Small Cell Osteosarcoma Successfully Treated by High-dose Ifosfamide and Methotrexate, Combined with Carboplatin and Pirarubicin
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1 Small Cell Osteosarcoma Successfully Treated by High-dose Ifosfamide and Methotrexate, Combined with Carboplatin and Pirarubicin HIROYUKI FUTANI 1, SATORU FUKUNAGA 1, YOSHITANE TSUKAMOTO 2, NOBUYUKI TERADA 2, JUNICHIRO ONO 3, NORIAKI OKAMOTO 3, YOSHITOSHI OTSUKA 3, TAKAKUNI TANIZAWA 3, MASAKI TOMATSURI 4 and SHINICHI YOSHIYA 1 Departments of 1 Orthopedic Surgery, 2 Pathology, and 3 Pediatrics, Hyogo College of Medicine, Hyogo, Japan; 4 Department of Orthopedic Surgery, Kawasaki Hospital, Kobe, Hyogo, Japan Abstract. Small cell osteosarcoma (SCO) is the most rare subtype of osteosarcoma and has a poor prognosis. An 11- year-old boy presented with 2-month history of painful tumefaction in the lower leg. Imaging analysis demonstrated a mixture of osteolytic and osteosclerotic lesions in the proximal tibia and extraskeletal area. Histology of the open biopsy showed small round cells producing mucous matrix. Based on these findings, SCO was suspected. The patient received three cycles of neoadjuvant chemotherapy using high-dose ifosfamide, high-dose methotrexate, pirarubicin and carboplatin. Wide-margin resection was performed followed by tibial lengthening using the Ilizarov method and two cycles of adjuvant chemotherapy with the same drugs as for neoadjuvant chemotherapy. Histology of the resected specimen showed that almost all tumor cells were necrotized. Neither recurrence nor metastasis was found after 4 years. Our experience suggests that neoadjuvant chemotherapy, such as the one used here, would be exceedingly effective for SCO without serious non-hematological toxicities. Small cell osteosarcoma (SCO), composed of small round cells, which mimic Ewing sarcoma cells (1), is the most rare variant of osteosarcoma, comprising approximately 1.3% of all osteosarcomas (1, 2). Nakajima et al. (1) have reported that chemotherapy in addition to surgery improves the prognosis of patients with SCO although the number of cases analyzed in their study was small due to the rarity of this disease. Correspondence to: Dr. Hiroyuki Futani, Department of Orthopaedic Surgery, Hyogo College of Medicine, 1-1 Mukogawa Nishinomiya, Hyogo , Japan. Tel: , Fax: , h-futani@hyo-med.ac.jp Key Words: Osteosarcoma, tibia, chemotherapy, small cell tumor, ifosfamide, methotrexate, carboplatin, pirarubicin. Regarding chemotherapy for osteosarcoma, four drugs, such as methotrexate, doxorubicin, cisplatin and ifosfamide have generally been used and the best disease-free-survival rate has been achieved by a combination of all four drugs (3, 4). However, toxicities occur in a substantial population of osteosarcoma patients (3, 5, 6, 7). In particular, cisplatin causes irreversible renal impairment and ototoxicity (5) and doxorubicin causes cardiac failure. Recently, it has been reported that carboplatin (8) and pirarubicin (9) can be used for the treatment of osteosarcomas instead of cisplatin and doxorubicin, respectively, with less toxicity. Therefore, we modified the regimen of chemotherapy of the Italian and Scandinavian sarcoma groups (3), which comprises high-dose ifosfamide, high-dose methotrexate, cisplatin and doxorubicin and we adopted a new regimen of chemotherapy for osteosarcoma comprising of high-dose ifosfamide, high-dose methotrexate, in combination with pirarubicin and carboplatin to reduce toxicities. Here, we present a case of localized tibial SCO, which was successfully treated with preoperative (neoadjuvant) chemotherapy using this new regimen, followed by tibial lengthening. Furthermore, we discuss the clinical manifestations and treatment. Case Report An 11-year-old boy noted a tender mass in the proximal left lower leg. The pain developed gradually over 2 months. The patient was diagnosed with a tibial tumor by radiographs at the regional hospital before being referred to the Bone and Soft Tumor Section of the Department of Orthopedic Surgery, Hyogo College of Medicine. On physical examination, a painful tumefaction was found, with slight local heat in the proximal tibia. Radiographs showed a mixture of osteolytic and osteosclerotic lesions in the metaphyseal region of the proximal tibia, suggesting osteosarcoma (Figure 1). Computed /2012 $
