Clinical outcome of leiomyosarcomas of vascular origin: comparison with leiomyosarcomas of other origin

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1 Annals of Oncology 21: , 2010 doi: /annonc/mdq039 Published online 18 February 2010 Clinical outcome of leiomyosarcomas of vascular origin: comparison with leiomyosarcomas of other origin A. Italiano 1 *, M. Toulmonde 1, E. Stoeckle 2, M. Kind 3, G. Kantor 4, J.-M. Coindre 5 & B. Bui 1 Departments of 1 Medical Oncology; 2 Surgery; 3 Radiology; 4 Radiotherapy and 5 Pathology, Institut Bergonie, Bordeaux, France. Received 5 November 2009; revised 11 January 2010; accepted 12 January 2010 Background: There are no data about the natural history of leiomyosarcoma of vascular origin (vlms) in comparison with leiomyosarcoma (LMS) of other origin and about the management of advanced disease. Methods: Among 1472 patients diagnosed with sarcoma from January 1980 to December 2008 at our institution, 195 patients (13%) had LMS. LMS had a vascular origin in 14 cases (7%). Results: Patients with vlms had a significantly worse median metastasis-free survival (MFS) (0.25 versus 9.6 years, P = 0.001) and overall survival (OS; 2.1 versus 7 years, P < ) than patients with LMS of other origin. On multivariate analysis, grade and vascular origin were the sole independent adverse prognostic factors for OS. Eight metastatic patients with vlms received a first-line anthracycline chemotherapy regimen. Two patients had partial response, four had stable disease and two had progressive disease. OS of patients with metastatic vlms was not significantly different from that observed in patients with metastatic LMS of other origin (22.1 versus 16.5 months, P = 0.84). Conclusions: Vascular origin is an independent adverse prognostic factor for MFS and OS in patients with LMS. Patients with metastatic vlms had a similar outcome than patients with metastatic LMS of other origin. Key words: chemotherapy, leiomyosarcoma of vascular origin introduction Leiomyosarcomas of vascular origin (vlmss) are extremely rare lesions representing less than one in every malignant tumors [1]. Clinical descriptions are mainly limited to single case reports and only few instances are recorded in several large autopsy series [1]. The sites most frequently involved are large veins such as the vena cava. Pulmonary and systemic arteries locations are exceptional. The prognosis for patients with vlmss is very poor [2 5]. Surgery is the cornerstone of treatment and represents frequently a challenge even for the most experienced surgeons because of disease location. More than 50% of patients with complete macroscopic resection experienced disease recurrence and died of disease progression [2 6]. Moreover, many patients present with locally advanced or metastatic disease at the time of initial diagnosis and are not amenable to surgery. Due to its rarity, no comparison has never been made between vascular and nonvascular soft tissue leiomyosarcomas (LMSs). Moreover, there are no data about the medical management and the role of chemotherapy in patients with advanced vlmss. We report here the first series addressing these specific issues. *Correspondence to: Dr. A. Italiano, Department of Medical Oncology, Institut Bergonié, 229 cours de l Argonne, Bordeaux Cedex, France. Tel: ; Fax: ; italiano@bergonie.org patients and methods patients From 1980 to 2008, 1472 adult patients ( 16 years old) with a diagnosis of soft tissue sarcoma were admitted to our institution (Institut Bergonie, Bordeaux, France). Clinical and pathologic data were collected by reviewing medical records and were entered in a comprehensive database. Among these patients, 195 (13%) had a LMS. LMS had a vascular origin in 14 cases (7%). Histological diagnosis was confirmed for all patients by the same pathologist (J-MC), according to the World Health Organization (WHO) Classification of Tumors [7]. Tumor grade was evaluated according to the Fédération Nationale des Centres de Lutte Contre le Cancer grading system [8, 9]. Variables collected from the medical records included demographic data, tumor