Comparison of Doxorubicin and Weekly Paclitaxel Efficacy in Metastatic Angiosarcomas
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1 Comparison of Doxorubicin and Weekly Paclitaxel Efficacy in Metastatic Angiosarcomas Antoine Italiano, MD, PhD 1,2 ; Angela Cioffi, MD 2,3 ; Nicolas Penel, MD, PhD 4 ; Matteo Giaj Levra, MD 3 ; Corinne Delcambre, MD 5 ; Elsa Kalbacher, MD 6 ; Christine Chevreau, MD 7 ; François Bertucci, MD, PhD 8 ; Nicolas Isambert, MD 9 ; Jean-Yves Blay, MD, PhD 10 ; Binh Bui, MD 1 ; Cristina Antonescu, MD 2 ; David R. D Adamo, MD 2 ; Robert G. Maki, MD, PhD 11 ; and Mary Louise Keohan, MD 2 BACKGROUND: Data regarding the role of anthracyclines and taxanes as first-line treatments of metastatic angiosarcoma are limited. METHODS: Records of 117 metastatic angiosarcoma patients who were treated with either doxorubicin or weekly paclitaxel were reviewed. RESULTS: Seventy-five patients (64%) were treated with weekly paclitaxel and 42 (36%) with single-agent doxorubicin. Patients in the weekly paclitaxel group were older and more frequently had angiosarcomas arising from the skin. In the doxorubicin group, 34 patients were evaluable for response: 2 (6%) had complete response, 8 (23.5%) had partial response, 10 (29.5%) had stable disease, and 14 (41%) had progressive disease. In the weekly paclitaxel group, 68 patients were evaluable for response: 9 (13%) had complete response, 27 (40%) had partial response, 20 (29.5%) had stable disease, and 12 (17.5%) had progressive disease. Objective responses to weekly paclitaxel were more frequent in cutaneous angiosarcomas, whereas tumor location did not impact response to doxorubicin. Median progression-free survival (PFS) was 4.9 months (95% confidence interval [95% CI], months). Median overall survival (OS) was 8.5 months (95% CI, months). On multivariate analysis, ECOG performance status (PS) was the sole independent factor associated with PFS and OS. CONCLU- SIONS: First-line single-agent doxorubicin and weekly paclitaxel seem to have similar efficacy in metastatic angiosarcomas. Cutaneous angiosarcomas respond favorably to weekly paclitaxel. Best supportive care should be considered in patients with poor PS. Cancer 2012;118: VC 2011 American Cancer Society. KEYWORDS: angiosarcoma, chemotherapy, doxorubicin, paclitaxel, prognosis. Angiosarcoma represents a rare (< 2%) subgroup of soft tissue sarcomas (STS) characterized by an aggressive clinical behavior. 1 Radical surgery and adjuvant radiotherapy when indicated represent the cornerstone of treatment for patients with localized disease. However, despite an adequate locoregional treatment, up to 50% of patients will develop metastatic relapse and will die of disease. 2 The role of chemotherapy in advanced angiosarcomas is not clear. Indeed, the interpretation of the literature related to this topic is complicated by the fact that prospective studies have, until recently, considered STS as a homogeneous tumor type, with chemotherapy comprising essentially doxorubicin and/or ifosfamide in various regimens. Because multiagent chemotherapy has not been shown superior to single-agent chemotherapy with doxorubicin alone in term of overall survival (OS), doxorubicin monotherapy is still considered the first-line standard treatment for patients with metastatic STS. 3 In recent years, however, the insight has emerged that systemic therapy should become more tailored, in particular with respect to specific sarcoma histology. This approach is clearly illustrated by the remarkable efficacy of imatinib in advanced dermatofibrosarcoma protuberans, 4,5 the significant activity of gemcitabine in Corresponding author: Antoine Italiano, MD, PhD, Institut Bergonié, 229 Cours de l Argonne, Bordeaux Cedex, France; Fax: (011) ; italiano@bergonie.org 1 Department of Medical Oncology, Institut Bergonié, Bordeaux, France; 2 Sarcoma Service, Memorial Sloan-Kettering Cancer Center, New York, New York; 3 Department of Medicine, Institut Gustave Roussy, Villejuif, France; 4 Department of Medical Oncology, Centre Oscar Lambret, Lille, France; 5 Department of Medical Oncology, Centre François Baclesse, Caen, France; 6 Department of Medical Oncology, Centre Hospitalier Universitaire Besançon, Besançon, France; 7 Department of Medical Oncology, Institut Claudius Regaud, Toulouse, France; 8 Department of Medical Oncology, Institut Paoli Calmettes, Marseille, France; 9 Department of Medical Oncology, Centre Georges-François Leclerc, Dijon, France; 10 Department of Medical Oncology, Centre Léon Bérard, Lyon, France; 11 Departments of Medicine and Pediatric Hematology/Oncology, Mount Sinai School of Medicine, New York, New York We thank Dr Emmanuelle Bompas, Dr Didier Cupissol, and Professor Florence Duffaud for providing patient data. The first 2 authors (visiting investigators at the Memorial Sloan Kettering Cancer Center) contributed equally to this study. DOI: /cncr.26599, Received: May 17, 2011; Revised: July 6, 2011; Accepted: July 11, 2011, Published online November 1, 2011 in Wiley Online Library (wileyonlinelibrary.com) 3330 Cancer July 1, 2012
