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1 SPECIAL EXHIBIT Residents Teaching Files Epithelioid Hemangioendothelioma of the Lower Extremity 1 Elizabeth A. Ignacio, MD Kathryn M. Palmer, MD Sharad C. Mathur, MD Arnold M. Schwartz, MD, PhD Wayne J. Olan, MD INTRODUCTION Hemangioendothelioma is a rare vasoformative tumor with an intermediately aggressive nature. This tumor can occur in soft tissue or bone and has a propensity for the deep soft tissues near vessels, as well as the long, tubular bones of the lower extremity. Only rarely does a hemangioendothelioma involve the patella. When there is involvement of the knee joint, the tumor is radiographically similar to hemangiopericytoma, synovial sarcoma, or even pigmented villonodular synovitis. Therefore, definitive diagnosis of hemangioendothelioma requires histopathologic correlation. In this article, we describe a case of multifocal epithelioid hemangioendothelioma of the right patella, distal femur, and proximal tibia that was verified by means of radiologic and histopathologic correlation. CASE PRESENTATION A 41-year-old man was examined by his primary care physician because of a 1-year history of pain and swelling in the right knee. The patient denied any history of infection or trauma. At physical examination, the right knee was markedly enlarged secondary to osseous change with no soft-tissue swelling. The medial aspect of the knee and the patella were extremely sensitive to the touch, but the sensitivity of the overlying skin was within normal limits. A radiograph of the right knee obtained for minor trauma 1 year before presentation had been normal. However, a radiograph of the right knee obtained at the time of presentation showed a large, lytic lesion of the medial femoral condyle that extended into the metadiaphysis; the lesion had poorly defined margins and an expanded zone of transition. There also appeared to be involvement of the patella and proximal tibia (Fig 1). Index terms: Bone neoplasms, diagnosis, , Hemangioendothelioma, , Knee, neoplasms, , RadioGraphics 1999; 19: From the Departments of Radiology (E.A.I., K.M.P., W.J.O.) and Pathology (S.C.M., A.M.S.), The George Washington University Medical Center, rd St NW, Washington, DC Received October 27, 1998; revision requested November 11; final revision received January 5, 1999; accepted January 6. Address reprint requests to E.A.I. RSNA,
2 a. b. Figure 1. (a) Anteroposterior radiograph shows a large, lytic lesion of the medial femoral condyle. The margins of the lesion are poorly defined with an expanded zone of transition. (b) Lateral radiograph shows multiple lytic lesions in the distal femur and patella. A subtle area of lucency is present in the posterior tibia (arrowhead). There is a soft-tissue mass adjacent to the area of cortical destruction along the anterior margin of the distal femur (arrows). a. b. Figure 2. Coronal T1-weighted MR images (repetition time msec/echo time msec = 666/15) (a obtained anterior to b) show a nodular mass involving the medial femoral condyle, the medial aspect of the lateral femoral condyle, and the medial tibial plateau. The signal intensity of the mass is similar to that of muscle and hyaline cartilage. Magnetic resonance (MR) images of the right lower extremity showed large, irregular, nodular masses involving the femur, tibia, and patella (Figs 2 4). The largest focus was in the medial femoral condyle and was 8 cm in diameter. Smaller masses were present in the proximal tibia and patella. The masses appeared to arise from the medullary cavity; they destroyed nearby cortex and extended into the adjacent soft tissue. These heterogenous masses were 532 Special Exhibit Volume 19 Number 2
3 3a. 3b. 3c. 4. Figures 3, 4. (3a) Coronal T2-weighted fat saturation MR image (3,300/63) shows the mass in the medial and lateral femoral condyles, which has heterogeneous high signal intensity. Numerous nodules are outlined by low signal intensity (arrowhead). Edema is present in the suprapatellar soft tissues (arrow). (3b) Coronal T2-weighted fat saturation MR image (3,300/63) obtained posterior to a shows cortical destruction along the medial femoral condyle (arrowheads). Tumor is present in the metadiaphysis (straight arrow). A small joint effusion is also present (curved arrow). (3c) Axial T2- weighted fat saturation MR image (3,900/51) shows heterogeneous high signal intensity in the medial and lateral femoral condyles and mixed signal intensity in the patella (arrowhead). (4) Sagittal protondensity weighted MR image (2,500/20) shows nodular masses with hypointense rims in the medial femoral condyle and superior patella (arrowheads). primarily isointense to muscle on T1-weighted images and hyperintense on T2-weighted images. Peripheral low signal intensity was present with all pulse sequences. There was a small joint effusion as well. The patient did not receive gadolinium. These findings were highly suggestive of a synovial process such as pigmented villonodular synovitis or synovial sarcoma. A computed tomographic (CT) scan of the thorax showed no evidence of pulmonary metastatic disease. March-April 1999 Ignacio et al RadioGraphics 533
