitinib. PR, partial remission; SD, stable disease; PD, progressive disease. Table 2. Median PFS and OS according to Choi and RECIST response criteria evaluated on CT carried out 3 and 6 months after commencement of second-line treatment with sunitinib in patients with advanced GIST Response 3 months 6 months category RECIST Choi RECIST Choi PFS OS PFS OS PFS OS PFS OS (weeks) (weeks) (weeks) (weeks) (weeks) (weeks) (weeks) (weeks) PR 68.0 n.e n.e SD PD PFS, progression-free survival; OS, overall survival; CT, computed tomography; GIST, gastrointestinal stromal tumor; PR, partial remission; n.e., not evaluable; SD, stable disease; PD, progressive disease. discussion In a randomized placebo-controlled phase III trial, sunitinib was proven highly effective following imatinib intolerance or failure with a median time to tumor progression (TTP) of 27.3 weeks and a median PFS of 24.1 weeks compared with 6.4 weeks with placebo following discontinuation of imatinib [5]. An ongoing global treatment-use study with 1126 patients with imatinib-resistant/-intolerant advanced GIST reported a median TTP of 41.0 weeks and a median OS of 75.0 weeks [18]. Furthermore, in a multicentric phase II trial, continuous daily dosing of sunitinib (37.5 mg/day) has proven effective with reported median PFS and OS of 34 and 107 weeks, respectively [19]. Our data confirmed these promising results with a median PFS of 38.7 weeks and a median OS of 72.6 weeks according to RECIST. Thus, second-line therapy with sunitinib can result in a long-term disease stabilization of patients with advanced GIST after failure of imatinib. Nevertheless, there is considerable concern that RECIST might not be optimal for response assessment in GIST because of the cystic change of lesions with no further decrease in size when responding, which may result in underassessment of objective activity [10, 11, 14, 15]. In our patients, 19.6% (n = 10) showed such density changes in tumor deposits, while objective tumor shrinkage as assessed with RECIST was an uncommon finding. We identified only 2% (n = 1) of patients with PR according to RECIST as compared with as much as 27.5% (n = 14) using Choi criteria (compare Table 2). This was the most striking disagreement when response evaluations with RECIST and Choi criteria were compared. This discrepancy was due to a decrease in tumor diameter between 10% and 30% in 8 patients, a decrease in tumor density in 10 patients, and due to both in 2 patients. In result, cystic transformation may not be a very sensitive parameter to detect tumor response, as it was observed in only 60% (n = 12) of patients identified as PR according to Choi criteria. Furthermore, irritation in Choi categorization arises as patients with an increase in tumor size may still be ranked as PR solely on the basis of a decrease in tumor density of >15%. This resulted in a dramatic discrepancy in response categorization as one patient had a tumor size increase of 25% and was subsequently rated PD according to RECIST but also demonstrated a decrease in tumor density of 36% and thus was rated PR according to Choi criteria. Interestingly, this patient displayed PD on subsequent follow-up and survived only 15.5 months. In two other patients with tumor growth of 31% and 60%, a decrease in tumor 4 Dudeck et al.
5 original article Figure 2. Overall survival of patients with advanced gastrointestinal stromal tumor according to response evaluation with RECIST and Choi criteria at 3 months of treatment with sunitinib. PR, partial remission; SD, stable disease; PD, progressive disease. density of 11% each was found, almost consequenting a similar discrepancy in tumor response evaluation by RECIST and Choi criteria, but general conclusions should not be drawn from these case-based observations. In addition, certain variations of parenchymal enhancement on contrast-enhanced CT have to be taken into account, particularly when a scanning protocol with fixed scan delay after administration of contrast media is applied. Nevertheless, even with the use of bolus tracking as a simple and repeatable CT technique to achieve scans with comparable parenchymal HU, we advise caution to evaluate treatment response primarily on tumor density changes. Undoubtedly, validation of Choi criteria on a large independent dataset is urgently needed. Moreover, an analysis of the largest imatinib GIST trial published to date showed that the much simpler RECIST were sufficient to exclude PD, which turned out to be an excellent predictive marker of benefit [16]. This absence of tumor progression has also been highlighted by the Soft Tissue and Bone Sarcoma Group of European Organization for Research and Treatment of Cancer for patients with soft tissue sarcomas treated with new agents as well as with classic cytotoxic drugs, as outcomes were similar for patients with prolonged SD as compared with those who experienced PR [20 22]. Our data confirm this finding, which again emphasizes the importance of absence of tumor progression as a highly relevant measure of therapeutic benefit. In conclusion, second-line therapy with sunitinib resulted in a long-term disease stabilization of patients with advanced GIST after failure of imatinib or intolerance. Objective tumor shrinkage measured on the basis of RECIST was an uncommon finding, but patients rated