2 Chemotherapy in Angiosarcomas/Italiano et al leiomyosarcomas, 6,7 of trabectedin in myxoid/round cell liposarcomas, 8 and of mtor (mammalian target of rapamycin) inhibitors in perivascular epithelioid cell tumors (PEComas). 9,10 Interestingly, single case reports, single-center retrospective series, and 1 histology-specific phase 2 study 19 have shown that paclitaxel, a drug considered inactive against STS, has significant activity in angiosarcomas, particularly when administered in a weekly schedule. Therefore, STS guidelines recommend paclitaxel as an alternative option to single-agent doxorubicin in this specific histological type. 20 However, angiosarcoma itself represents a heterogeneous group of tumors with distinct presentations, natural history, and genomic profiles, depending on etiology and tumor location. 2,21,22 The aim of this multi-institutional, retrospective study is to compare the respective efficacy of single-agent doxorubicin and weekly paclitaxel and to identify predictive factors of outcome that may help clinicians choose the more appropriate regimen for their patients. MATERIALS AND METHODS Patients From 1990 to 2010, 269 patients with a diagnosis of metastatic angiosarcoma were admitted to 1 of the 14 participating institutions (13 institutions of the French Sarcoma Group and the Memorial Sloan-Kettering Cancer Center, New York, NY). Clinical and pathologic data were collected by reviewing medical records and were entered in a comprehensive database. The histological diagnosis was established according to the World Health Organization Classification of Tumours 1 by an expert pathologist. Among these patients, 117 patients received single-agent doxorubicin (60-75 mg/m 2 on day 1, cycle ¼ day 21) or weekly paclitaxel (typically 80 mg/m 2 /day on days 1, 8, 15, cycle ¼ day 28) in the first-line setting. Treatments and Evaluation The choice of chemotherapy regimen and duration of treatment were at the discretion of the treating physician. The best response to treatment was evaluated by magnetic resonance imaging or computed tomography according to Response Evaluation Criteria in Solid Tumours (RECIST). 23 Progression-free survival (PFS) was defined as the time from the start of chemotherapy until disease progression, death, or last patient contact. OS was defined as the time from the start of chemotherapy until death or last patient contact. Statistical Analysis The statistical analysis of baseline demographics and clinical outcome is based on all data available up to the cutoff date of December 30, Survival rates were estimated with the use of the Kaplan-Meier method. Descriptive statistics were used to show the distribution of variables in the population. Differences between groups were evaluated by the chi-square test or Fisher exact test for categorical variables and the Student t test for continuous variables. Prognostic factors were planned to be identified by univariate and multivariate analyses by using the Cox regression model. Variables tested in univariate analysis included: age (< 63 years vs 64 years), sex, primary tumor location (cutaneous angiosarcoma vs other locations), histological subtype (epithelioid vs nonepithelioid), primary versus radiation-induced angiosarcoma, synchronous versus metachronous metastases, number of metastatic sites (1 vs 2), metastatic sites (nonvisceral vs visceral), Eastern Cooperative Oncology Group performance status (PS) (0 or 1 vs 2), and type of chemotherapy regimen (doxorubicin vs weekly paclitaxel). Variables associated with PFS or OS with a P value <.05 in the univariate analysis were included in the multivariate regression. Analyses were performed using SPSS version 12.0 statistical software (SPSS Inc, Chicago, Ill). All statistical tests were 2-sided, and P <.05 was used to define statistical significance. RESULTS Patients and Treatments The study population included 117 patients. Their characteristics are described in Table 1. Seventy-five patients (64%) were treated with weekly paclitaxel and 42 (36%) with single-agent doxorubicin. Patients