characteristics and staging, treatment, patterns of recurrence and followup. Cause of death was coded according to the WHO classification [10]. statistical analyses The statistical analyses of baseline demographics and clinical outcomes were based on all data available up to the cut-off date of 30 April Tumor response was assessed according to RECIST [11]. Overall survival (OS) was defined as the interval between diagnosis and the time of death. Progression-free survival was defined for patients treated with chemotherapy as the interval between initiation of chemotherapy and the time of progression or death from any cause. Univariate and multivariate analyses were carried out using Cox regression and included the following variables: age (<50 or 50 years), sex, tumor size (<5 or 5 cm), tumor site (extremities, internal trunk, head and neck and trunk wall), tumor depth (superficial or deep), grade according to the FNCLCC 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@oxfordjournals.org

2 system and vascular origin (yes or no). Variables that were associated with survival with a P value <.05 in the univariate analysis were included in the multivariate regression. Analyses were carried out using SPSS 12.0 statistical software (SPSS Inc., Chicago, IL). All statistical tests were two-sided, and P values <.05 indicated statistical significance. results patients The study population included 195 patients. Their characteristics are summarized in Table 1. Fourteen patients had a vlms Annals of Oncology (Table 2). Tumors arose from veins in 12 cases (86%) and from systemic arteries in only 2 cases (14%). Inferior vena cava was the most frequent tumor location (36%). vlmss tend to be larger ( 5 cm) than LMSs of other origin (93% versus 74%, P = 0.09) and are characterized by a higher rate of synchronous metastases than LMS of other origin (36% versus 15%, P = 0.04). patterns of treatment of patients with vascular LMSs localized setting. At diagnosis, nine vlms patients presented with localized disease (Figures 1 3). Patterns of care and Table 1. Patients characteristics Characteristic All (N = 195) Nonvascular leiomyosarcoma (N = 181) Vascular leiomyosarcoma (N = 14) P value No. of patients % No. of patients % No. of patients % Age, years 0.29 < Sex 0.51 Male Female Size, cm 0.09 < Location 0.06 Superficial Deep Anatomic site 0.42 Extremities Head and neck Trunk wall Internal trunk FNCLCC grade 0.21 Grade Grade Grade Unknown FNCLCC, Fédération Nationale des Centres de Lutte Contre le Cancer. Table 2. Characteristics of patients with vascular leiomyosarcomas (N = 14) Patient Sex/age Eastern Cooperative Oncology Group Tumor site Tumor size Grade Metastases at diagnosis 1 Female/69 1 Great saphenous vein 10 3 No 2 Male/49 2 Inferior vena cava 10 2 No 3 Male/68 1 Great saphenous vein 10 2 Yes Lung 4 Female/83 1 Great saphenous vein 10 3 No 5 Female/72 1 Femoral vein 7 3 No 6 Female/65 0 Popliteal vein 4 3 No 7 Female/84 3 Common iliac artery 15 3 Yes Lung 8 Male/73 3 Superficial femoral artery 15 3 No _ 9 Male/49 1 Great saphenous vein 9 2 No 10 Male/51 1 Inferior vena cava 6 3 Yes Lung 11 Male/59 1 Inferior vena cava 10 3 Yes Liver 12 Female/69 0 Inferior vena cava 9 2 No 13 Male/58 0 Inferior vena cava 8 3 Yes Liver 14 Male/77 1 Inferior vena cava 8 2 No Metastatic sites at diagnosis 1916 Italiano et al. Volume 21 No. 9 September 2010

3 Annals of Oncology original article Figure 1. Locoregional treatment of nine patients with localized leiomyosarcoma of vascular origin. Figure 2. Chemotherapy in 3 patients with localized leiomyosarcoma of vascular origin. outcome for these patients are detailed in Figure 1. Seven of them underwent resection with a curative intent. Complete gross resection was achieved in all these cases. Two patients (patients 2 and 12) with localized disease at presentation received doxorubicin-based chemotherapy in a neo-adjuvant setting. One of them (case 2) died of cardiac failure before Volume 21 No. 9 September 2010 doi: /annonc/mdq

