Surgery for Dedifferentiated Liposarcoma, Presenting Two Radiologically and Pathologically Distinctive Patterns
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1 Surgery for Dedifferentiated Liposarcoma, Presenting Two Radiologically and Pathologically Distinctive Patterns Manabu Hoshi 1, Seiichi Matsumoto 1, Jun Manabe 1, Taisuke Tanizawa 1, Toshio Shigemitsu 1, Hirotaka Koyanagi 1, Keisuke Ae 1, Kengo Takeuchi 2 and Noriyoshi Kawaguchi 1 1 Department of Orthopaedic Oncology and 2 Department of Pathology, Cancer Institute Hospital, Japanese Foundation for Cancer Research, Tokyo, Japan Received November 21, 2005; accepted April 1, 2006 Jpn J Clin Oncol 2006;36(7) doi: /jjco/hyl073 In this paper, we report three cases with dedifferentiated liposarcoma in the lower extremities, presenting two patterns that are distinctively different radiologically and pathologically. The first case was a 67-year-old male who had discovered a mass in his left thigh, which was shown as a low and iso density mass between the muscles on computed tomography (CT). The second case was a 61-year-old male who had suffered from an intramuscular tumor with a non-fatty sarcomatous area within the fatty components as shown on magenetic resonance imaging (MRI). The third case was a 52-year-old female who had presented with an intramuscular tumor of the left thigh, consisting of a mass with fat and another soft tissue tumor adjacent to the lipomatous component as detected with CT and MRI. The final pathological diagnoses of the resected specimens in all three cases were concluded to be dedifferentiated liposarcoma, composed of welldifferentiated liposarcomas and spindle and/or pleomorphic sarcomas, compatible with malignant fibrous histiocytoma. In all three cases, wide resection of the tumor was successfully carried out, and all patients have been continuously disease-free up to the most recent follow-up. Evaluation of the surgical margins for the resected specimens indicated that the safety margin for a dedifferentiated lesion should be accomplished as an adequate margin or more, and a marginal margin or more could be considered as safe only for the confined part of a well-differentiated liposarcoma. Key words: two distinctive patterns dedifferentiated liposarcoma surgical margin INTRODUCTION Liposarcoma is a malignant soft tissue sarcoma that occurs in adults, which makes up 16 18% of all soft tissue sarcomas (1). Liposarcoma is generally classified into four subtypes: well-differentiated, dedifferentiated, myxoid/round and pleomorphic. According to the World Health Organization (2), dedifferentiated liposarcoma is defined as malignant adipocytic neoplasm showing transition from atypical lipomatous tumor/well-differentiated liposarcoma to non-lipogenic sarcoma of variable histological grade. Therefore, this definition may entail coexistence of both fatty and non-fatty solid components. These two components could be radiologically and pathologically detectable as having two distinctive patterns in our cases. Among 133 liposarcomas that were surgically treated at our institution between April 1978 and September 2005, only three cases, presenting two distinctive patterns radiologically and For reprints and all correspondence: Seiichi Matsumoto, Cancer Institute Hospital, Japanese Foundation for Cancer Research, Ariake, Koto-ku, Tokyo , Japan. smatsumoto@jfcr.or.jp pathologically, fulfilled these criteria at first visit to our institution. Here we report three cases with dedifferentiated liposarcomas occurring in the lower extremities. The aim of this study is to elucidate the clinical behaviors of dedifferentiated liposarcoma, representing two distinctive patterns radiologically and pathologically. In addition, we propose a surgical treatment most appropriate for these tumors. All three patients and/or their families were informed that data from their cases would be submitted for publication, and we received their consent. CASE REPORTS Case 1 A 67-year-old male suffered from a gradual buildup of a mass on his left thigh over a 3 month period. Existence of tumor was indicated at a local hospital, and he was immediately introduced to our hospital. As for his past history, diabetes mellitus was previously diagnosed. At first visit to our hospital, physical examination revealed a 10 8 cm tumor in the proximal region of the left thigh. Regional CT (computed tomography) demonstrated a tumor between the muscles of the rectus femoris and sartorius. Radiologically, the tumor was # 2006 Foundation for Promotion of Cancer Research