2 Figure 2. An axial CT image demonstrates osteolytic and ostosclerotic lesions with partial cortical destruction and fracture. Figure 1. An anteroposterior radiograph reveals a mixture of osteolytic and osteosclerotic lesions in the metaphyseal region of the proximal tibia, suggesting osteosarcoma. tomographic (CT) images clearly demonstrated osteolytic and osteosclerotic lesions, with partial cortical destruction and fracture (Figure 2). Magnetic resonance imaging (MRI) revealed an abnormal signal intensity in the metaphyseal region and an extraosseous mass. The tumor had invaded beyond the growth plate into the epiphysis. The size of the tumor was cm (Figure 3). Clinically, no metastasis was found. An open biopsy of the tibial lesion was performed. Histological examination revealed that the lesion was composed of predominantly small round cells producing mucous matrix (Figure 4). The EWS-FLI1 chimeric fusion gene transcripts, which clinically characterize Ewing sarcoma, were not detected by reverse transcriptionpolymerase chain reaction analysis. Finally, based upon radiological, histological, and genetic findings, an SCO of the proximal tibia was diagnosed. Neoadjuvant chemotherapy, comprising high-dose ifosfamide, high-dose methotrexate, pirarubicin and carboplatin, was administered. The drugs were given sequentially as follows: methotrexate at mg/m 2 /day and pirarubicin at 30 mg/m 2 /day for 2 days, carboplatin at 150 mg/m 2 /day for 2 days, and ifosfamide at 3000 mg/m 2 /day for 5 days. After three cycles of the chemotherapy, the painful tumefaction disappeared. MRI showed that the extraosseous mass had completely vanished (Figure 5). In addition, the tumor uptake in bone scintigraphy disappeared. According to physical and radiological examinations, the neoadjuvant chemotherapy was effective. Regarding complications of chemotherapy, leucopenia (grade 4) causing a neutropenic fever occured as a hematologic toxicity after two cycles of the neoadjuvant chemotherapy, and treatment with granulocyte colony-stimulating factor was required. However, nonhematological toxicities, including ototoxicity, renal impairment and cardiac failure, did not occur. An en-bloc, wide resection was performed, followed by tibial lengthening using the Ilizarov method. Intraepiphyseal excision was carried out to obtain margins free of tumor invasion into the epiphysis (10). The patellar tendon was reattached to the soft tissue of the tibia. Macroscopically, the resected tissue consisted of white fibrous tissue, suggesting the effectiveness of the neoadjuvant chemotherapy. Histological examination clearly revealed the osteoid formation, which provides histological evidence of SCO. An almost complete response (a necrotic area of more than 90%) was achieved by the neoadjuvant chemotherapy (Figure 6). In addition, two courses of postoperative (adjuvant) chemotherapy, comprising of the same drugs as for the neoadjuvant chemotherapy, were started 10 days after surgery. 966
3 Futani et al: Successful Treatment of Small Cell Osteosarcoma Figure 3. A coronal T1-weighted MRI (left) shows an expansive mass with low to intermediate signal intensity area in the metaphyseal region and the extraosseous mass (arrows). The tumor has invaded beyond the growth plate into the epiphysis (arrowhead). An axial T2-weighted MRI (right) demonstrates the intraosseous and extraosseous extent of the tumor. The length of the defect produced by the excision of the tumor was 13 cm. Distraction osteogenesis by modified bone transport was applied to regenerate the new bone into the defect by the use of an Ilizarov external fixator (Smith and Nephew, Memphis, TN, USA) (10). Distraction was started 7 days after the initial surgery at 0.5 mm, twice daily. The external fixation index (EFI), which was obtained by dividing the external fixation time by the length of distraction, was 32 days/cm. The external fixator was removed when sufficient bone regeneration had been obtained (Figure 7). On the same day, iliac bone grafting between the middle and proximal segments of the tibia (docking site) was performed followed by internal fixation with two plates and screws. At the last follow-up, the patient needed a 2-cm shoe lift for leg length discrepancy of 3 cm (Figure 8). The active range of motion of the knee was from 0 to 110 degrees. The limb function was evaluated by the scoring system of the Musculoskeletal Tumor Society (MSTS) (11). The score is based on six categories; pain, function, emotional acceptance, Figure 4. Histology shows the tumor consisting of neoplastic small round cells (Bar=100 μm). 967
