Efficacy of carbon-ion radiotherapy and high-dose chemotherapy for patients with unresectable Ewing s sarcoma family of tumors
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1 DOI /s y ORIGINAL ARTICLE Efficacy of carbon-ion radiotherapy and high-dose chemotherapy for patients with unresectable Ewing s sarcoma family of tumors Shintaro Iwata Tsukasa Yonemoto Takeshi Ishii Kyoya Kumagai Reiko Imai Yoko Hagiwara Tadashi Kamada Shin-ichiro Tatezaki Received: 10 May 2012 / Accepted: 10 September 2012 Ó Japan Society of Clinical Oncology 2012 Abstract Background Treatment for unresectable Ewing s sarcoma family of tumors (ESFT) is a formidable challenge because of its high tendency for local and distant failure. Recently, carbon-ion radiotherapy (CIRT) has been applied to unresectable bone and soft tissue sarcoma. Additionally, highdose chemotherapy (HDC) with stem cell rescue has been used to improve the survival of patients with relapsed ESFT. Here we report our experience with CIRT and HDC in the treatment of unresectable ESFT. Methods Five unresectable ESFT patients including 4 who underwent CIRT and HDC and one who underwent CIRT from were retrospectively studied. After neoadjuvant chemotherapy, CIRT was conducted at the National Institute of Radiological Sciences in Chiba as local therapy. Consecutively, we employed HDC including busulfan, melphalan, and thiotepa with stem cell rescue. Results Two patients showed tumor shrinkage after CIRT, including 1 patient who achieved partial response. S. Iwata (&) T. Yonemoto T. Ishii S. Tatezaki Division of Orthopedic Surgery, Chiba Cancer Center, Nitona 666-2, Chuo-ku, Chiba , Japan siwata@chiba-cc.jp K. Kumagai Division of Hematology-Oncology, Chiba Cancer Center, Nitona 666-2, Chuo-ku, Chiba , Japan R. Imai T. Kamada Research Center Hospital for Charged Particle Therapy, National Institute of Radiological Sciences, Anagawa 4-9-1, Inage-ku, Chiba , Japan Y. Hagiwara Department of Orthopedic Surgery, Tokyo Women s Medical University, Kawada 8, Shinjuku-ku, Tokyo , Japan No severe acute toxicity related to CIRT was observed. Local failure was observed in only 1 patient at 22 months after CIRT. Four patients conducted HDC with stem cell rescue after CIRT and 1 patient suffered from venoocclusive disease just after HDC. Distant failure was observed in 3 patients after completion of the treatment. Conclusions CIRT and HDC for unresectable ESFT patients show favorable local control, with unsatisfactory results for distant control. Keywords Ewing s sarcoma family of tumors Unresectable tumor Carbon-ion radiotherapy High-dose chemotherapy Introduction The treatment of patients with Ewing s sarcoma family of tumors (ESFT) has been improved by multimodal therapy, including surgery, radiotherapy, and chemotherapy over the past 40 years. To date, patients with localized disease at primary diagnosis show a long-term event-free survival rate of about 75 % [1]. However, the outcome for ESFT patients with unresectable disease still remains poor, especially with large tumors occurring in the pelvis or spine [2 4]. The treatment strategy for unresectable ESFT is still controversial and has never been established. ESFT are regarded as radiosensitive tumors, and radiation therapy was the mainstay of local treatment for ESFT until the 1980s. Nevertheless, definitive surgical resection has been widely accepted these days, due to several reports where not only local, but also distant failure occurred more frequently in patients treated with radiotherapy only than in those treated with surgery or surgery radiotherapy
2 combined therapy [2, 4, 5]. These results suggested that, for the patients with unresectable ESFT, more effective radiotherapy and more intensive systemic therapy such as high-dose chemotherapy (HDC) should be conducted to reduce the risk of local and distant failure, respectively. For unresectable bone and soft tissue sarcoma, carbonion radiotherapy (CIRT) has been applied to clinical trials at the National Institute of Radiological Sciences, Chiba, Japan since 1996 [6]. The phase I study showed marked antitumor effects without severe complications in most sarcomas, including ESFT. A phase II clinical trial is currently being conducted, and a number of tertiary hospitals specializing in musculoskeletal tumor treatment have been involved in this trial in Japan, whereas clinical results of CIRT for ESFT have not been reportedtodate. Here we report our experience with CIRT and HDC in the treatment of unresectable ESFT. Patients and methods Treatment strategy for unresectable ESFT in our hospital Open biopsy was performed in most cases to make an accurate diagnosis through histopathological, immunohistochemical, and, more recently, molecular genetic examinations such as fluorescence in situ hybridization. Pretreatment staging was explored using plain radiographs and magnetic resonance imaging (MRI) of the primary site, computerized tomography (CT) of the chest, and technetium-99 bone scintigraphy. Neoadjuvant chemotherapy (NAC), consisting of VDC-I (vincristine, doxorubicin, cyclophosphamide, and ifosfamide) or VDC-IE (VDC-I plus etoposide) was administered as soon as the final diagnosis was made. Evaluation