2 Jpn J Clin Oncol 2006;36(7) 463 composed of two components. One lesion, which comprised the larger part, was very low density, consistent with subcutaneous fat density showing a well-defined border. The other component was iso-dense, comparable with muscle density. Its border was relatively distinct. Therefore, a fat-containing sarcoma forming two distinctive patterns was suspected (Fig. 1a). The patient underwent a needle biopsy. Pathologically, the tumor was diagnosed to be a pleomorphic sarcoma, with myxoid matrix and with some scattered liboblast-like cells. Wide resection of the tumor was carried out. Macroscopical evaluation of the resected specimen confirmed the radiological imaging of these two distinctively separated lesions, which were composed of a yellow fat-like mass and a firm and round white mass, with the latter lesion being encircled by the former (Fig. 1b). The surgical margins of the resected specimens were evaluated according to the evaluation system of the Japanese Orthopedic Association (3,4). An adequate margin was obtained for the dedifferentiated lesion, and for a part of the yellow lipomatous tumor, a 1 cm wide margin was determined. Consequently, the result for this case was inadequate wide margin. Microscopically, there was a distinctive border between lipomatous tumor and the dedifferentiated lesion (Fig. 1c). The microscopical feature of the yellow component was characterized by a proliferation of fat cells including multilobular lipoblasts, representing welldifferentiated liposarcoma (Fig. 1d). That of the white component was pleomorphic and spindle cell sarcoma with a storiform pattern, resembling malignant fibrous histiocytoma (Fig. 1e). The final pathological diagnosis was made as dedifferentiated liposarcoma. A total of four courses of post-operative systemic chemotherapy were carried out. No recurrence and no distant metastasis have been detected 14 years after the surgery. Case 2 A 61-year-old male presented with an elastic hard mass in the left thigh. He had first noticed it 3 months previously. He visited a local hospital, where the tumor was pointed out. He received a needle biopsy of the lesion, and the cytological diagnosis was class V, with liposarcoma suspected. At the first visit to our hospital, physical examination revealed a cm mass on the medial side of the left thigh. Magnetic resonance imaging (MRI) demonstrated two components of the tumor in the left adductor muscles. One was low-tointermediate signal intensity on T1-weighted sequences with heterogeneously high signal intensity on T2-weighted sequence. The other was high signal intensity on T1-weighted and T2-weighted sequences, consistent with a lipomatous tumor (Fig. 2a and b), and this lesion had thick septa with a well-defined border. The borderline of these tumors was distinct. Clinically, fat tissue sarcoma containing a non-fat component was considered. He underwent a needle biopsy and the pathological diagnosis of well-differentiated liposarcoma was made. A wide resection of the tumor was performed. Grossly, the tumor was composed of two distinctive lesions. In the larger part, the lesion was lipomatous yellow tumor. Within this tumor, a yellow, firm nodule was found (Fig. 2c). Judging from the resected specimens, more than a 2 cm wide margin was achieved for most of the lesion including the dedifferentiated lesion, but at the site in which the yellow lipomatous tumor attached to the femur, the evaluation was marginal margin. Therefore, the final surgical margin was concluded to be marginal margin (3,4). Microscopically, the transition from well-differentiated liposarcoma to dedifferentiated lesion was abrupt (Fig. 2d). One was composed of a proliferation of mature adipose tumor involving lipoblast (Fig. 2e). The other was determined to be pleomorphic-spindle cell sarcoma, suggesting malignant fibrous histiocytoma (Fig. 2f). The final pathological diagnosis was concluded to be dedifferentiated