4 Figure 6. Histology of the resected specimen reveals necrotic tumor cells forming osteoid (arrow) (Bar=100 μm). Discussion Figure 5. A coronal T1-weighted MRI (left) and an axial T2-weighted MRI (right) demonstrate disappearance of the extraosseous mass shown in Figure 3. supports, walking abilities and gait; the scores for each category (1-5) are added and presented as a percentage of maximum scores obtainable. A higher percentage means better function. The functional score was 73%, indicating that functional recovery was successfully achieved. Neither recurrence nor metastases have been found 4 years after the surgery. The prognosis of patients with non-metastatic conventional osteosarcoma of the extremity has been improved dramatically with the introduction of multidrug neoadjuvant chemotherapy in combination with surgical removal of the tumor (3, 12). The present article is the first report to show a case of nonmetastatic tibial SCO successfully treated by neoadjuvant chemotherapy with high-dose ifosfamide, high-dose methotrexate in combination with pirarubicin and carboplatin. SCO was first reported by Sim in 1979 (13). More than 50% of the patients are in the second and third decades of life (1). The most common location is the metaphysis of the long bones, and the distal femur is affected in 33% (24 out of 73 patients), followed by the proximal tibia in 12% (9 out of 73 patients) (14). Based upon patient series (1, 14), SCOs affect patients of the same age group and anatomical location as conventional osteosarcomas. The clinical and radiological findings of SCO resemble those of the conventional osteosarcoma. Clinically, the common symptoms are pain and swelling (1, 14). Radiographically, there is a mixture of osteolytic and osteosclerotic lesions, which is not different from those of conventional osteosarcomas. Mineralized lesions are observed in most SCOs, either intramedullary and/or in extraosseous lesions, strongly suggesting a diagnosis of osteosarcoma rather than Ewing sarcoma. In the present case, intramedullary osteosclerosis was detected by radiographic and CT images. In the histological diagnosis of SCO, the osteoid formation is an essential finding since this is not seen in 968
5 Futani et al: Successful Treatment of Small Cell Osteosarcoma Figure 7. The defect after excision of the tumor can be seen (left). Sequential radiographs at 2 weeks and 2, 4, and 11 months after the surgery show reconstruction with bone transport brought out by the Ilizarov technique (right). Ewing sarcoma (1, 13, 14). The histological diagnosis of SCO can be difficult since SCO sometimes produces only scant osteoid lesions. In such cases, the EWS-FLI1 chimeric fusion gene transcripts, which clinically characterize Ewing sarcoma, could facilitate differentiation of SCO from Ewing sarcoma, in conjunction with radiological findings. Regarding the neoadjuvant chemotherapy of patients with non-metastatic osteosarcomas of the extremity, the Italian and Scandinavian sarcoma groups first presented a regimen for neoadjuvant chemotherapy consisting of two cycles of high-dose methotrexate (12 g/m 2 ), cisplatin (120 mg/m 2 ), doxorubicin (75 mg/m 2 ) and high-dose ifosfamide (15 g/m 2 ). Postoperatively, patients received two cycles of doxorubicin (90 mg/m 2 ), and three cycles of high-dose ifosfamide, methotrexate and cisplatin. The results were promising: the 5-year probability of event-free survival was 64% (95% confidential intervals=57% to 71%) and overall survival was 77% (95% confidential intervals=67% to 81%). However, the incidence of non-hematologic toxicities was high, with ototoxicity, renal impairment and cardiac failure being 40%, 10% and 0.4%, respectively (3). Since carboplatin (8) and pirarubicin (9) can be used for treatment of osteosarcomas instead of cisplatin and doxorubicin, respectively, with less toxicity, we modified the regimen of neoadjuvant chemotherapy of the Italian and Scandinavian sarcoma groups and adopted a new regimen of chemotherapy for osteosarcoma comprising high-dose ifosfamide, high-dose methotrexate, in combination with pirarubicin and arboplatin to reduce toxicities. As expected, in the present case, the neoadjuvant chemotherapy of our regimen resulted in the necrosis of almost all tumor cells, without causing nonhematological toxicities and thus enabling safe limb salvage. In the treatment of limb salvage in a skeletally immature child, functional impairment due to subsequent limb-length 969
