Imaging of Liposarcoma: Classification, Patterns of Tumor Recurrence, and Response to Treatment
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1 Special Article Pictorial Essay O Regan et al. Imaging of Liposarcoma Special Article Pictorial Essay Kevin N. O Regan 1 Jyothi Jagannathan Katherine Krajewski Katherine Zukotynski Frederico Souza Andrew J. Wagner Nikhil Ramaiya O Regan KN, Jagannathan J, Krajewski K, et al. Keywords: CT, liposarcoma, MRI DOI: /AJR Received September 10, 2010; accepted after revision January 25, This work was presented as an electronic exhibit at the 2010 annual meeting of the American Roentgen Ray Society San Diego, CA, and was awarded a Certificate of Merit. 1 All authors: Department of Imaging, Dana Farber Cancer Institute, 450 Brookline Ave, Boston, MA Address correspondence to K. N. O Regan (kevin.oregan1@hse.ie). WEB This is a Web exclusive article. AJR 2011; 197:W37 W X/11/1971 W37 American Roentgen Ray Society Imaging of Liposarcoma: Classification, Patterns of Tumor Recurrence, and Response to Treatment OBJECTIVE. The purpose of this study was to illustrate the subtypes of liposarcoma (LPS) and the significance of the nonlipomatous tumor components using multiple imaging modalities. CONCLUSION. The subtypes of LPS with greater nonlipomatous soft-tissue components on imaging studies tend to show less differentiation and are usually more aggressive both histologically and clinically. Imaging plays an important role in the diagnosis, surveillance, and response assessment of LPS. L iposarcoma (LPS) is a histologically diverse group of tumors arising from mesenchymal cells. LPS accounts for 20 25% of adult soft-tissue sarcomas, and the peak age of onset is in the fifth to seventh decades [1 3]. The clinical behavior of LPS ranges from indolent nonmetastasizing disease to aggressive subtypes that can recur and metastasize rapidly. Therefore, accurate diagnosis and staging, using a multidisciplinary approach, are important to establish appropriate management and prognosis. LPS can occur anywhere in the body but occurs most frequently in the extremities and retroperitoneum [4]. The presence of intratumoral adipose tissue on CT or MRI can suggest the diagnosis, but in some subtypes macroscopic fat is not detectable with imaging [4]. In the case of the pleomorphic liposarcoma subtype, imaging features may be indistinguishable from other aggressive soft-tissue sarcomas. However, in the myxoid subtype, other features, such as site, MR signal characteristics, CT appearance, and enhancement pattern, can suggest the diagnosis. The challenge for radiologists dealing with LPS is in recognizing the diverse imaging features that reflect its histologic heterogeneity. In our experience, the more differentiated the tumor, the more its imaging appearance will approach that of adipose tissue. The aim of this article is to show the multimodality imaging of LPS in our experience at a tertiary cancer center. Liposarcoma Subtypes and Imaging Characteristics Although LPS can be classified into five subtypes, recent developments in molecular biology and genetic mapping now support designation of three major categories. The first category includes atypical lipomatous tumor (ALT), well-differentiated LPS, and dedifferentiated LPS. The second category includes myxoid LPS and round cell LPS. The third category is composed of pleomorphic LPS. Atypical Lipomatous Tumor, Well-Differentiated Liposarcoma, and Dedifferentiated Liposarcoma This category of LPS, which includes ALT, well-differentiated LPS, and dedifferentiated LPS, is the most common subtype of LPS, accounting for approximately 50% of all cases. ALT and well-differentiated LPS have a predilection for the extremities, retroperitoneum, and paratesticular and inguinal regions [1]. ALT and well-differentiated LPS are synonyms for the same pathologic entity, but the difference in terminology is because of the likelihood of curative resection for tumors of the limbs and subcutaneous tissues (ALT), whereas surgery for tumors arising in the deep tissues of the trunk (well-differentiated LPS) is rarely curative [1]. In fact, the recurrence rate for retroperitoneal well-differentiated LPS approaches 100% [1, 5]. The different nomenclature also exists because of the belief of some that a nonmalignant (i.e., nonmetastasizing) neoplasm is a tumor and not a sarcoma. Well-differentiated LPS is W37