of tumor resectability was clinically assessed with gadolinium-enhanced MRI after the end of NAC, and we chose CIRT as local therapy for patients whose tumors were judged as unresectable tumors. Lung surgery was performed for patients in whom pulmonary metastases were detected with appropriate timing. CIRT CIRT was conducted at the National Institute of Radiological Sciences in Chiba. Features of the accelerator and carbon-ion beam have been described previously [6, 7]. Briefly, the heavy ion medical accelerator in Chiba generates carbon-ion beams with accelerated energies of 290, 350, and 400 MeV/n. Patients were positioned in the treatment rooms with fixed vertical and horizontal beam lines in customized cradles and immobilized with a lowtemperature thermoplastic sheet. A set of 5-mm-thick CT images was taken, and three-dimensional treatment planning was performed using HIPLAN software (National Institute of Radiological Sciences, Chiba, Japan) [8]. The clinical target volume was covered by [90 % of the prescribed dose. We employed dosages of 70.4 or 73.6 Gray equivalents (GyE) [carbon physical dose in Gray 9 relative biologic effectiveness] for a total of 16 fixed fractions within 4 weeks on the basis of the results of previous trials [6, 9]. HDC with stem cell rescue We have employed HDC with stem cell rescue for unresectable ESFT patients after CIRT or conventional radiotherapy. The HDC protocol has been published in detail elsewhere [10, 11]. In brief, autologous CD34?-selected peripheral blood stem cells were harvested during postoperative chemotherapy or simply after receiving granulocyte colony-stimulating factor. Peripheral blood stem cell harvesting was performed one to five times until total counts of CD34? cells reached /kg, which was required per transplantation. All patients received busulfan (4 mg/kg/oral) on days -10 to -7 for a total dose of 16 mg/kg. Melphalan (140 mg/m 2 /i.v.) was given on day -6, and thiotepa (200 mg/m 2 /day/i.v.) was administered on days -5to-3 for a total dose of 600 mg/m 2. Peripheral blood stem cells were transplanted on day 0, followed by daily administration of G-CSF (2 mg/kg) from day 5 until the absolute neutrophil count recovered [5,000/mL. After completion of HDC, careful follow-up was undertaken with laboratory studies and chest CT every 1 and 3 months, respectively. Results Patient characteristics Five patients (3 males and 2 females, median age 22 years) had unresectable tumors and received CIRT as local therapy from (Table 1). Three patients had pelvic lesions and 2 had spinal lesions (L5 and S1-2). Two patients (No. 3 and 4) showed lung metastases at presentation. Four out of 5 patients had huge tumors [100 ml, including 3 patients [200 ml. Three patients (Nos. 1-3) were administered VDC-I and two (Nos. 4 and 5) were administered VDC-IE as a NAC. Radiographic evaluation after NAC revealed that partial response was observed in 3 patients (Nos. 1, 2, and 4) and stable disease in 2 patients. The follow-up period ranged from months after diagnosis and months after CIRT.
3 CIRT and local control CIRT was performed at the dosage of 70.4 GyE for 2 patients and 73.6 GyE for 3 patients. During the follow-up period after CIRT, 2 patients showed tumor shrinkage 4 and 6 months after CIRT, including 1 patient (No. 2) whose extraskeletal mass had almost disappeared (Fig. 1). The other 3 patients were categorized as no change 6 months after CIRT. In all tumor lesions, we found varying sizes of high-signal intensity change on T2-weighted MRI images, reflecting necrotic change. No severe acute toxicity relating to CIRT was observed, although 1 patient (No. 2) with L5 lesion demonstrated paraplegia 54 months after CIRT. Local failure was observed in only 1 patient (No. 1) 22 months after CIRT, resulting in an overall local control rate of 80 %. Precise investigation of this case, comparing the irradiation area of CIRT and localization of recurrence, suggested that recurrence occurred in the irradiation field (Fig. 2). HDC and overall survival Four of the five patients received HDC with stem cell rescue after CIRT, with one patient (No. 4) refusing. All patients had grade 4 hematological toxicities, although there were no patients with sepsis or severe Table 1 List of patients No. Age (years) Gender Site Tumor volume (ml) CIRT dose (GyE) Response to CIRT Follow-up (months) Outcome Local failure Distant failure 1 11 Female Spine NC 79 DOD Yes No 2 23 Male Spine PR 160 CDF No No 3 22 Male Pelvis NC 12 DOD No Yes 4 22 Female Pelvis NC 61 DOD No Yes 5 16 Male Pelvis PR 31 DOD No Yes CIRT dose carbon-ion radiotherapy dose, PR partial response, NC no change, DOD death of disease, CDF continuous disease-free Fig. 1 Magnetic resonance imaging of patient No. 2 before (a) and after (b) CIRT. Extraskeletal mass (arrow) disappeared after CIRT Fig. 2 Magnetic resonance imaging of patient No. 1 just after CIRT (a) and after occurrence of local failure (arrow) (b)
