Various subtypes of osteosarcoma have been described,
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1 Resident Short Review N Osteosarcoma is one of the most common primary malignant bone tumors in children and adolescents. Telangiectatic osteosarcoma is an unusual variant of osteosarcoma, forming 3% to 10% of all osteosarcomas. Radiographically, these tumors appear as purely lytic destructive lesions located in the metaphyses of long bones. The location and x-ray appearance of telangiectatic osteosarcomas are reminiscent of an aneurysmal bone cyst and can test the acumen of a diagnostic radiologist. Distinguishing between the two entities microscopically can also be quite challenging. Telangiectatic osteosarcoma shows dilated blood-filled spaces lined or traversed by septa containing atypical stromal cells, with or without production of a lacelike osteoid matrix. This review highlights the diagnostic features of telangiectatic osteosarcoma and discusses differential diagnostic considerations, treatment options, and prognostic implications. (Arch Pathol Lab Med. 2012;136: ; doi: / arpa rs) Various subtypes of osteosarcoma have been described, including conventional, small-cell, parosteal, periosteal, intracortical, intramedullary, giant cell-rich, and telangiectatic sarcomas. As many as 3% to 10% of osteosarcomas are of the telangiectatic subtype. 1,2 Paget 3 was the first to describe telangiectatic osteosarcoma (TO). Gaylord 4 considered these lesions to be malignant aneurysms of the bone. Ewing 5 was first to consider and describe TO as a variant of osteogenic sarcoma. The incidence of TO varies in different studies: TO accounted for 3% of all osteosarcomas in a series by Matsuno et al, 6 while the incidence was significantly higher at 10% in another series. 1 The histogenesis of TO is presumed to be either transformed osteoblasts or stem cells of mesenchymal derivation. At the ultrastructural level, angiosarcomatous features are identified in addition to osteoblast-like and fibroblast-like cells. Weibel-Palade bodies, pinocytic vesicles, and tight intercellular junctions are identified within the cell cytoplasm; these features further suggest this tumor derives from multipotential stem cells of mesenchymal origin. 7,8 Accepted for publication June 17, From the Department of Pathology, University of Utah Health Sciences Center, Salt Lake City; and Associated Regional and University Pathologists Institute for Clinical and Experimental Pathology, Salt Lake City, Utah (Drs Sangle and Layfield). The authors have no relevant financial interest in the products or companies described in this article. Reprints: Nikhil A. Sangle, MD, Department of Pathology, University of Utah Health Sciences Center, 50 N Medical Dr, Salt Lake City, UT ( nikhil_sangle@yahoo.com). Telangiectatic Osteosarcoma Nikhil A. Sangle, MD; Lester J. Layfield, MD CLINICAL FEATURES The clinical presentation of TO is similar to that of conventional osteosarcoma. The most common signs and symptoms include recent onset of local pain, soft tissue mass, or both. 9,10 Occasional cases present with pathologic fracture 11 ; in one study, pathologic fracture was identified in 29% of cases during the course of the disease or at the time of initial diagnosis. 1 There is a male predominance, with a male to female ratio of 2:1. The median age at presentation is 17.5 years old and ranges from 15 and 20 years old. The most common location at presentation is the metaphyses of long bones, with the following location distribution pattern 11 : distal femur (41.6%), proximal tibia (16.9%), proximal humerus (9.2%), proximal femur (7.7%), mid-femur (6.2%), mid-humerus (4.6%), mid-tibia (3.1%), pelvis (3.1%), fibula (1.5%), skull bones (1.5%), and ribs (1.5%). Occasional cases of extraosseous TO are described in the literature, 12 with TO arising in the soft tissues of the popliteal fossa, thigh, and forearm. RADIOGRAPHIC FINDINGS Various imaging modalities, including plain radiographs, magnetic resonance imaging (MRI), and computed tomography (CT) scanning, are available for establishing a definitive diagnosis. Among these modalities, traditional plain radiograph findings are most helpful. Classically, radiographs from patients with TO show a purely lytic destructive lesion, although some cases may demonstrate minimal intralesional sclerosis (Figure 1, A). 13 Most lesions are localized to the metaphyseal region; however, these lesions may involve the diaphysis and, in individuals with closed epiphyseal plates, may also extend into the epiphysis. 