2 O Regan et al. further subdivided into four pathologic subtypes, including the more common adipocytic and sclerosing LPS and the rarer inflammatory and spindle cell LPS [6]. Radiologically, there is currently no reliable method to differentiate these subtypes. On imaging, ALT and well-differentiated LPS are composed mostly of fatty tissue on CT and MRI, but thick septa (> 2 mm), nodular soft-tissue elements, or soft-tissue masses < 1 cm may also be seen [3] (Figs. 1 3). ALT and well-differentiated LPS are lowgrade neoplasms that do not metastasize. However, dedifferentiation can occur in these tumors, most often in a time-dependent manner, and is most common in well-differentiated LPS of the retroperitoneum, seen in up to 15% of cases [5]. When dedifferentiated elements are present, the tumor is classified as well-differentiated dedifferentiated LPS, an aggressive neoplasm with the potential to metastasize. The presence of dedifferentiation is suggested on imaging by a focal nodular nonlipomatous region > 1 cm, often in the retroperitoneum [5]. In some cases, the nonlipomatous component predominates and can be very large (Fig. 4). Well-differentiated dedifferentiated LPS is characterized genetically by overexpression of the MDM2 protein [6, 7]. Histologically, the dedifferentiated tumor component resembles undifferentiated high-grade pleomorphic sarcoma in 90% of cases. In contrast, in about 10% of dedifferentiated LPS, there is heterologous differentiation, often with rhabdomyosarcomatous, leiomyosarcomatous, or osteosarcomatous elements [5]. Calcification on imaging may suggest the presence of osteosarcomatous dedifferentiation (Figs. 5 and 6). Because of the heterogeneous appearance, unpredictable growth patterns, and often infiltrative appearance of well-differentiated dedifferentiated LPS, it is difficult to apply standard tumor response criteria such as Response Evaluation Criteria in Solid Tumors (RECIST). In our experience, when monitoring patients with well-differentiated dedifferentiated LPS using serial CT or MRI, close attention should be paid to the nonlipomatous tumor components for evidence of tumor progression or recurrence (Figs. 7 and 8). Distant metastases from dedifferentiated LPS occur in 15 20% of cases, and the most common sites of spread are the liver and lungs [5] (Fig. 9). LPS can metastasize to the peritoneum, resulting in peritoneal sarcomatosis, the radiologic findings of which have been recently reported in the literature by Oei et al. [8] (Fig. 10). Myxoid Liposarcoma and Round Cell Liposarcoma Myxoid LPS and round cell LPS were formerly classified as distinct entities but are now recognized as a continuum of the same entity on the basis of a common chromosomal translocation found in up to 90% of cases [9]. This is the second most common subtype of LPS, often occurring in young adults. Tumors with a greater round cell component (> 5%) follow a more aggressive course with a greater risk of metastases and death [9]. Tumors in this category most often present as a mass in the deep tissues of the thigh that contains only small amounts of microscopic fat (usually < 10% of the tumor volume) [3]. Myxoid LPS has a characteristic appearance on MRI. Usually seen as a multilobulated intramuscular mass, the high water content of these tumors produces low signal intensity on T1- and high signal intensity on T2-weighted sequences [3]. Occasionally, such masses can be mistaken for cystic lesions, but the differentiating features, when present, include the presence of fatty (T1-hyperintense) septa and diffuse enhancement after contrast administration [5] (Fig. 11). The pure round cell variant (round cell LPS) is a high-grade aggressive tumor that has a nonspecific, heterogeneous appearance on MRI, often indistinguishable from other high-grade soft-tissue sarcomas. Myxoid LPS differs from other subtypes of LPS in its unusual pattern of metastatic spread. The most common metastatic sites include the paraspinal regions, bone, retroperitoneum, and opposite extremity [10] (Fig. 12). Pleomorphic Liposarcoma Pleomorphic LPS is the least common subtype of LPS, most often occurring in the deep soft tissues of the extremities in elderly patients [3]. These are aggressive high-grade sarcomas with a high incidence of recurrence and metastasis [5]. On CT and MRI, the imaging appearance of pleomorphic LPS is of a well-circumscribed mass containing little or no fat. The MRI appearance is similar to other aggressive soft-tissue sarcomas, often showing internal hemorrhage and necrosis (Fig. 13). Management of Liposarcoma Surgical resection is the mainstay of curative therapy. Neoadjuvant or adjuvant chemotherapy may be considered in patients with large (> 5 cm) tumors or high-grade round cell or pleomorphic subtypes, often with regimens based on ifosfamide and anthracycline [2]. Neoadjuvant or adjuvant radiation therapy may be used for local control in large highgrade LPS [2]. Myxoid LPS can be quite sensitive to the agent trabectedin (Yondelis ET 743, Johnson & Johnson), a marine-derived alkaloid with reported response rates of up to 51% in one expanded