4 infection disease. One patient suffered from veno-occlusive disease just after HDC and recovered within a few weeks. Distant failure was observed in 3 patients 1, 6, and 13 months after completion of the treatment. These patients died because of lung (and brain) metastases progression. Another patient died by extensive progression of a locally recurrent tumor. Discussion In the present study, we performed retrospective analysis to clarify whether combination therapy with CIRT and HDC is effective for unresectable ESFT patients. Our results indicated that this combination therapy shows favorable local control, but unsatisfactory results for overall survival. We found favorable results for CIRT for local control of unresectable ESFT. Radiation therapy had been the mainstay of local treatment for ESFT and several analyses reported that the 5-year local control rate of patients treated with radiotherapy ranged from % [4, 12 14]. We replaced local therapy with CIRT for superior dose intensification and distribution, and obtained favorable local control. CIRT has represented a promising local control effect for patients with bone and soft tissue tumors. Kamada et al. [6] reported that phase I/II clinical trials of CIRT for unresectable bone and soft tissue tumor at the National Institute of Radiological Sciences concluded that CIRT seemed to be a safe and effective modality for these tumors. In addition, Imai et al. [7] reported a high local control rate for unresectable sacral chordoma without severe side-effects. However, it is difficult to distinguish the effect of postoperative chemotherapy from the effect of CIRT. Unfortunately, we have 1 patient who suffered paraplegia [4 years after CIRT; this patient underwent treatment during the phase I/II dose escalation study, and received 73.6 GyE for extensive irradiation field. Recently, CIRT has been performed \70.6 GyE with an irradiation field that strictly excludes the spinal cord. Patients with unresectable ESFT should receive intensive systemic therapy to prevent distant failure, although HDC would not be appropriate for such cohorts. Several reports suggested that distant metastases occurred in [40 % of patients with localized ESFT who received radiotherapy as local therapy [15, 16]. This metastases rate is actually higher than that of patients who received definitive surgery, suggesting that unresected ESFT might have more potential to possess micrometastases. We introduced CIRT to improve the local control rate and HDC to improve the distant control rate of our unresectable EFST cases. HDC for metastatic ESFT patients has been referred to as promising. Rosenthal et al. [17] reported that they applied 2 cycles of HDC containing melphalan and busulfan or carboplatin with stem cell rescue for metastatic bulky or recurrent ESFT, and the 3-year event-free survival was 47 %. The effectiveness, however, of HDC as systemic therapy for this cohort was not seen in the present study. One explanation of distant failure is the existence of bone marrow metastases. Bone marrow aspiration is recommended to be included for staging in several guidelines, although we did not perform bone marrow screening. Those 4 cases demonstrating metastases may also have had bone marrow metastases at presentation. Another expected reason for worse distant control is the contamination of viable tumor cells at the time of harvesting or transplantation of stem cells. To date, the existence of minimal residual disease in transfused peripheral blood stem cells has been an important indication of disease relapse [18]. When we plan peripheral blood stem cell harvest from patients with ESFT for induction of HDC after local therapy, confirmation of negative contamination of tumor cells in transplanted stem cells by a molecular biological method such as RT-PCR will be desirable in the future. A limitation of this study is the small number of patients. The rarity of ESFT and lack of consensus regarding HDC make it difficult to accumulate an adequate number of ESFT patients for analysis. The retrospective nature of this study is also inherently limiting. Additional limitation of this study is the short follow-up period. In all 5 patients, only 3 were able to be followed for 5 years. However, our results identify clinical trends that facilitate further evaluation in the setting of prospective trials. Thus, we conclude that combination therapy with CIRT and HDC for unresectable ESFT patients shows favorable local control, but unsatisfactory results for distant control. Acknowledgments This work was supported by Cancer Research Funds for Patients and Family. Conflict of interest of interest. References The authors declare that they have no conflict 1. Balamuth NJ, Womer RB (2010) Ewing s sarcoma. Lancet Oncol 11: Indelicato DJ, Keole SR, Shahlaee AH et al (2008) Impact of local management on long-term outcomes in Ewing tumors of the pelvis and sacral bones: the University of Florida experience. Int J Radiat Oncol Biol Phys 72: Paulussen M, Ahrens S, Dunst J et al (2001) Localized Ewing tumor of bone: final results of the cooperative Ewing s Sarcoma Study CESS 86. J Clin Oncol 19: Rodriguez-Galindo C, Navid F, Liu T et al (2008) Prognostic factors for local and distant control in Ewing sarcoma family of tumors. Ann Oncol 19: Ozaki T, Hillmann A, Hoffmann C et al (1996) Significance of surgical margin on the prognosis of patients with Ewing s
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