in the weekly paclitaxel group were significantly more likely to be older and to have angiosarcomas arising from the skin. Response In the doxorubicin group, 34 patients were evaluable for response: 2 (6%) had complete response, 8 (23.5%) had partial response, 10 (29.5%) had stable disease (6 of them lasting > 6 months), and 14 (41%) had progressive disease. In the weekly paclitaxel group, 68 patients were evaluable for response: 9 (13%) had complete response, 27 (40%) had partial response, 20 (29.5%) had stable disease (9 of them lasting > 6 months), and 12 (17.5%) had progressive disease. In the doxorubicin group, the clinicopathologic factors significantly associated with a higher objective response rate were: radiation-related Cancer July 1,
3 Table 1. Patient Characteristics (N ¼ 117) Characteristic Weekly Paclitaxel (n 5 75) No. of Patients (%) Doxorubicin (n 5 42) No. of Patients (%) Age, y Median Range y 21 (28) 4 (9.5) Sex Male 28 (37.5) 21 (50).24 Female 47 (63.5) 21 (50) Primary tumor location Cutaneous 25 (33.5) 3 (7).001 Extracutaneous 50 (66.5) 39 (93) Histological subtype Epithelioid 11 (14.5) 4 (9.5) Nonepithelioid 48 (64) 28 (66.5).72 Unknown 16 (22.5) 10 (24) Grade 1 5 (6.5) 3 (7) 2 9 (12) 10 (24) (52) 17 (40.5) Unknown 22 (29.5) 12 (28.5) Etiology Primary 54 (72) 27 (64).41 Radiation-induced 21 (28) 15 (36) Metastatic disease Synchronous 38 (50.5) 29 (69).055 Metachronous 37 (49.5) 13 (31) No. of metastatic sites 1 17 (22.5) 5 (6.5) (67.5) 37 (93.5) Sites of metastases Nonvisceral 24 (32) 8 (19).13 Visceral 51 (68) 34 (81) ECOG performance status 1 47 (62.5) 20 (47.5) (26.5) 15 (36) Unknown 8 (11) 7 (16.5) Abbreviation: ECOG, Eastern Cooperative Oncology Group. etiology (50% vs 15%; P ¼.03) and absence of visceral metastasis (74% vs 42%; P ¼.015). In the paclitaxel group, the clinicopathologic factors significantly associated with a higher objective response rate were: age > 64 years (66.5% vs 34.5%; P ¼.009), radiation-related etiology (74% vs 45%; P ¼.03), cutaneous primary tumor site (78% vs 40%; P ¼.003), absence of visceral metastasis (66.7% vs 21.5%; P ¼.03), and 1 metastatic site versus 2 metastatic sites (75% vs 46%; P ¼.04). The objective P response rate was significantly higher in the weekly paclitaxel group than in the doxorubicin group (53% vs 29%; P ¼.02). Because the primary tumor site was the sole characteristic significantly unbalanced between the 2 groups, an analysis restricted to the group of noncutaneous angiosarcomas was performed. No significant difference in terms of objective response rate between weekly paclitaxel and doxorubicin was observed in this subgroup (40% vs 26%; P ¼.2). Survival The median follow-up was 37.8 months (range, months). Median PFS was 4.9 months (95% confidence interval [CI], months) (Fig. 1A). The 3-month, 6-month, and 1-year PFS rates were 66% (95% CI, 64-69%), 38% (95% CI, 29-47%), and 18% (95% CI, 13-23%), respectively. On univariate analysis, extracutaneous location, visceral metastases, > 1 metastatic site, and a PS 2 were adverse prognostic factors for PFS (Table 2). On multivariate analysis, PS was the sole factor independently associated with PFS, with a hazard ratio of 1.9 (95% CI, 1.2-3; P ¼.003). At the time of analysis, 94 patients (64%) had died and 23 (36%) were still alive. Eighty-six deaths (91.5%) were related to the disease, and 2 were related to the toxicity of chemotherapy (1 patient with neutropenic sepsis in each treatment group). A total of 25 deaths (26.5%) occurred < 3 months after the onset of chemotherapy, and 15 of these patients (60%) had a PS 2 when treatment was started. Median OS was 8.5 months (95% CI, months) (Fig. 1B). The 6-month, 1-year, and 2- year OS rates were 63% (95% CI, 55-71%), 37% (95% CI, 34-41%), and 19% (95% CI, 17-22%), respectively. On univariate analysis, male sex, extracutaneous location, visceral metastases, > 1 metastatic sites, a PS 2, and single-agent doxorubicin were adverse prognostic factors for OS (Table 2). On multivariate analysis, PS was the sole factor independently associated with OS, with a hazard ratio of 2.7 (95% CI, ; P <.0001). Patient Care After First-Line Chemotherapy Data regarding the management of patients after first-line chemotherapy were available for 43 individuals. Twentysix patients (18 patients in the weekly paclitaxel group, 8 patients in the doxorubicin group) received at least 1 new line of chemotherapy. The proportion of patients receiving second-line chemotherapy was similar in the paclitaxel group and in the doxorubicin group (64% vs 53%; P ¼.7) Cancer July 1, 2012