as SD demonstrated similar PFS and OS as compared with patients rated as PR or SD with Choi criteria. The most important predictive marker of therapeutic benefit was absence of progression, no matter which response evaluation criteria were applied. acknowledgement Several patients have been treated within the context of a clinical trial (ClinicalTrials.gov identifier: NCT ). disclosure The authors declare no conflict of interest. references 1. Dagher R, Cohen M, Williams G et al. Approval summary: imatinib mesylate in the treatment of metastatic and/or unresectable malignant gastrointestinal stromal tumors. Clin Cancer Res 2002; 8: van Oosterom AT, Judson I, Verweij J et al. Safety and efficacy of imatinib (STI571) in metastatic gastrointestinal stromal tumours: a phase I study. Lancet 2001; 358: Demetri GD, von Mehren M, Blanke CD et al. Efficacy and safety of imatinib mesylate in advanced gastrointestinal stromal tumors. N Engl J Med 2002; 347: Judson I, Demetri G. Advances in the treatment of gastrointestinal stromal tumours. Ann Oncol 2007; 18 (Suppl 10): x20 x Demetri GD, van Oosterom AT, Garrett CR et al. Efficacy and safety of sunitinib in patients with advanced gastrointestinal stromal tumour after failure of imatinib: a randomised controlled trial. Lancet 2006; 368: Roskoski R Jr.. Sunitinib: a VEGF and PDGF receptor protein kinase and angiogenesis inhibitor. Biochem Biophys Res Commun 2007; 356: doi: /annonc/mdq696 5
6 original article 7. Blay JY. Pharmacological management of gastrointestinal stromal tumours: an update on the role of sunitinib. Ann Oncol 2010; 21: Stroobants S, Goeminne J, Seegers M et al. 18FDG-Positron emission tomography for the early prediction of response in advanced soft tissue sarcoma treated with imatinib mesylate (Glivec). Eur J Cancer 2003; 39: Antoch G, Kanja J, Bauer S et al. Comparison of PET, CT, and dual-modality PET/CT imaging for monitoring of imatinib (STI571) therapy in patients with gastrointestinal stromal tumors. J Nucl Med 2004; 45: Choi H, Charnsangavej C, Faria SC et al. Correlation of computed tomography and positron emission tomography in patients with metastatic gastrointestinal stromal tumor treated at a single institution with imatinib mesylate: proposal of new computed tomography response criteria. J Clin Oncol 2007; 25: Choi H, Charnsangavej C, de Castro FS et al. CT evaluation of the response of gastrointestinal stromal tumors after imatinib mesylate treatment: a quantitative analysis correlated with FDG PET findings. AJR Am J Roentgenol 2004; 183: Holdsworth CH, Badawi RD, Manola JB et al. CT and PET: early prognostic indicators of response to imatinib mesylate in patients with gastrointestinal stromal tumor. AJR Am J Roentgenol 2007; 189: Vanel D, Albiter M, Shapeero L et al. Role of computed tomography in the follow-up of hepatic and peritoneal metastases of GIST under imatinib mesylate treatment: a prospective study of 54 patients. Eur J Radiol 2005; 54: Van den Abbeele AD, Badawi RD. Use of positron emission tomography in oncology and its potential role to assess response to imatinib mesylate therapy in gastrointestinal stromal tumors (GISTs). Eur J Cancer 2002; 38 (Suppl 5): S60 S Benjamin RS, Choi H, Macapinlac HA et al. We should desist using RECIST, at least in GIST. J Clin Oncol 2007; 25: Le Cesne A, Van Glabbeke M, Verweij J et al. Absence of progression as assessed by response evaluation criteria in solid tumors predicts survival in advanced GI stromal tumors treated with imatinib mesylate: the intergroup EORTC-ISG-AGITG phase III trial. J Clin Oncol 2009; 27: Therasse P, Arbuck SG, Eisenhauer EA et al. New guidelines to evaluate the response to treatment in solid tumors. European Organization for Research and Treatment of Cancer, National Cancer Institute of the United States, National Cancer Institute of Canada. J Natl Cancer Inst 2000; 92: Reichardt P, Kang YK, Ruka W et al. Detailed analysis of survival and safety with sunitinib in a worldwide treatment-use trial of patients with advanced GIST. J Clin Oncol 2008; 26 (Suppl): (Abstr 10548). 19. George S, Blay JY, Casali PG et al. Clinical evaluation of continuous daily dosing of sunitinib malate in patients with advanced gastrointestinal stromal tumour after imatinib failure. Eur J Cancer 2009; 45: Le Cesne A, Blay JY, Judson I et al. Phase II study of ET-743 in advanced soft tissue sarcomas: a European Organisation for the Research and Treatment of Cancer (EORTC) Soft Tissue and Bone Sarcoma Group Trial. J Clin Oncol 2005; 23: Le Cesne A, Judson I, Crowther D et al. Randomized phase III study comparing conventional-dose doxorubicin plus ifosfamide versus high-dose doxorubicin plus ifosfamide plus recombinant human granulocyte-macrophage colony-stimulating factor in advanced soft tissue sarcomas: a trial of the European Organization for Research and Treatment of Cancer/Soft Tissue and Bone Sarcoma Group. J Clin Oncol 2000; 18: Van Glabbeke M, van Oosterom AT, Oosterhuis JW et al. Prognostic factors for the outcome of chemotherapy in advanced soft tissue sarcoma: an analysis of 2,185 patients treated with anthracycline-containing first-line regimens a European Organization for Research and Treatment of Cancer Soft Tissue and Bone Sarcoma Group Study. J Clin Oncol 1999; 17: Dudeck et al.
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