4 Annals of Oncology Figure 3. Outcome of patients with metastatic leiomyosarcomas of vascular origin treated with chemotherapy. completion of the neo-adjuvant treatment and was not assessed for tumor response. One patient (case 14) was deemed unresectable because of locoregional extension and received palliative chemotherapy. Patients 12 and 14 were assessable for response. The best response according to RECIST criteria was stable disease in both cases. Five out of seven patients with complete resection received postoperative radiotherapy (RT), administered as external beam therapy. The median dose of external beam RT was 45 Gy (range Gy). In one case (case 6), additional brachytherapy by intraoperative seed implantation was carried out. metastatic setting. Ten patients presented with metastatic disease at diagnosis (n = 5) or during the course of their disease (n = 5). The sites of metastases were lung (n = 8), liver (n = 5), skin (n = 3), bone (n = 1) and brain (n = 1). Eight patients received chemotherapy for metastases (Table 3). All of them received an anthracycline-based regimen as first-line therapy Italiano et al. Volume 21 No. 9 September 2010

5 Annals of Oncology Their outcome is summarized in Figure 3. The best response was partial response in two cases, stable disease in four cases and progressive disease in two cases. Six patients received second line chemotherapy and one patient received four lines of chemotherapy. Surgical resection of metastases was carried out in only one patient (case 9). Two patients had not been treated with chemotherapy at the time of analysis because of poor cardiac function (case 4) or low-burden, asymptomatic disease (case 5). OS of patients with metastatic vlms was not significantly different from that observed in patients with metastatic LMS of other origin (median OS: 22.1 versus 16.5 months, P = 0.84). metastasis-free survival original article The median metastasis-free survival (MFS) for the entire cohort of LMS patients was 7.4 years [95% confidence interval (CI) ] (Tables 4 and 5, Figure 4). On univariate analysis, tumor site, tumor size, tumor depth, grade and vascular origin were significantly associated with MFS. On multivariate analysis, grade and vascular origin were the sole independent prognostic factors of MFS. Table 5. Independent prognostic factors on MFS and OS (multivariate analysis) Table 3. Chemotherapy regimens in patients with leiomyosarcoma of vascular origin Protocol Drugs MAID Doxorubicin 20 mg/m 2 (days 1 3) Ifosfamide 2.5 g/m 2 (days 1 3) Dacarbazine 300 mg/m 2 (days 1 3) AD Doxorubicin 20 mg/m 2 (days 1 3) Dacarbazine 300 mg/m 2 (days 1 3) Metronomic etoposide Oral daily etoposide 75 mg/day on 21 of 28-days cycle Metronomic cyclophosphamide Oral daily cyclophosphamide 50 mg/ day on 21 of 28-days cycle Doxorubicin Doxorubicin mg/m 2 Docetaxel gemcitabine Gemcitabine 900 mg/m 2 (days 1 and 8) Docetaxel 100 mg/m 2 (day 8) MAID, mesna, adriamycin, ifosfamide, dacarbazine; AD, adriamycin, dacarbazine. Table 4. Significant prognostic factors on MFS and OS (univariate analysis) Variable Hazard ratio 95% CI P value MFS FNCLCC grade Grade Grade Grade Vascular origin No Yes 1 OS FNCLCC grade Grade Grade Grade 3 1 Size, cm < Vascular origin Yes No 1 CI, confidence interval; FNCLCC, Fédération Nationale des Centres de Lutte Contre le Cancer; MFS, metastasis-free survival; OS, overall survival. Variable MFS OS Median MFS (years) 95% CI P value Median OS (years) 95% CI P value Whole population Anatomic Site Extremities (ns) Head and neck NR NR Internal trunk Trunk wall NR FNCLCC grade 1 NR 0.03 NR Location Superficial NR Deep Size, cm <5 NR < Vascular origin Yes < No CI, confidence interval; FNCLCC, Fédération Nationale des Centres de Lutte Contre le Cancer; MFS, metastasis-free survival; NR, median not reached; ns, not significant; OS, overall survival. Volume 21 No. 9 September 2010 doi: /annonc/mdq