access trial [11]. The exact mechanism of action of trabectedin is unclear, but there is evidence that it induces differentiation of the tumor cells by inactivating the FUS-CHOP fusion oncogene, which is present in approximately 90% of myxoid LPS cases [9, 12]. In our experience with imaging of myxoid LPS in patients receiving trabectedin, tumors can show transformation from soft-tissue signal intensity on MRI (or density on CT) to adipose-tissue signal intensity, further supporting this theory of unique tumor response to treatment [11] (Fig. 14). Conclusion LPS is a histologically diverse soft-tissue sarcoma with a wide range of appearances on imaging and unusual metastatic patterns. The classification of LPS has been recently modified with advances in the molecular biology of these tumors, and the radiologist should be aware of the major subtypes. In well-differentiated subtypes, adipose tissue predominates and is easily recognizable on imaging studies. However, more aggressive LPS subtypes show a progressively smaller lipomatous composition. When monitoring patients with LPS using serial imaging, careful attention must be paid to the nonlipomatous tumor elements for evidence of disease progression or recurrence and treatment response. References 1. Coindre JM, Pedeutour F, Aurias A. Well-differentiated and dedifferentiated liposarcomas. Virchows Arch 2010; 456: Dalal KM, Antonescu C, Singer S. Diagnosis and management of lipomatous tumors. J Surg Oncol 2008; 97: Van Vliet M, Kliffen M, Krestin G, et al. Soft tissue sarcomas at a glance: clinical, histological, and MR imaging features of malignant extremity soft tissue tumors. Eur Radiol 2009; 19: Peterson JJ, Kransdorf MJ, Bancroft LW, O Connor MI. Malignant fatty tumors: classification, clinical course, imaging appearance and treatment. Skeletal Radiol 2003; 32: Murphey MD, Arcara LK, Fanburg-Smith J. From the archives of the AFIP: imaging of musculo- W38
3 Imaging of Liposarcoma skeletal liposarcoma with radiologic-pathologic correlation. RadioGraphics 2005; 25: Fletcher D, Unni K, Mertens F. Liposarcoma of bone. In: Fletcher DM, Unni KK, Mertens F, eds. WHO classification of tumors, pathology, and genetics: tumors of soft tissue and bone. Lyon, France: IARC Press, 2002: Pires de Camargo V, van de Rijn M, Maestro R, et al. Other targetable sarcomas. Semin Oncol 2009; 36: Oei TN, Jagannathan JP, Ramaiya N, Ros PR. Peritoneal sarcomatosis versus peritoneal carcinomatosis: imaging findings at MDCT. AJR 2010; 195:692; [web]w229 W Fiore M, Grosso F, Lo Vullo S, et al. Myxoid/round cell and pleomorphic liposarcomas: prognostic factors and survival in a series of patients treated at a single institution. Cancer 2007; 109: Sheah K, Ouellette H, Torriani M, Nielson P, Kattapuram S, Bredella M. Metastatic myxoid liposarcomas: imaging and histopathologic findings. Skeletal Radiol 2008; 37: Grosso F, Jones RL, Demetri GD, et al. Efficacy of trabectedin (ecteinascidin-743) in advanced pretreated myxoid liposarcomas: a retrospective study. Lancet Oncol 2007; 8: Forni C, Minuzzo M, Virdis E, et al. Trabectedin (ET-743) promotes differentiation in myxoid liposarcoma tumors. Mol Cancer Ther 2009; 8: Fig year-old man with well-differentiated liposarcoma of retroperitoneum. Contrast-enhanced CT image of abdomen shows predominantly fatty mass in left retroperitoneum with sparse thin internal septa (arrow). Fig year-old man with atypical lipomatous tumor of right thigh. A C, Axial proton density (A), axial T1-weighted fat-saturated (B), and coronal T1-weighted fat-saturated (C) contrast-enhanced MR images show predominantly fat signal intensity mass (arrows) with thin internal septations. There are no nodular or enhancing soft-tissue components. Fig year-old man who presented with palpable left groin mass. A and B, Coronal T2-weighted (A) and coronal T1-weighted (B) contrast-enhanced images from pelvic MRI show soft-tissue mass in left spermatic cord (arrows) with fat-containing elements and enhancing soft-tissue components. Histology showed well-differentiated liposarcoma of spermatic cord. W39