4 a. b. Figure 5. (a) Photomicrograph (original magnification, 150; hematoxylin-eosin stain) shows a vascular spindle cell tumor involving the bone. (b) Photomicrograph (original magnification, 600; hematoxylin-eosin stain) shows some epithelioid spindle cells with intracytoplasmic vacuoles that contain erythrocytes (arrows). A femoral needle biopsy was performed, and the specimen revealed an epithelioid hemangioendothelioma. At low power, the tumor was distinctly vascular (Fig 5a) with a vaguely nodular configuration and some areas of myxoid stroma. The cells were variably spindle shaped and epithelioid with moderate amounts of eosinophilic cytoplasm. Intracytoplasmic vacuoles containing erythrocytes were present (Fig 5b) as evidence of primitive vascular differentiation (1,2). There were rare mitotic figures. No tumor necrosis was noted. After consultation with the orthopedic surgery department, the patient elected surgical treatment with curettage. DISCUSSION Hemangioendothelioma is an intermediately aggressive neoplasm that arises from vascular endothelial cells. Definitively described in 1982, this tumor has several histologic subtypes, which include epithelioid, spindle cell, and kaposiform, as well as malignant endovascular papillary angioendothelioma (3). The soft-tissue epithelioid type of hemangioendothelioma has no gender predilection and occurs in the 2nd to 9th decades of life. Local pain and swelling that may be of weeks to years duration are the most common clinical symptoms. Pathologic fractures occur in 10% of patients secondary to osseous invasion. Constitutional signs and symptoms of weight loss and fatigue, microangiopathic hemolytic anemia, and consumption coagulopathy are rare clinical abnormalities. Although most often found in the deep soft tissues of the extremities as well as the liver, lung, and breast, epithelioid hemangioendothelioma also has a propensity to grow in long, tubular bones. Unlike the soft-tissue primary tumor, osseous epithelioid hemangioendothelioma is slightly more frequent in men than in women (male-female ratio, approximately 2:1). In approximately 60% of cases, the long bones are affected. There is preferential involvement of the tibia (23% of cases), femur (18%), and humerus (13%) (4). Osseous hemangioendothelioma lesions are of variable size with margins that may be well delineated or poorly defined. The tumor can localize to cortical or medullary bone. Rarely, the 534 Special Exhibit Volume 19 Number 2
5 epiphysis is involved, but most growth occurs in the metaphysis and diaphysis. One of the typical features of osseous hemangioendothelioma is synchronous or metachronous multicentric disease, which is observed in 20% 50% of cases (3,5). There may be multiple lesions apparent in a single bone or one or more tumor foci in multiple bones of a single extremity. Osteolysis is the principal radiographic pattern, and calcification is unusual. Multiple neoplastic foci in cortical bone, the spongiosa, or both that lead to a bubblelike appearance and osseous expansion without periostitis in the tubular bones of a lower extremity are also highly characteristic (4). At ultrasonography, epithelioid hemangioendothelioma may be hypoechoic or hyperechoic with prominent cystic areas due to hemorrhage. Doppler studies may demonstrate arteriovenous shunting (6). CT shows a soft-tissue mass with attenuation comparable with that of muscle. The mass will enhance after intravenous administration of contrast material. The signal intensity characteristics on MR images are nonspecific. There is intermediate signal intensity on T1-weighted images and high signal intensity on T2-weighted images. The presence of flow voids may indicate a neoplasm of vascular origin, but this finding is not typical of hemangioendothelioma and should suggest an alternative diagnosis. Because many benign and malignant tumors arising from bone and soft tissues should be included in the differential diagnosis of epithelioid hemangioendothelioma, histopathologic evaluation is essential in the diagnosis of this tumor. At pathologic analysis, the tumor may be well circumscribed or have indistinct borders. The surface is bright red or purple, resembling currant jelly, with a consistency that is soft or fleshy. The cortex of the bone may be partially or totally destroyed. Weiss et al (3) describe this tumor as composed of small nests or cords of eosinophilic cells, which may be in a basophilic myxoid stroma. The distinct well-lined anastomosing vascular channels often seen in hemangiopericytoma are absent in this tumor. Cells may be round or fusiform with a central nucleus and prominent intracytoplasmic vacuolation, as in the specimen in our case (3). Classification of malignant potential, as