6 Annals of Oncology Figure 4. Kaplan Meier curves of metastasis-free (A, C) and overall (B, D) survival of all patients entered into the study (A, B) and according to the vascular origin (C, D). overall survival The median OS for the entire cohort of LMS patients was 5.5 years (95% CI ) (Tables 4 and 5, Figure 4). On univariate analysis, tumor size, tumor depth, grade and vascular origin were significantly associated with OS. In particular, OS of patients with vlms was significantly worse than that of patients with LMS of other origin (median: 2 versus 7 years, P = ). On multivariate analysis, tumor size, grade and vascular origin are the sole independent prognostic factors of OS. discussion LMS is generally recognized as an aggressive disease with a generally poor prognosis compared with other soft tissue sarcomas. Only one study has compared the prognosis of vlms with LMS of other anatomic sites [12]. The authors reported similar prognosis in localized LMS of different origin. However, this study included only patients with LMS of the vena cava. Moreover, the comparison was not made with other soft tissue LMSs but mainly with a small series of selected cases of visceral LMS (stomach: n = 13, small intestine: n = 18 and uterus: n = 10). All these cases were diagnosed between October 1972 and November 1996, e.g. before the discovery of KIT mutations in stromal gastrointestinal tumors (GIST) and were not submitted to a central histological review [13]. Therefore, we believe that the gastric and intestinal LMSs included in this series were not true LMSs but GIST. Indeed, most tumors referred to as gastrointestinal leiomyomas and LMSs in the older medical literature are actually GISTs [14]. This may explain the similar or better outcome of LMS of the vena cava in comparison with the other cases included in this series Italiano et al. Volume 21 No. 9 September 2010

7 Annals of Oncology Our study identified vascular origin as an independent adverse prognostic factor for MFS and OS in patients with softtissue LMSs. In our experience, vlmss account for <2% of soft tissue sarcomas with the inferior vena cava representing the predominant location. In the context of localized disease, complete surgical resection of the vessel segment is the treatment of choice. However, surgery remains a challenge due to the location of the tumor. In our series, only eight patients (57%) had potentially resectable disease at diagnosis. This proportion is consistent with that of previous reports [6]. Due to its rarity, the role of neo-adjuvant chemotherapy and RT in the management of this rare disease is still unknown. RT has been indicated to improve outcome of patients with LMS of inferior vena cava [12]. In our small series, only one patient had local recurrence 27 months after the initial diagnosis. Of the five patients in our series who received adjuvant RT after resection of their primary tumor, one developed a local recurrence and four developed distant metastases. Of the two patients who did not receive adjuvant RT, one developed distant metastases without evidence of local recurrence and one remain disease free at last follow-up. In the series of Ito et al. [15], the rate of local recurrence was not significantly different between patients who received perioperative RT and those who did not. Of the eight patients who received perioperative RT, one developed a local recurrence, five developed distant metastases and two remained disease free at last follow-up. Altogether, such data indicate only a limited role of RT in the management of vlms which are essentially characterized by a metastatic risk. In our series, this metastatic risk is significantly higher than that observed for LMS of other origin. This difference remained significant even after exclusion in the second group of the superficial tumors, which are mainly cutaneous LMSs (data not shown). Several hypotheses may explain the higher metastatic potential of vlms. Obviously, the location of vlms favors hematogeneous spread. Intrinsic biological difference between vlms and LMS of other origin is possible but not likely. For instance, the proportion of patients with intermediate-grade (grade 2) and high-grade (grade 3) disease was similar between the two groups. Moreover, the survival of patients with metastatic disease was very similar, whatever the origin of the primary tumor. Another explanation of the