6 Telangiectatic osteosarcomas are rapidly progressive lesions affecting the medullary and cortical bones, with poorly demarcated margins. 14 Lesions are largely hemorrhagic or necrotic, and osteoid matrix mineralization was noted radiographically in only 58% of cases, in one study. Viable (atypical stromal) cells are localized within the septa and/or toward the periphery of the lesion; identification of mineralized matrix, therefore, correlates with these locations. 13 Cortical destruction is invariably present, with the pattern of bone destruction described as geographic, moth-eaten, and/or permeative. A Codman triangle signifying periosteal new bone formation is a common occurrence. 14 A bone scintigraphy study demonstrates central photopenic areas representing the fluid component and uptake in the septa and peripheral solid areas. This feature is described as the doughnut sign by Murphey et al. 15 CT scanning and MRI (Figure 1, B) are helpful in assessing the extent of the 572 Arch Pathol Lab Med Vol 136, May 2012 Telangiectatic Osteosarcoma Sangle & Layfield
2 Figure 1. A, Anteroposterior radiograph shows a permeative lesion of the distal femoral metaphysis. Codman triangles (short arrows) are seen laterally. There is a small amount of bone matrix in the tumor (long arrow), but most of the tumor shows no matrix formation. The radiographic appearance is consistent with a lytic osteosarcoma but is not specific for a telangiectatic type. B, Sagittal T 2 -weighted magnetic resonance imaging (MRI) of the femur shows an aggressive mass with pathologic fracture. The combination of radiographic and MRI findings are pathognomic. lesion and in distinguishing it from aneurysmal bone cyst (ABC), which is discussed further below. GROSS FINDINGS Macroscopically, TO is a predominantly cystic lesion filled with blood (Figure 1, C). In one series, the lesion size ranged from 5 to 13 cm in the greatest dimension. 6 Most resections show evidence of tumor penetration through the cortex into the surrounding soft tissues. The solid portions of the tumor (when present) demonstrate a fishflesh appearance reminiscent of any high-grade sarcoma. 11 When the blood is washed away, the cyst demonstrates many thin fibrous septa, giving it a honeycomb or sponge-like appearance. MICROSCOPIC FINDINGS On lower magnification, the histologic appearance of a TO (Figure 1, D) is similar to that of an ABC. The TO lesion is composed largely of hemorrhage and necrotic debris. Blood pools do not demonstrate an endothelial lining. Within these blood lakes, variously sized septa are identified, which contain atypical stromal cells with nuclear hyperchromasia, atypical mitoses, and pleomorphism (Figure 1, E). 14 In some cases, where septa have broken down, atypical stromal cells may be identified, free-floating within the blood clot. In some cases, extensive sampling and a careful search are essential in order to demonstrate malignant cells. A delicate and lacelike osteoid matrix is identified between the malignant cells in some cases (Figure 1, F) 6 ; however, this feature is not essential to establish the diagnosis of TO. The presence of atypical and/or overtly malignant cells is enough to rule out the diagnosis of ABC. The presence of benign multinucleated giant cells admixed with the atypical stromal cells is a common microscopic feature. 11 In addition, foci of hemosiderin-laden macrophages are common. Histologically, TO can be divided into low-grade (mild to moderate nuclear atypia and few mitoses) and high-grade (poorly differentiated tumor with marked anaplasia and high mitotic activity) cells. Occasionally, cases with numerous multinucleated giant cells have been confused with giant cell-rich osteosarcoma. A high index of suspicion is essential to entertain the diagnosis of TO in lytic bone lesions, particularly lesions with a destructive pattern. Cytogenetics Although many cytogenetic abnormalities are associated with osteosarcomas, a specific diagnostic cytogenetic or molecular marker has not been identified. Mutations of the retinoblastoma (RB) and TP53 genes have been well established in osteosarcoma tumorigenesis. 16 Abnormal expression of certain other genes, such as the SAS, CDK4, and MDM2 genes, has also been reported in cases of osteosarcomas. 17 The most frequently reported cytogenetic abnormalities include 1p11-13, 1q21-22, 11p14-15, 14p11-13, 15p11-13, and 19q13, and +1, 210, and ; however, cytogenetic differences among the various histologic subtypes (conventional, telangiectatic, smallcell, giant cell, parosteal, and others) have not been systematically explored. DIFFERENTIAL DIAGNOSIS The most common and most important differential diagnostic consideration is ABC. The radiographic and gross appearances of TO and ABC show varying similarities. Arch Pathol Lab Med Vol 136, May 2012 Telangiectatic Osteosarcoma Sangle & Layfield 573