described in more recent investigations, relies on the degree of vasoformative activity, atypia of the endothelial cells, and the frequency of mitotic activity as predictive signs (1). Soft-tissue hemangioendotheliomas have a generally favorable prognosis, but the experience with primary osseous tumors remains limited. Although some series show a 30% frequency of metastases for the soft-tissue lesions (2), there are very few reported cases of osseous epithelioid hemangioendothelioma that have truly metastasized (7). Part of the difficulty in determining the prognosis of this tumor is the concept of multicentricity at clinical presentation. Fechner and Mills (7) note that some patients with osseous tumors developed cutaneous involvement without progression of disease; those cutaneous tumors may actually have represented separate cutaneous primary lesions in multicentric disease rather than true metastases. Many studies found that multifocal lesions have a better prognosis than solitary lesions, but the experience of Kleer et al (5) does not support this result. On the contrary, these authors found visceral involvement to be the most important criterion in predicting the clinical course of osseous epithelioid hemangioendothelioma. Because this entity has only recently been defined (1982), the natural history remains enigmatic. In a review of the literature, Fechner and Mills (7) postulate that 35% 50% of osseous low-grade angiosarcomas reported before the description of epithelioid hemangioendothelioma most likely represented the latter lesion. As a result, questions regarding treatment planning still exist, although most sources regard radical wide excision as the treatment of choice. Given the multifocality of osseous lesions, it has been suggested that a complete skeletal survey be performed before definitive treatment (5,8). CT may be the modality of choice for evaluation of the thorax and exclusion of pulmonary metastases. Curettage may be adequate for removal of low-grade lesions. Radiation therapy has been effective in some patients with multicentric tumors. March-April 1999 Ignacio et al RadioGraphics 535
6 The differential diagnosis of epithelioid hemangioendothelioma at this site can be extensive. However, the main considerations include hemangiopericytoma, synovial sarcoma, and pigmented villonodular synovitis. Hemangiopericytoma is an uncommon tumor that behaves in an erratic and unpredictable manner, which makes classification as a benign or malignant neoplasm difficult. Occurring primarily in middle-aged or elderly men or women, hemangiopericytoma most frequently involves the axial skeleton and proximal long bones (eg, the spine or sacrum, humerus, femur, or mandible). Forty percent of cases occur in the long bones (4); another common site is the pelvis (2). Like hemangioendothelioma, this tumor also has a predilection for the metaphysis and diaphysis. However, hemangiopericytoma typically manifests as a solitary skeletal focus, whereas hemangioendothelioma may be multicentric. The radiographic features of hemangiopericytoma may be nonspecific, but MR imaging can be helpful in differentiating hemangiopericytoma from hemangioendothelioma because hemangiopericytoma demonstrates characteristic vascular channels, usually in the periphery of the mass (6). These serpentine vascular structures can be hypointense due to rapid blood flow or hyperintense due to slow blood flow. Fluid-fluid levels may be present as a result of hemorrhage. At pathologic analysis, hemangiopericytoma has a gray, white, or pink hue with a solid or spongy texture and a granular or friable consistency. The tumor cells have vesicular or hyperchromatic nuclei; at electron microscopy, the tumor cells resemble pericytes cells that are normally found surrounding capillaries. Positive results of immunohistochemical staining for the CD34 antigen support the diagnosis, which is confirmed with electron microscopy (2). Synovial sarcoma is a relatively common primary soft-tissue sarcoma that arises from undifferentiated mesenchymal tissue. Most synovial sarcomas (80% 95%) occur in the extremities, knee, ankle, or foot (4). Intraarticular involvement is rare. In one-half of patients with synovial sarcoma, radiographs will be interpreted as normal (6). If a mass is visible at plain radiography, it is usually well circumscribed and round or lobulated; there is peripheral calcification in one-third of cases. The presence of such calcification makes plain radiography and CT useful in distinguishing synovial sarcoma from epithelioid hemangioendothelioma. CT may also show areas of hemorrhage. At MR imaging, synovial sarcoma usually appears as a heterogenous mass. Signal intensity consistent with hemorrhage is present in 40% of patients (6), and fluid-fluid levels are present in 10% 25%. In one series of 32 patients, the tumor appeared hyperintense, isointense, and hypointense to fat on T2-weighted images owing to a mixture of cystic and