high metastatic potential of vlms is related to a possible delay in diagnosis particularly for those originating form the inferior vena cava. This may explain the higher proportion of lesions 5 cm (93% versus 74%, P = 0.09) and the higher rate of synchronous metastases (36% versus 15%, P = 0.04) in the group of vlms even if theses difference were only marginally significant. There are no data in the literature about the outcome of patients with metastatic vlms. In our study, the objective response rate of vlms patients treated with first-line anthracycline-based chemotherapy was not different from the results reported by previous studies including patients with LMS of other sites [16, 17]. Moreover, our results demonstrated that the survival of patients with metastatic vlms was not different from that observed in patients with LMS of other sites. In our series, the two patients with metastatic LMS originating from peripheral arteria had the worst outcome. These data confirm that arterial LMSs tend to behave more aggressively than their venous counterparts as suggested by previous authors [18]. In conclusion, our study demonstrates that vascular origin is an independent adverse prognostic factor for MFS and OS in patients with LMS. For patients with advanced disease, standard medical management including first-line anthracycline-containing regimen produces survival results that are similar to those observed with other subtypes of LMSs. references original article 1. Enzinger F, Weiss S. Soft Tissue Tumors. St Louis: Mosby Kevorkian J, Cento DP. Leiomyosarcoma of large arteries and veins. Surgery 1973; 73: Stringer BD. Leiomyosarcoma of artery and vein. Am J Surg 1977; 134: Dzsinich C, Gloviczki P, van Heerden JA et al. Primary venous leiomyosarcoma: a rare but lethal disease. J Vasc Surg 1992; 15: Sakpal SV, Mehta R, Babel N, Chamberlain RS. Peripheral artery leiomyosarcoma. J Vasc Surg 2009; 49: Mingoli A, Cavallaro A, Sapienza P et al. International registry of inferior vena cava leiomyosarcoma: analysis of a world series on 218 patients. Anticancer Res. 1996; 16: Fletcher C, Unni K, Mertens F (eds). World Health Organization Classification of Tumours Pathology and Genetics of Tumours of Soft Tissue and Bone. 2002; IARC Press, Lyon. 8. Trojani M, Contesso G, Coindre JM et al. Soft-tissue sarcomas of adults; study of pathological prognostic variables and definition of a histopathological grading system. Int J Cancer 1984; 33: Guillou L, Coindre JM, Bonichon F et al. Comparative study of the National Cancer Institute and French Federation of Cancer Centers Sarcoma Group grading systems in a population of 410 adult patients with soft tissue sarcoma. J Clin Oncol 1997; 15: World Health Organization. International Classification of Diseases, 1965 Revision. Geneva, Switzerland: World Health Organization 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: Hines OJ, Nelson S, Quinones-Baldrich WJ, Eilber FR. Leiomyosarcoma of the inferior vena cava: prognosis and comparison with leiomyosarcoma of other anatomic sites. Cancer 1999; 85: Hirota S, Isozaki K, Moriyama Y et al. Gain-of-function mutations of c-kit in human gastrointestinal stromal tumors. Science 1998; 279: Miettinen M, Lasota J. Gastrointestinal stromal tumors definition, clinical, histological, immunohistochemical, and molecular genetic features and differential diagnosis. Virchows Arch. 2001; 438: Ito H, Hornick JL, Bertagnolli MM et al. Leiomyosarcoma of the inferior vena cava: survival after aggressive management. Ann Surg Oncol 2007; 14: 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: Penel N, Italiano A, Isambert N et al. Factors affecting the outcome of patients with metastatic leiomyosarcoma treated with doxorubicin-containing chemotherapy. Ann Oncol Oct 30. [Epub ahead of print] doi: /annonc/mdp Penel N, Taieb S, Ceugnart L et al. Report of eight recent cases of locally advanced primary pulmonary artery sarcomas: failure of Doxorubicin-based chemotherapy. J Thorac Oncol 2008; 3: Volume 21 No. 9 September 2010 doi: /annonc/mdq

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