liposarcoma. This case has been continuously disease-free during the 19 months that have passed since tumor resection. Case 3 A 52-year-old female presented to a previous hospital with 2 months history of an enlarging mass in her left thigh. Physical examination revealed a cm mass in the medial region of the left thigh. In the intermedius muscle, MRI demonstrated that a lesion on the anterior and lateral side of the left femur showed high signal intensity on T1-weighted and T2-weighted sequences within thick septa. The medial lesion had homogeneous low signal intensity on T1-weighted sequences and heterogeneously high on T2-weighted sequences (Fig. 3a and b). Regional CT revealed a low density area, comparable with muscle, on the anterior side of the femur, and a low-iso density area on the medial side (Fig. 3c). Intramuscular sarcoma composed of biphasic pattern, lipogenic and non-lipogenic tumor, was suspected. Needle biopsy of the medial lesion was performed. The pathological diagnosis was pleomorphic sarcoma. Thereafter, wide resection combined with in situ preparation (5) for the left femur, which was adjacent to the tumor, was carried out. Grossly, the anterior and lateral lesion was mainly fat-like tissue tumor and the medial lesion was white, roundish, firm tissue (Fig. 3d). Judging from the resected specimen (3,4), a 2-cm-wide margin was accomplished for both of the fat-like and non-fatlike tumors. Pathologically, in addition to the area of welldifferentiated liposarcoma, pleomorphic sarcoma producing collagen resembling malignant fibrous histiocytoma was recognized (Fig. 3e, f and g). The pathological final diagnosis was dedifferentiated liposarcoma. During the follow-up of 5 months after surgery, she has been continuously disease-free. DISCUSSION Dedifferentiated liposarcoma occurs in up to 10% of welldifferentiated liposarcoma and has a predilection to occur in the retroperitneum, extremities, spermatic cord, and rarely in the head and neck (2). This entity was first introduced
3 464 Surgery for dedifferentiated liposarcoma a b c e d Figure 1. (a) Regional computed tomography (CT) showed two distinctive patterns of low and iso density mass. (b) Gross finding of the resected specimen displayed a yellow fatty tumor and white solid firm mass. (c) Microscopical findings showed the abrupt transition between two areas (magnification 20). (d) One pattern was composed of well-differentiated liposarcoma containing lipoblast (magnification 200). (e) The other was composed of pleomorphic-spindle cell sarcoma resembling malignant fibrous histiocytoma (magnification 200). by Evans (6) in 1979 to describe a histologically distinctive lesion in which a high-grade sarcoma appeared within or near well-differentiated liposarcoma. The clinical behavior of dedifferentiated liposarcoma was seen to be worse than well-differentiated liposarcoma, but was less aggressive than that of high-grade sarcoma. These tumors show a local recurrence rate of 41%, a metastatic rate of 17% and disease-related mortality of 28% (7). The phenomenon of dedifferentiation, or histological progression to a high grade, less welldifferentiated neoplasm has sometimes been reported for relatively low-grade mesenchymal tumors including parosteal osteosarcoma and chordoma (1,8). Both pathologically and cytogenetically, well-differentiated and dedifferentiated liposarcoma comprise one subgroup (2,9). Though dedifferentiation pathologically and cytogenetically is not a rare phenomenon in bone and soft tissue tumors, not much data is
4 Jpn J Clin Oncol 2006;36(7) 465 a b c e Figure 2. (a) Axial T1 magnetic resonance imaging (MRI) of the left thigh showed the two distinctive mass of low-to-intermediate and high signal intensity. (b) Axial T2 MRI demonstrated the mass with heterogeneously high and high signal intensity, representing lipogenic mass and non-lipogenic mass in the adductor muscles. (c) Axial view of the resected specimen showed yellow lipomatous and yellow firm lesion. (d) Low-power of microscopical findings demonstrated an abrupt transition (magnification 20). (e) Well-differentiated liposarcoma showing scattered lipoblast was found (magnification 200). (f) Dedifferentiated area, mimicking the appearance of malignant fibrous