A Review of Ewing Sarcoma Treatment: Is it Still a Subject of Debate?
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1 Send Orders for Reprints to RESEARCH ARTICLE Reviews on Recent Clinical Trials, 2017, 12, A Review of Ewing Sarcoma Treatment: Is it Still a Subject of Debate? Wala Ben Kridis 1,*, Nabil Toumi 1, Hadil Chaari 1, Afef Khanfir 1, Kamel Ayadi 2, Hassib Keskes 2, Tahia Boudawara 3, Jamel Daoud 4 and Mounir Frikha 1 1 Department of Oncology Habib Bourguiba hospital Sfax, Tunisia; 2 Department of orthopedics Habib Bourguiba hospital Sfax, Tunisia; 3 Department of Pathology Habib Bourguiba hospital Sfax, Tunisia; 4 Department of Radiotheray Habib Bourguiba hospital Sfax, Tunisia A R T I C L E H I S T O R Y Received: August 19, 2016 Revised: December 10, 2016 Accepted: January 09, 2017 DOI: / Abstract: Background: The Ewing sarcoma (ES) represents 10 to 15% malignant bone tumors and 40 to 45% pediatric malignant bone tumors. The aim of this review is to clarify the therapeutic results and prognostic factors of this entity. Methods: A systematic review of the literature was performed. Studies focused on the management of ES were considered for inclusion. Result: ES represents a model of multidisciplinary approach. The optimization of ES multimodality therapeutic strategies has resulted from the efforts of several national and international groups in Europe and North America and from cooperation between the pediatric and medical oncologists. The overall 5- year survival of Ewing localized tumors was 70% versus 30% in metastatic ES. Conclusion: The treatment of ES includes neoadjuvant and adjuvant chemotherapies with surgery and/or radiotherapy for control of the primary site and possible metastatic disease. The role of high-dose chemotherapy is still debated. Keywords: Ewing sarcoma, prognostic factor, treatment. 1. INTRODUCTION Ewing sarcoma (ES) and peripheral primitive neuroectodermal tumor (PNET, previously called peripheral neuroepithelioma) were originally described in the early 1900s as distinct clinicopathologic entities. It became evident that these entities are actually part of a spectrum of neoplastic diseases known as the ES family of tumors (EFT), which also includes extraosseous ES (EES), PNET, malignant small-cell tumor of the thoracopulmonary region (Askin's tumor), and atypical ES. Because of their similar histologic and immunohistochemical characteristics, and shared nonrandom chromosomal translocations, these tumors are considered to be derived from a common cell of origin. Although the histogenetic origin has been debated over the years, increasing evidence from immunohistochemical, cytogenetic, and molecular genetic studies supports a mesenchymal progenitor cell origin for all the EFTs [1]. Ewing's sarcoma represents 10 to 15% malignant bone tumors and 40 to 45% pediatric malignant bone tumors. According to the register of southern Tunisia, bone Ewing tumors represents 3.1% of pediatric cancers [2]. The therapeutic management of these tumors was benefited fully from the progress made *Address correspondence to this author at the Department of Oncology Habib Bourguiba hospital Sfax, Tunisia, El-Ferdaous Avenue 3029 Sfax, Tunisia; Tel: ; Fax: ; walabenkridis@yahoo.fr by the cooperative work of the various learned societies. Thus the prognosis of localized forms has been improved significantly while that of metastatic is poor [3, 4]. The aim of this review was to clarify the therapeutic results and prognostic factors of this entity. 2. ROLE OF CHEMOTHERAPY Major therapeutic progress has been made in recent years through the work of various European and North American cooperative groups. The major role of doxorubicin was confirmed in particular by the US trial IESS 1 which compared the VAC protocol (Vincristine, Actinomycin and Cyclophosphamide) in the VACD protocol (VAC + doxorubicin) and showed a significant improvement in the disease-free survival 5 years with VACD (60% vs 24% p = 0.001) [5]. These results were confirmed by several other trials with an objective response rate of 80 to 95% and disease free survival at 5 years from 50 to 80% [6, 7]. Other trials have also demonstrated the impact of histological response on survival and the interests in the intensification of neoadjuvant chemotherapy [8]. This led some teams to introduce ifosfamide and etoposide immediately in neoadjuvant chemotherapy in combination with doxorubicin with good outcomes. Indeed in the INT-0091 US trial VACD (Vincristine, Actinomycin, Cyclophosphamide, and Doxorubicin) the protocol was compared to a protocol alternating VACD and ifosfamide /17 $ Bentham Science Publishers