6 Figure 8. At 4 years after the surgery, the patient has leg length discrepancy of 3 cm (left). An anteroposterior radiograph shows completion of new bone maturation with consolidation of the docking site. discrepancy must be considered. Recently, we reported that satisfactory function could be maintained despite a frequent requirement for limb-lengthening surgery in the femur (15). In the present case, the patient regained satisfactory functional outcome after tibia lengthening. However, he will need additional limb lengthening until or just after skeletal maturity. In conclusion, even though SCO is a rare subtype of osteosarcoma, it should be kept in mind as one of the differential diagnoses from Ewing sarcoma. In the treatment of SCO, high-dose methotrexate, high-dose ifosfamide in addition to carboplatin and pirarubicinas neoadjuvant chemotherapy should be considered, in order to obtain good local control with less toxicity and to improve prognosis. Acknowledgements Written consent was obtained from the patient and his family for publication of this study. This work was in part supported by a Grant-in-Aid (C) ( ) from the Ministry of Education, Culture, Sports, and Science. 970
7 Futani et al: Successful Treatment of Small Cell Osteosarcoma References 1 Nakajima H, Sim FH, Bond JR and Unni KK: Small cell osteosarcoma of bone. Review of 72 cases. Cancer 79: , Dahlin DC and Unni KK: Osteosarcoma of bone and its important recognizable varieties. Am J Surg Pathol 1: 61-72, Ferrari S, Smeland S, Mercuri M, Bertoni F, Longhi A, Ruggieri P, Alvegard TA, Picci P, Capanna R, Bernini G, Müller C, Tienghi A, Wiebe T, Comandone A, Böhling T, Del Prever AB, Brosjö O, Bacci G and Saeter G: Neoadjuvant chemotherapy with high-dose ifosfamidesfamide, high-dose methotrexate, cisplatin, and doxorubicin for patients with localized osteosarcoma of the extremity: a joint study by the Italian and Scandinavian Sarcoma Groups. J Clin Oncol 23: , Winkler K, Beron G, Delling G, Heise U, Kabisch H, Purfürst C, Berger J, Ritter J, Jürgens H, Gerein V, Graf N, Russe W, Gruemayer ER, Ertelt W, Kotz R, Preusser P, Prindull G, Brandeis W and Landbeck G: Neoadjuvant chemotherapy of osteosarcoma: results of a randomized cooperative trial (COSS- 82) with salvage chemotherapy based on histological tumor response. J Clin Oncol 6: , Jaffe N, Keifer R 3rd, Robertson R, Cangir A and Wang A: Renal toxicity with cumulative doses of cis-diamminedichloroplatinum-ii in pediatric patients with osteosarcoma. Effect on creatinine clearance and methotrexate excretion. Cancer 59: , Sleijfer DT, Smit EF, Meijer S, Mulder NH and Postmus PE: Acute and cumulative effects of carboplatin on renal function. Br J Cancer 60: , van der Hulst RJ, Dreschler WA and Urbanus NA: High frequency audiometry in prospective clinical research of ototoxicity due to platinum derivatives. Ann Otol Rhinol Laryngol 97: , Meyer WH, Pratt CB, Poquette CA, Rao BN, Parham DM, Marina NM, Pappo AS, Mahmoud HH, Jenkins JJ, Harper J, Neel M and Fletcher BD: Carboplatin/ifosfamidesfamide window therapy for osteosarcoma: results of the St Jude Children's Research Hospital OS-91 trial. J Clin Oncol 19: , Shinozaki T, Watanabe H, Yanagawa T, Shirakura K and Takagishi K: Pirarubicin-based versus doxorubicin-based osteosarcoma chemotherapy. Ann Pharmacother 36: , Tsuchiya H, Abdel-Wanis ME, Sakurakichi K, Yamashiro T and Tomita K: Osteosarcoma around the knee. Intraepiphyseal excision and biological reconstruction with distraction osteogenesis. J Bone Joint Surg Br 84: , Enneking WF, Dunham W, Gebhardt MC, Malawar M and Pritchard DJ: A system for the functional evaluation of reconstructive procedures after surgical treatment of tumors of the musculoskeletal system. Clin Orthop 286: , Rosen G, Murphy ML, Huvos AG, Gutierrez M and Marcove RC: Chemotherapy, en bloc resection, and prosthetic bone replacement in the treatment of osteogenic sarcoma. Cancer 37: l-11, Sim FH, Unni KK, Beabout JW and Dahlin DC: Osteosarcoma with small cells simulating Ewing s tumor. J Bone Joint Surg Am 61: , Ayala AG, Ro JY, Papadopoulos NK, Raymond AK and Edeiken J: Small cell osteosarcoma. Cancer Treat Res 62: , Futani H, Minamizaki T, Nishimoto Y, Abe S, Yabe H and Ueda T: Long-term follow-up after limb salvage in skeletally immature children with a primary malignant tumor of the distal end of the femur. J Bone Joint Surg Am 88: , Received December 30, 2011 Revised February 4, 2012 Accepted February 6,
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