4 Chemotherapy in Angiosarcomas/Italiano et al Figure 1. Kaplan Meier curves for (A,C) progression-free survival and (B,D) overall survival of (A,B) the entire cohort of patients and (C,D) according to performance status (PS). Blue line indicates a PS of 1; green line, PS 2. Several types of chemotherapy regimen were used. In the second-line setting, 3 patients out of 26 experienced an objective response (partial response): 2 patients from the weekly paclitaxel group (1 was treated with secondline pegylated liposomal doxorubicin and the other with second-line gemcitabine) and 1 patient from the doxorubicin group who was treated with second-line weekly paclitaxel plus bevacizumab. Median PFS was 1.9 months (95% CI, months). DISCUSSION To the best of our knowledge, this study represents the largest series of metastatic angiosarcoma patients treated in first-line with either single-agent doxorubicin or weekly Cancer July 1,
5 Table 2. Significant Prognostic Factors on Progression-Free and Overall Survival (Univariate Analysis) PFS OS Variable Median (95% CI), Months P Median (95% CI), Months P Whole population 4.9 (3.9-6) 8.5 ( ) Sex Female 5.2 ( ) NS 10.3 ( ).02 Male 4.4 ( ) 6.1 ( ) Primary tumor location Cutaneous 8.9 ( ) ( ).01 Extracutaneous 3.8 ( ) 7.5 ( ) Sites of metastases Nonvisceral 8.9 ( ) ( ).01 Visceral 4.2 ( ) 7.7 ( ) No. of metastatic sites ( ) ( ) ( ) 7.8 ( ) ECOG performance status ( ) ( ) < ( ) 3.7 ( ) Chemotherapy regimen Doxorubicin 3 ( ) NS 5.5 ( ).002 Weekly paclitaxel 5.8 (5-6.6) 10.3 ( ) Abbreviations: CI, confidence interval; ECOG, Eastern Cooperative Oncology Group; NS, not significant; OS, overall survival; PFS, progression-free survival. paclitaxel. Our results showed that cytotoxic chemotherapy was associated with a clinical benefit (objective response plus stable disease > 6 months) in approximately 60% of patients, indicating the relatively high chemosensitivity of this sarcoma subtype. In our series, weekly paclitaxel was the most frequent regimen used in the first-line setting. This underscores the increasing use of histologydriven chemotherapy regimen for the treatment of advanced soft-tissue sarcoma, even if no level 1 evidence is available. Indeed, the strength of evidence that is achievable in common cancers is difficult to achieve in the field of soft-tissue sarcomas. Therefore, retrospective studies are informative and are used for therapeutic decision-making by medical oncologists involved in the management of rare tumors. Our results suggest that single-agent doxorubicin and weekly paclitaxel have similar efficacy in angiosarcomas. Doxorubicin was associated with an objective response rate of 29.5% but a median PFS of only 3 months. These results are in agreement with the limited available literature consisting of a phase 2 study showing response in 1 of 3 angiosarcoma patients treated with single-agent doxorubicin 24 and in a retrospective series of 12 patients showing a PFS of 3.7 months. 17 Weekly paclitaxel was associated with an objective response rate of 53% and a longer median PFS of 5.8 months. These results also confirm those of previous smaller retrospective series showing response rates ranging between 62% and 89% and PFS between 4 and 7.6 months In our series, objective responses to weekly paclitaxel were more frequent in angiosarcomas arising from the skin, whereas tumor location did not affect response to doxorubicin. This confirms the higher sensitivity to paclitaxel of cutaneous angiosarcomas, which was previously suggested in retrospective studies and in a small histology-specific phase 2 trial. 19 Therefore, at least 1 reason for the higher response rate observed in the weekly paclitaxel group was the imbalance in the proportion of cutaneous angiosarcomas between the 2 groups. Moreover, no significant difference in terms of PFS was observed. This suggests that PFS, rather than objective tumor response, is a better endpoint for future randomized phase 2 trials assessing the activity of potential new agents of interest compared with existing therapeutic strategies (doxorubicin, weekly paclitaxel). Moreover, in our experience, evaluation by RECIST is difficult for cutaneous angiosarcomas. Interestingly, objective responses were more frequent in radiation-induced angiosarcomas than in primary angiosarcomas, irrespective of the drug used. Radiation-induced angiosarcomas are characterized by a consistent amplification of the MYC oncogene. 22 Several preclinical studies have suggested that MYC overexpression sensitizes tumor cells to radiotherapy and chemotherapy, although conflicting results have been reported Our data seem to support the contention of relative sensitivity of c-myc overexpressing angiosarcomas. However, we have also observed objective response in primary angiosarcomas, and a significant percentage of secondary angiosarcomas did not respond to chemotherapy. Therefore, although the predictive value of MYC amplification may deserve 3334 Cancer July 1, 2012