2 2 Reviews on Recent Clinical Trials, 2017, Vol. 12, No. 1 Kridis et al. Etoposide combination. There were a significant improvement in the relapse-free survival with the alternating arm (72% vs 61% p = 0.01) [9]. The VIDE regimen (vincristine, ifosfamide, doxorubicin and etoposide) is used as a neoadjuvant chemotherapy for all patients in the European study Euro-Ewing 99 [3]. The randomized EICESS-92 trial (by Gesellschaft für Pädiatrische Onkologie und Hämatologie [GPOH] and Children s Cancer and Leukaemia Group [CCLG]) addressed ifosfamide and cyclophosphamide equivalence in localized ES. The survival was similar in both arms, but the trial was only powered to show VACA versus vincristine, dactinomycin, ifosfamide, and doxorubicin (VAIA) differences of>15%. Designed as a successor study, the large EuroEwing 99 trial compared cyclophosphamide with ifosfamide in combination with vincristine and dactinomycin (VAC versus VAI) for standard-risk ES (histologic response < 10% in resected tumors or initial tumor volume < 200 ml for unresected tumors) in the maintenance phase. The conclusion of this large trial was that cyclophosphamide might be able to replace ifosfamide in the consolidation treatment of standard risk ES [3]. In case of refractory disease, there is no standard treatment. Several combinations of agents have shown promising responses in retrospective or phase II studies, such as topotecan plus cyclophosphamide, temozolomide plus irinotecan, gemcitabine plus docetaxel, and high-dose ifosfamide [10-12]. 3. INTENSIFICATION VERSUS MAINTENANCE THERAPY To improve treatment outcomes particularly among poor responders to neoadjuvant chemotherapy, several teams have analyzed the role of high-dose chemotherapy followed by transplantation of peripheral stem cell (PSC) in these patients. The results of the multicenter ISG / SSG III were interesting with improved disease-free survival of 33% to 72% with intensive chemotherapy in poor responders to neoadjuvant chemotherapy [13]. This question will probably find an answer due to Euro-Ewing 99 trial in which poor responders were randomized into maintenance therapy cures VAI (Vincristine, Actinomycin and ifosfamide) or high dose (HD) chemotherapy with autologous PSC. For metastatic tumors, the results with conventional chemotherapy remain poor with an overall survival of 30% [14]. An increase in the dose intensity of chemotherapy has been evaluated in several studies with improved clinical and histological response without improving survival [15]. The role of HD chemotherapy with autologous PSC in the metastatic Ewing tumors remains controversial with positive studies [16] and other negative [17]. EURO-EWING 99 is the only randomized study comparing the HD chemotherapy with autologous PSC with conventional chemotherapy for metastatic Ewing tumors. The results of this trial showed a significant improvement in the disease-free survival at 3 years from 25% to 57% with intensive chemotherapy in patients with bone metastases or medullar metastases having complete response after chemotherapy [18]. Therefore, the HD chemotherapy with busulfan-melphalan is currently recommended as the protocol of consolidation in patients with metastatic Ewing tumors with good response after conventional induction chemotherapy [19-21]. 4. LOCOREGIONAL TREATMENT Locoregional treatment of Ewing's tumors is based on surgery and radiotherapy. To date, there were no randomized trials comparing these two modalities in Ewing tumors. Retrospective analysis of several groups gives the impression of greater local control when surgery is possible. Then Surgery was considered the preferred local treatment modality, whenever a marginal or wide resection seems possible, because surgical resection seems to be superior to definitive radiotherapy for local control [22]. It increases the chances of local control of the disease and allows to avoid radiotherapy in certain situations. In addition, it allows to evaluate the histological response to chemotherapy and to guide the postoperative chemotherapy. Intralesional resection or debulking procedures followed by radiotherapy do not offer superior local control or survival compared with definitive radiotherapy and should be