4 O Regan et al. Fig year-old woman who presented with abdominal mass. Contrastenhanced abdominal CT image shows large right-sided retroperitoneal mass (arrow) that is predominantly of soft-tissue attenuation with faint enhancing septa. Note displacement of adjacent liver and right kidney and paucity of fatty elements. Histology showed well-differentiated liposarcoma/dedifferentiated liposarcoma. Fig year-old man with dedifferentiated liposarcoma (LPS) of retroperitoneum. A, Axial CT image of abdomen and pelvis at presentation shows predominantly calcified mass (arrow) surrounding aortic bifurcation. Histology of this mass showed dedifferentiated LPS with chondrosarcomatous and osteosarcomatous differentiation. B, Follow-up axial CT image obtained after 3 months shows significant interval progression with enlargement of calcified mass and new large soft-tissue component (arrow). Fig year-old woman with recurrent dedifferentiated liposarcoma (LPS) of retroperitoneum. Patient presented with abdominal fullness 2 years after initial resection of well-differentiated LPS. A and B, Axial (A) and coronal reformatted (B) contrast-enhanced CT images of abdomen and pelvis show large partially calcified mass in right lobe of liver (arrow) with multiple partially calcified masses in retroperitoneum and peritoneum (arrowheads). Biopsy showed dedifferentiated LPS with heterologous osteosarcomatous differentiation. W40
5 Imaging of Liposarcoma Fig year-old woman with extensive well-differentiated liposarcoma/dedifferentiated liposarcoma of retroperitoneum. A, Coronal reformatted contrast-enhanced CT image of abdomen and pelvis obtained at baseline study shows mixed fat (arrowheads) and soft tissue (asterisk) attenuation masses throughout abdomen and pelvis. B, Coronal reformatted contrast-enhanced CT image of abdomen and pelvis obtained at 3-month follow-up shows progressive enlargement of right perinephric softtissue mass (asterisk) consistent with dedifferentiated component while fatty components (arrowheads) remain stable. C, Coronal reformatted contrast-enhanced CT image of abdomen and pelvis obtained 3 months after B shows surgical debulking of right perinephric mass (asterisk). Fat attentuation masses (arrowheads) in pelvis remain stable. D, Coronal reformatted contrast-enhanced CT image of abdomen and pelvis obtained 3 months after C shows regrowth of right perinephric mass and several new softtissue masses (asterisks). Note relative stability of fatty well-differentiated tumor components throughout (arrowheads). Fig year-old man with asymptomatic incidentally detected mass in superior mediastinum. Biopsy of lesion confirmed primary mediastinal well-differentiated liposarcoma/dedifferentiated liposarcoma. A, Unenhanced CT image at diagnosis shows anterior mediastinal mass with mixed fatty (arrow) and softtissue (asterisk) components. B and C, Follow-up CT images obtained at 6 months (B) and 12 months (C) show progressive enlargement of preaortic soft-tissue element (asterisk) that corresponds histologically to more malignant dedifferentiated tumor component, whereas fat component (arrow) remains stable. W41
6 O Regan et al. Fig year-old man with history of resected left inguinal dedifferentiated liposarcoma 13 years previously who presented with new left lower abdominal wall mass. A, Coronal reformatted CT image shows recurrent soft-tissue mass deep in relation to left lower abdominal wall (arrow) and large metastasis on surface of right lobe of liver (arrowhead). B, Chest CT image shows extensive left pleural metastasis evidenced by nodular pleural thickening and enhancement (arrow). Fig year-old woman with right thigh mass. A, Coronal T2-weighted MR image shows characteristic high signal intensity of lesion (arrow). B and C, T1-weighted fat-saturated axial MR images before (B) and after (C) administration of gadolinium show intense enhancement of mass (arrows). Histology showed myxoid liposarcoma. Fig year-old man with recurrent dedifferentiated liposarcoma (LPS). Coronal reformatted CT image of abdomen and pelvis shows multiple large masses throughout peritoneal cavity, consistent with peritoneal sarcomatosis from metastatic dedifferentiated LPS. W42
7 Imaging of Liposarcoma Fig year-old man with metastatic myxoid liposarcoma/round cell liposarcoma. A, Contrast-enhanced CT image through upper chest shows well-circumscribed mass in left periscapular region, relatively hypoattenuating to muscle (arrow). B, Axial T2-weighted MR image of thoracic spine shows multilobulated predominantly high-signal-intensity mass (arrow) involving right paraspinal muscles. C, Contrast-enhanced CT image through upper abdomen shows multiple lobulated low-density peritoneal deposits (arrow). Fig year-old man who presented with mass in right gluteal region. A and B, Axial T2-weighted (A) and coronal STIR T2-weighted (B) MR images of pelvis show heterogeneous but predominantly high-signal-intensity mass deep in relation to gluteal muscles (arrow). Biopsy of mass showed pleomorphic liposarcoma. Fig year-old man with metastatic myxoid liposarcoma in pelvis, treated with trabectedin (Yondelis ET 743, Johnson & Johnson). A and B, Contrast-enhanced CT images through pelvis before (A) and after (B) treatment show change in density (treatment response) of dedifferentiated component (arrow, A) from soft-tissue to well-differentiated fat density (arrow, B). W43
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