3 Figure 1. C, Gross appearance of a telangiectatic osteosarcoma shows a predominantly cystic, blood-filled cavity. D, Microscopic image of a telangiectatic osteosarcoma shows thick septa surrounded by blood-filled spaces. Septa contain streamers of osteoid and atypical osteoblasts (hematoxylin-eosin, original magnification 3 40). Microscopic examination is the only definitive diagnostic aid in such cases. Aneurysmal bone cysts are largely hemorrhagic lytic lesions located in the metaphyses of long bones (Figure 1, G). Because ABC is a benign process, it has more discrete margins on radiographic examination. MRI with contrast is helpful in distinguishing between these two entities 13 : TO shows enhancement, thickening, and nodularity of the septa and the periphery of the lesion, while an ABC shows enhancement but lacks thickening and nodularity in the corresponding regions. Osteoid matrix can be identified in CT scans and is found in the septa and/or nodular regions. The presence of atypical or malignant stromal cells identified in TO is never seen in ABC (Figure 1, H) and helps exclude the latter condition. Another important diagnostic consideration includes giant cell tumor of bone. Giant cell tumors are located in the epiphyseal regions of long bones. Histologically, the stromal cells in giant cell tumors show no cytologic atypia or mitotic figures and resemble the nuclei of the multinucleated giant cells in the background. Also, it is rare to see septa within cystic giant cell tumors of bone. 6 Some additional entities, by virtue of their lytic radiographic appearance, enter the differential diagnostic consideration and include lytic lesions like Brodie abscess, blood clot, so-called malignant fibrous histiocytoma, fibrosarcoma, and plasmacytoma. 1 The histologic appearances of these entities are very different and are easily distinguishable from TO. However, if the TOs are not adequately sampled, some of the characteristic histologic findings might be overlooked, and these lesions would be misdiagnosed. TREATMENT AND PROGNOSIS One of the earliest published series from the Mayo Clinic 6 proposed that TO behaved more aggressively than conventional osteogenic sarcoma. This observation was in contrast to that of a study by Farr et al, 19 who found no prognostic differences between the two entities. A later study at the Mayo Clinic 14 showed results similar to those of Farr et al. Much has changed since those reports, with the advent of preoperative neoadjuvant chemotherapy, leading to a much improved prognosis. 20,21 Chemotherapeutic protocols for TO are similar to those of conventional osteogenic sarcoma. Regimens of 2 to 6 cycles of chemotherapy are administered prior to surgery, either intravenously or intra-arterially. Commonly used chemotherapeutic agents include methotrexate, ifosfamide, cisplatin, carboplatin, and doxorubicin. 22 Among these, at least 2 agents need to be administered. Following completion of chemotherapy, the effect of chemotherapy on the tumor is reassessed. Finally, surgical resection of the tumor is performed, the extent of which depends on the location, size, and response to neoadjuvant therapy. Conventionally, most patients have needed radical surgery in the form of amputation; however, recent literature has favored options such as limb salvage procedures. 23 Resected surgical specimens need to be meticulously sampled. The specimen needs to be mapped, and the complete face of bone needs to be sampled to document the percentages of viable and necrotic tumor. Tumor necrosis greater than 95% is considered one of the most important prognostic factors. 24 Additionally, uninvolved neurovascular bundles and soft tissue and bone resection margins are important for a favorable prognosis. Weiss et al 21 have reported overall survival (67%) and 5-year event-free survival (58%) rates similar to those of conventional osteogenic sarcoma (58.3% and 44.3%, respectively). SUMMARY Telangiectatic osteosarcoma needs to be considered in the differential diagnosis for a lytic bone tumor that appears to be malignant. The clinical presentation and demographics of TO are similar to those of conventional osteosarcoma. There are certain radiographic and pathologic similarities between TO and ABC, causing occasional challenges to diagnosticians and straining the acumen of the radiologist and pathologist alike. Telangiectatic osteosarcoma has a more aggressive growth pattern, with cortical destruction and infiltration into the surrounding 574 Arch Pathol Lab Med Vol 136, May 2012 Telangiectatic Osteosarcoma Sangle & Layfield