avoided [23]. Amputations are rarely indicated (<10%) in patients, for whom radiation therapy would likely result in poor functional results because of tumor site or age. The radiosensitivity of ES has been recognized since the description of this tumor was provided by James Ewing. However, radiotherapy as the single modality results in a high incidence of local recurrence (up to 30% to 35%) [24], especially for large tumors, and an increased risk of late effects. Currently, definitive radiotherapy is only advised for inoperable lesions, with a recommended dose of 54 to 55 Gy to the tumor with a 2cm security margin that should also include scars from surgery or biopsy [25, 26]. Debate continues about the indications for postoperative radiation therapy, because current knowledge is based on conflicting results from observational studies. Postoperative radiation therapy is universally recommended in cases of incomplete surgical resection; however, in Europe, patients with completely resected tumors with poor histologic response also receive postoperative radiation therapy. The recommended dose varied from 45 to 54 Gy [3]. Although additional studies are required to assess the balance between postoperative radiation therapy benefits and risks, postoperative radiation therapy indications have been broadened in the Euro-Ewing 2012 trial. Preoperative radiotherapy is less used. In fact, interpretation of histologic response after radiotherapy is then not reliable, because its impact on the survival has not been studied after preoperative radiotherapy. According to euroewing 99, pulmonary radiotherapy is indicated for patients with metastatic tumors in the lungs or Pleura at diagnosis and treated with conventional maintenance chemotherapy (VAI + Pulmonary radiotherapy), even if it is in complete pulmonary remission at the end of chemotherapy. Both lungs should be irradiated at a dose of 15 grays for patients under 14 years of age and 18 grays for patients over 14 years of age, given the correction-air. The irradiation must be delivered to the photons by the opposite anteroposterior fields. The therapeutic strategy is summarized in Fig. (1).
3 A Review of Ewing Sarcoma Treatment: Is it Still a Subject of Debate? Reviews on Recent Clinical Trials, 2017, Vol. 12, No. 1 3 Fig. (1). Management of Ewing sarcoma in TARGETED THERAPY In the last three decades the outcome for patients with localised Ewing sarcoma (ES) has improved significantly since the introduction of multimodality primary treatment. However, for patients with (extra-) pulmonary metastatic and/or non-resectable relapsed disease the outcome remains poor and new treatment options are urgently needed. Currently the insulin-like growth factor 1 receptor (IGF-1R) pathway and the poly-adp(adenosinediphosphate)-ribose-polymerase (PARP) pathway are being investigated for potential targeted therapies. The IGF-1R pathway is known to be deregulated by the EWSR1-FLI1 translocation which makes it a potential target for therapy. Clinical trials have been reported in which only ES patients were treated with an IGF-1R inhibitor, either as single agent or in combination. In total 291 ES patients were included in these trials, in which two (0.7%) complete responses, 32 (11%) partial responses of which some durable and 61 (21%) stable diseases were observed [27]. The IGF-1R pathway is an interesting target for ES and should be explored further, as biomarkers to select patients that might benefit from treatment are lacking. PARP inhibitors as single agent have so far failed to show improvement in outcome. Future directions include dual insulin receptor/igf-1r blockade with linsitinib as well as chemotherapy- PARP combinations. Both therapeutic strategies are currently being explored [27]. 6. SURVIVAL AND PROGNOSTIC FACTORS Thanks to various modern therapeutic strategies, the overall 5-year survival of Ewing localized tumors was 70% [28-30]. For metastatic disease, the prognosis remains reserved with an overall 5-year survival does not exceed 25 to 30% [8, 26]. Age was a significant prognostic factor for overall survival according Cotterill et al. in a series involving 975 patients. The overall 5-year survival was better in patients under 15 years (63% vs 52% p <0.05) [8]. However in other series including one published by Oberlin [14], age was not identified as a prognostic factor. In most published series, gender has no impact on overall survival. This