histiocytoma, was found (magnification 200). d f available on radiological or pathological typical cases with dedifferentiated liposarcomas. Surprisingly little data are available for tumors involving the extremities (10). This may be due to the fact that the diagnosis of dedifferentiated liposarcoma is often made after the local recurrence of well-differentiated liposarcoma. So, two distinct components are not usually observed simultaneously. Moreover, only limited papers are available on either radiological or pathological findings. Therefore, in this study we were restricted to just three cases with dedifferentiated liposarcoma that presented two distinctive patterns radiologically and pathologically at the same time. Radiological findings on liposarcomas, based on CT and MRI, are nowadays analyzed in detail, and radiological information has shown to be closely related to pathological results (11). Radiological features that suggest well-differentiated liposarcoma are deeply situated and show a characteristic signal similar to subcutaneous fat with the presence of thick septa (12,13). All our three cases displayed two distinct features, having different signals and being
5 466 Surgery for dedifferentiated liposarcoma a b c e g d f Figure 3. (a) Axial T1-weighted image showed the medial lesion had homogeneously low signal intensity and the antero-lateral lesion had high signal intensity. (b) Axial T2-weighted image showed the medial lesion had heterogeneously high and the antero-lateral lesion had high intensity. (c) Regional CT showed the two distinctive patters composed of fatty tumor and sarcomatous change. (d) Axial view of the resected specimen demonstrated yellow adipose tissue and a white firm nodule. (e) Microscopically, there was the transitional area (magnification 20). (f) High-power of microscopical findings demonstrated well-differentiated liposarcoma containing atypical lipomatous cell (magnification 200). (g) The dedifferentiated part was similar to malignant fibrous histiocytoma (magnification 200).
6 Jpn J Clin Oncol 2006;36(7) 467 adjacent to each other. The other newly appearing sarcomatous signals arose from the radiological feature characteristic of well-differentiated liposarcoma (14). The two distinctive patterns in liposarcoma have been generally adopted to explain dedifferentiated liposarcoma. But, in practice, making the final diagnosis of dedifferentiated liposarcoma using only radiological imaging was difficult, because there was always a possibility that some liposarcoma may display a mixedhistological appearance within the same lesion. A previous author reported mixed-type liposarcoma consisting of welldifferentiated and myxoid liposarcoma, and pleomorphic liposarcoma showing radiologically and histopathologically two distinctive patterns (15). Therefore, biopsy can be helpful for preoperative diagnosis of these conditions. In this study, all three cases showed two macroscopic components consisting of a large multi-nodular yellow fatty lesion and a slightly firmer nodule corresponding to dedifferentiated foci. This finding was consistent with the radiological finding. Microscopically, the fatty lesions were diagnosed as welldifferentiated liposarcoma, and the latter component was the anaplastic zones of spindle and pleomorphic cell lesions, and judged as malignant fibrous histiocytoma. The welldifferentiated and dedifferentiated components had abrupt transitions between their borders. As previously reported, the most common pattern of dedifferentiation was that of a high-grade tumor, often resembling MFH, fibrosarcoma and even rhabdomyosarcoma (7,16). With respect to the treatment of dedifferentiated liposarcoma, systemic chemotherapy was performed only for one patient (Case 1). The importance of systemic chemotherapy for this condition, however, remains to be discussed. Wide resections of the tumors were selected in all three cases, according to high-grade soft tissue sarcomas. Actually, 133 liposarcomas were surgically treated at our institution, where five cases were diagnosed as dedifferentiated liposarcomas, without distant metastases. Four of five cases occurred in the lower extremities. Wide resections were performed in all four cases, and no distant metastases and