solid elements with hemorrhage and fibrous tissue (6). In young adults, this finding in conjunction with hemorrhage and fluid levels in a deep mass is highly suggestive of the diagnosis. Although the presence of calcifications in the mass at plain radiography and CT may favor the diagnosis of synovial sarcoma over osseous epithelioid hemangioendothelioma, there are no absolute radiographic criteria for differentiation of these entities. Histopathologic correlation is required to arrive at the diagnosis. At pathologic analysis, synovial sarcoma is solid and may appear encapsulated. At histologic analysis, synovial sarcoma is biphasic, possessing both epithelial and spindle cell elements (2). Pigmented villonodular synovitis is a proliferative disorder of the synovial membrane. These benign lesions may arise from the synovial lining of joints, tendon sheaths, fascial planes, bursae, or ligamentous tissue. This dis- 536 Special Exhibit Volume 19 Number 2
7 order usually affects adults in the 3rd or 4th decade of life. As in soft-tissue epithelioid hemangioendothelioma, there is no gender predilection. Eighty percent of cases occur in the knee; other large joints affected are the hip, ankle, shoulder, and elbow (listed in order of decreasing frequency). The distribution is monoarticular as a rule, but polyarticular involvement does occur rarely. Radiographs of patients with pigmented villonodular synovitis may be normal or may show a noncalcified soft-tissue mass, joint effusion, or bone erosion on both sides of the joint. The joint space is preserved, and osteoporosis is absent or mild. Calcifications occur rarely; the presence of calcifications should suggest an alternative diagnosis. Pigmented villonodular synovitis has a characteristic MR imaging appearance. The mass is typically heterogeneous and synovial membrane based and extends away from the joint space. There may be septations. The margins may be well defined, although they are often difficult to distinguish from adjacent muscle. On T1- and T2-weighted images, the overall signal intensity of the tumor is similar to or slightly less than that of skeletal muscle. There may be additional foci of high signal intensity in scattered areas (6). Lipid-laden macrophages in the tumor may appear as focal areas of high signal intensity on T1-weighted images and intermediate signal intensity on T2-weighted images. This tumor enhances with gadolinium. Coexistent joint effusion is most common in the knee (50% of cases). Although the radiologic features of pigmented villonodular synovitis are distinctive, the nonspecific appearance of osseous epithelioid hemangioendothelioma makes differentiation between these entities difficult. Histopathologic analysis is essential to make the diagnosis. At pathologic analysis, pigmented villonodular synovitis is described as a shaggy beard, an appearance that reflects the villous or frondlike projections of synovial membrane. The histopathologic specimen shows synovial hyperplasia with multinucleated giant cells that have the characteristic brown pigmentation secondary to both intracellular and extracellular hemosiderin. CONCLUSIONS The experience with primary epithelioid hemangioendothelioma of bone is limited, and the long-term behavior of this neoplasm is uncertain. Using plain radiography, CT, and MR imaging, one can determine the full extent of disease, including local soft-tissue involvement, multifocality, and distant metastases. However, the radiologic features of this tumor must be correlated with the clinical and histopathologic findings to arrive at an accurate final diagnosis because the imaging findings are nonspecific. As epithelioid hemangioendothelioma has been more frequently identified during the past decade, a thorough evaluation of the clinical, histopathologic, and radiologic variables should be considered to properly assess and treat this entity. REFERENCES 1. Ellis TS, Schwartz A, Starr JK, Riedel CJ. Epithelioid hemangioendothelioma of the lumbar vertebral column: case report and review of literature. Neurosurgery 1996; 38: Enzinger FM, Weiss SW. Soft tissue tumors. 3rd ed. St Louis, Mo: Mosby, 1995; Weiss SW, Ishak KG, Dail DH, Sweet DE, Enzinger FM. Epithelioid hemangioendothelioma and related lesions. Semin Diagn Pathol 1986; 3: Resnick D. Diagnosis of bone and joint disorders. 3rd ed. Philadelphia, Pa: Saunders, 1995; Kleer CG, Krishnan Unni K, Mcleod RA. Epithelioid hemangioendothelioma of bone. Am J Surg Pathol 1996; 20: Kransdorf MJ, Murphy MD. Imaging of soft tissue tumors. Philadelphia, Pa: Saunders, 1997; Fechner RE, Mills SE. Tumors of the bones and joints. In: Rosai J, ed. Atlas of tumor pathology, fasc 8, ser 3. Washington, DC: Armed Forces Institute of Pathology, 1993; Boutin RD, Spaeth HJ, Mangalik A, Sell JJ. Epithelioid hemangioendothelioma of bone. Skeletal Radiol 1996; 25: March-April 1999 Ignacio et al RadioGraphics 537
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