was recently confirmed by a meta-analysis that included 86 studies and patients [30]. The presence of metastases at diagnosis is considered one of the most important poor prognostic factors [31]. Several studies have shown a better prognostic peripheral tumors compared to those of the axial skeleton. Indeed these have a generally larger tumor size and surgical approach are more difficult. However, this factor seems to lose importance with the intensification of neoadjuvant therapy. Indeed, in the IESS I and ET 1 studies (UKCCSG / MRC), the axial locations and pelvic had a worse prognosis, whereas in the IESS II studies and ET 2 of the cooperative groups and using neoadjuvant chemotherapy more intensified, the impact of tumor localization on survival becomes insignificant [32]. In the CESS study, 81 tumors having a volume> 100 cm3 had a worse prognosis. With the intensification of treatment in CESS 86 study, volume of 200 cm3 was chosen to have a prognostic impact [33]. Good response to neoadjuvant chemotherapy was found to be a positive prognostic factor for survival in several studies [31]. The prognostic role of local therapy remains controversial. In fact some studies have found improved survival with surgery and radiotherapy combination [34], while in other studies the type of local treatment did not influence survival [8]. However, in most studies, radiation therapy was usually indicated for a subgroup of poor prognosis: large tumor volume, axial locations, poor response to chemotherapy first. Intensified treatment protocols seem to have a positive impact on survival. Indeed, in a review of the experience of the St. Jude hospital for 222 patients in 5 consecutive tri-
4 4 Reviews on Recent Clinical Trials, 2017, Vol. 12, No. 1 Kridis et al. als with different protocols, prognosis was better for patients treated according to the latest 3 protocols, more intensive (EWI92, HIRISA and SJBCM) compared to those treated with the first two protocols (ES79 and ES87). Overall survival at 5 years was 83.1% ± 5.6% for the first group versus 68.5% ± 4.8% for the second (P =0.068) [34]. Last but not least, ES prognosis is critically determined by adequacy of local control of the primary tumor and efficacy of systemic chemotherapy to eradicate metastatic disease [35]. CONCLUSION Successive first-line trials addressed the efficacy of various cyclic combinations of drugs incorporating doxorubicin, vincristine, cyclophosphamide, ifosfamide, etoposide, and dactinomycin and identified prognostic factors now used to tailor therapies. The role of high-dose chemotherapy is still debated in localized ES. CONFLICT OF INTEREST The authors confirm that this article content has no conflict of interest. ACKNOWLEDGEMENTS Declared none. REFERENCE [1] Jedlicka P. Ewing Sarcoma, an enigmatic malignancy of likely progenitor cell origin, driven by transcription factor oncogenic fusions. Int J Clin Exp Pathol 2010; 3: 338. [2] Ayadi L, Chaari C, Kallel R et al. Sarcome d Ewing osseux et extra-osseux. Etude anatomo-clinique de 29 cas. Tunisie médicale 2010; 88(5): [3] Euro-E.W.I.N.G. Study Committee: EURO E.W.I.N.G. 99 Study Manual: European Ewing Tumour Initiative of National Groups Ewing Tumour Studies [On line] 2003 Available at http: [4] Buckley JD, Pendergrass TW, Buckley CM et al. Epidemiology of osteosarcoma and Ewing s sarcoma in childhood: a study of 305 cases by the Children s Cancer Group. Cancer 1998; 83: [5] Cotterill SJ, Ahrens S, Paulussen M et al. 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5 A Review of Ewing Sarcoma Treatment: Is it Still a Subject of Debate? Reviews on Recent Clinical Trials, 2017, Vol. 12, No. 1 5 [32] Annemiek M, Pancras C, Andrew B. The clinical use of biomarkers as prognostic factors in Ewing sarcoma. Clinical Sarcoma Research 2012; 2: 7. [33] Craft A, Cotterill S, Malcolm A et al. Ifosfamide-containing chemotherapy in Ewing s sarcoma: The second United Kingdom Children s Cancer Study Group and the Medical Research Council Ewing s Tumor Study. J Clin Oncol 1998; 16: [34] Rodríguez-Galindo C, Liu T, Krasin MJ et al. Analysis of prognostic factors in ewing sarcoma family of tumors: review of St. Jude Children's Research Hospital studies. Cancer 2007; 2: [35] Gaspar N, Hawkins DS, Dirksen U et al. Ewing Sarcoma: Current Management and Future Approaches Through Collaboration. J Clin Oncol. 2015; 20; 33(27):
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