no recurrences were found until last follow-up. In the present study, on evaluation of the resected specimens, more than an adequate margin was accomplished for the dedifferentiated lesion of malignant fibrous histiocytoma in all three cases. In most parts of the well-differentiated liposarcoma, an adequate margin could be obtained, but for the smaller lesions, a 1-cm-wide margin in Case 1 and a marginal margin in Case 2 were found. There were no recurrences or distant metastases in all cases upon last follow-up. Our evaluation of surgical margin indicated that the safety margin for newly appearing dedifferentiated tumors should be achieved as an adequate margin or more, and a marginal margin or more could be considerable as safe only for the confined part of well-differentiated liposarcoma. In conclusion, we reported three cases with dedifferentiated liposarcoma in the lower extremities, presenting two radiologically and pathologically distinctive patterns. CT and MRI were valuable for the detection of this unusual pattern. Pathologically each tumor consisted of two components: well-differentiated liposarcoma and a dedifferentiated area of malignant fibrous histiocytoma. All three cases underwent wide resection of the tumor. The safety margin of the dedifferentiated liposarcoma was discussed based on the evaluation approach for surgical margins of resected specimens. Acknowledgment The authors wish to thank Mrs S. Sakai for preparation of the photographs. References 1. Enzinger FM, Weiss SW. Liposarcomas. In: Enzinger FM, Weiss SW, editors. Soft Tissue Tumors, 3rd edn. St Louis: Mosby Dei Tos AP, Pedeutour F. Dedifferentiated liposarcoma. In: Flecher CDM, Unni KK, Mertens F, editors. World Health Organization Classification of Tumors: Pathology and Genetics; Tumors of Soft Tissue and Bone. Lyon: International Agency for Research on Cancer 2002; Kawaguchi N, Ahmed AR, Matsumoto S, Manabe J, Matsushita Y. The concept of curative margin in surgery for bone and soft tissue sarcoma. Clin Orthop 2004;419: Kawaguchi N, Matsumoto S, Manabe J. New method of evaluating the surgical margin and safety margin for musculoskeletal sarcoma, analyzed on the basis of 457 surgical cases. J Cancer Res Clin Oncol 1995;121: Matsumoto S, Kawaguchi N, Manabe J, Matsushita Y. In situ preparation : A new surgical procedure indicated for soft tissue sarcoma of a lower limb in close proximity to major neurovascular structures. Int J Clin Oncol 2002;7: Evans HL. Liposarcoma. A study of 55 cases with a reassessment of their classification. Am J Surg Pathol 1979;3: Henricks WH, Chu YC, Goldblum JR, Weiss SW. Dedifferentiated liposarcoma. A clinicopathological analysis of 155 cases with a proposal for an expanded definition of dedifferentiation. Am J Surg Pathol 1997;21: Dahlin DC, Beabout JW. Dedifferentiation of low grade chondrosarcoma. Cancer 1971;28: Shimoji T, Kanda H, Kitagawa T, Kadota K, Asai R, Takahashi K, et al. Clinico-molecular study of dedifferentiation in well-differentiated liposarcoma. Biochem Biophys Res Commun 2004;314: Krandorf MJ, Meis JM, Jelinek JS. Dedifferentiated liposarcoma of the extremities: imaging findings in four patients. Am J Roentgenol 1993;161: Arkun R, Memis A, Akalin T, Usrun EE, Sabah D, Kandiloglu G. Liposarcoma of soft tissue: MRI findings with pathologic correlation. Skeletal Radiol 1997;26: Kransdorf MJ, Bancroft LW, Peterson JJ, MurpheyMD, FosterWC, Temple HT. Imaging of fatty tumors: distinction of lipoma and well-differentiated liposarcoma. Radiology 2002;224: Jelinek JS, Krandorf MJ, Shmookler BM, Aboulafia AJ, Malawer MM. Liposarcoma of the extremities: MR and CT findings in the histologic subtype. Radiology 1993;186: Ehara S, Rosenberg AE, Kattapuram SV. Atypical lipomas, lipomas, and other fat-containing sarcomas: CT analysis of the fat element. Clin Imaging 1995;19: Irie T, Hatori M, Watanabe M, Ehara S, Kubun S. Radiologically and histologically mixed liposarcoma: a report of two biphasic cases. Jpn J Clin Oncol 2003;33: McCormick D, Mentzel T, Beham A, Fletcher CDM. Dedifferentiated liposarcoma. Clinicopathologic analysis of 32 cases suggesting a better prognostic subgroup among pleomorphic sarcomas. Am J Surg Pathol 1994;18:
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