6 Chemotherapy in Angiosarcomas/Italiano et al further investigation, it is likely that other molecular aberrations are involved in the sensitivity of angiosarcomas to anticancer drugs. Further studies are needed in this setting. For instance, a recent in vitro study suggested that mutations of VEGFR2 (vascular endothelial growth factor receptor 2; KDR), which are present in approximately 10% to 15% of angiosarcomas, may be predictive of efficacy of tyrosine kinase inhibitors targeting this crucial receptor of angiogenesis. 33 In our series, the sole clinical factor associated with PFS and OS was PS. PS was already found to be a crucial prognostic factor for OS in large STS database studies. 34 More recently, PS 2 was also identified as the most significant risk factor for early death (<3 months) in advanced STS patients who were treated with first-line chemotherapy. 35 Of note, in our study, 26.5% of deaths occurred < 3 months after onset of chemotherapy, and 60% of these patients had a PS 2 when treatment was started. Considering the high risk of early death of patients who have poor PS, the decision to administer chemotherapy instead of best supportive care should be carefully assessed in this setting, given its potential lack of benefit. The retrospective design of this study did not allow us to report exhaustively the adverse events related to chemotherapy. However, the review of the medical records indicated that the majority of patients did not exhibit significant complications, except for 2 deaths due to neutropenic sepsis. Because weekly paclitaxel and doxorubicin appears to have similar efficacy, the comorbidities and the preference of the patients should be considered for the choice of the chemotherapy regimen. In our series, the majority of elderly patients (aged 75 years) received weekly paclitaxel. This may be related to the fact that many medical oncologists are still reluctant to use anthracyclines in elderly patients because of concerns about cardiac tolerance. 36 However, our data indicate that weekly paclitaxel may represent an efficient alternative to doxorubicin in elderly patients, in particular those with cardiac and respiratory comorbidities that preclude the use of cardiotoxic drugs. Alternatively, low-dose weekly doxorubicin 37 or other forms of anthracyclines such as liposomal pegylated doxorubicin 16,17 may provide other means to treat angiosarcomas in an older population. The French Sarcoma Group has recently shown in a retrospective study that included 149 angiosarcoma patients treated with miscellaneous chemotherapy regimens that chemotherapy improves outcome in comparison with best supportive care. 38 By extending our initial data set, this European-American collaborative study confirms that angiosarcomas are at least initially chemosensitive, and indicates that doxorubicin and weekly paclitaxel appear largely equivalent in terms of efficacy in the first-line setting. However, the OS of patients of metastatic angiosarcoma remains poor. Recently, gemcitabine was shown to have some clinical efficacy, 39 and antiangiogenic agents 40,41 are also under investigation with at least minor activity. Moreover, a combination chemotherapy regimen might be associated with improved outcome in a subset of angiosarcoma patients, as suggested by Fury et al in a study showing higher PFS in 6 patients who were treated with doxorubicin-ifosfamide combined chemotherapy. 17 Further collaborative studies are needed to refine the role of new therapeutic options in the management of this rare disease. FUNDING SUPPORT No specific funding was disclosed. CONFLICT OF INTEREST DISCLOSURES The authors made no disclosures. REFERENCES 1. Fletcher CDM, Unni KK, Mertens F. World Health Organization Classification of Tumours: Pathology and Genetics of Tumours of Soft Tissue and Bone. Lyon, France: IARC Press; Fayette J, Martin E, Piperno-Neumann S, et al. Angiosarcomas, a heterogeneous group of sarcomas with specific behavior depending on primary site: a retrospective study of 161 cases. Ann Oncol. 2007;18: Bramwell VH, Anderson D, Charette ML; Sarcoma Disease Site Group. 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