4 Figure 1. E, Higher magnification shows highly atypical stromal cells with hyperchromasia, nuclear pleomorphism, and atypical mitoses. F, Microscopic image depicts streamers of lacelike osteoid within the septa. G, Microscopic section of an aneurysmal bone cyst reveals moderately thick septa surrounded by blood-filled spaces. Septa contain multinucleated giant cells and non-atypical stromal cells. H, Higher magnification of the septa depicts multinucleated giant cells and stromal cells with no nuclear pleomorphism, hyperchromasia, or atypical mitosis (hematoxylineosin, original magnifications 3400 [E and H], 3100 [F], and 340 [G]). soft tissue. MRI helps identify the enhancing nodular areas and thickened septa around the nonenhancing hemorrhagic component, and CT scanning demonstrates the osteoid matrix in the thickened areas. Diagnostic specimens should be obtained from these enhancing thickened areas, as these are most likely to demonstrate the atypical stromal cells with high mitotic activity and cytologic atypia. Current management protocols employ presurgery neoadjuvant chemotherapy followed by surgical resection. The overall prognosis for patients with TO, with the advent of neoadjuvant chemotherapy, has improved substantially and is currently similar to that for patients with conventional osteosarcoma. We thank Julia Crim, MD, University of Utah Health Sciences Center, for providing the radiographic images. References 1. Huvos AG, Rosen G, Bretsky SS, Butler A. Telangiectatic osteogenic sarcoma: a clinicopathologic study of 124 patients. Cancer. 1982;49(8): Larsson SE, Lorentzon R, Boquist L. Telangiectatic osteosarcoma. Acta Orthop Scand. 1978;49(6): Arch Pathol Lab Med Vol 136, May Paget J. Lectures on Surgical Pathology. Philadelphia, PA: Lindsay & Blackiston; 1854: Gaylord HR III. On the pathology of so-called bone aneurisms. Ann Surg. 1903;37(6): Ewing J. A review and classification of bone sarcomas. Arch Surg 1922;4: Matsuno T, Unni KK, McLeod RA, Dahlin DC. Telangiectatic osteogenic sarcoma. Cancer. 1976;38(6): Roessner A, Hobik HP, Immenkamp M, Grundmann E. Ultrastructure of telangiectatic osteosarcoma. J Cancer Res Clin Oncol. 1979;95(2): Metcalf DJ, Nightingale TD, Zenner HL, Lui-Roberts WW, Cutler DF. Formation and function of Weibel-Palade bodies. J Cell Sci. 2008;121(pt 1): Papagelopoulos PJ, Mavrogenis AF, Savvidou OD, Benetos IS, Galanis EC, Soucacos PN. Pathological fractures in primary bone sarcomas. Injury. 2008; 39(4): Kunze B, Burkle S, Kluba T. Multifocal osteosarcoma in childhood. Chir Organi Mov. 2009;93(1): Unni KK, Inwards CY, Bridge JA, Kindblom L, Wold LE. Tumors of the bone and joints. In: Silverberg S, Sobin L, eds. Atlas of Tumor Pathology. Washington, DC: American Registry of Pathology and Armed Forces Institute of Pathology; 2005: Mirra JM, Fain JS, Ward WG, Eckardt JJ, Eilber F, Rosen G. Extraskeletal telangiectatic osteosarcoma. Cancer. 1993;71(10): Discepola F, Powell TI, Nahal A. Telangiectatic osteosarcoma: radiologic and pathologic findings. Radiographics. 2009;29(2): Telangiectatic Osteosarcoma Sangle & Layfield 575
5 14. Mervak TR, Unni KK, Pritchard DJ, McLeod RA. Telangiectatic osteosarcoma. Clin Orthop Relat Res. 1991(270): Murphey MD, wan Jaovisidha S, Temple HT, Gannon FH, Jelinek JS, Malawer MM. Telangiectatic osteosarcoma: radiologic-pathologic comparison. Radiology. 2003;229(2): Hansen MF. Genetic and molecular aspects of osteosarcoma. J Musculoskelet Neuronal Interact. 2002;2(6): Ragland BD, Bell WC, Lopez RR, Siegal GP. Cytogenetics and molecular biology of osteosarcoma. Lab Invest. 2002;82(4): Boehm AK, Neff JR, Squire JA, Bayani J, Nelson M, Bridge JA. Cytogenetic findings in 36 osteosarcoma specimens and a review of the literature. Pediatr Pathol Mol Med. 2000;19: Farr GH, Huvos AG, Marcove RC, Higinbotham NL, Foote FW Jr. Telangiectatic osteogenic sarcoma. A review of twenty-eight cases. Cancer. 1974;34(4): Rosen G, Huvos AG, Marcove R, Nirenberg A. Telangiectatic osteogenic sarcoma. Improved survival with combination chemotherapy. Clin Orthop Relat Res. 1986(207): Weiss A, Khoury JD, Hoffer FA, et al. Telangiectatic osteosarcoma: the St. Jude Children s Research Hospital s experience. Cancer. 2007;109(8): Basaran M, Bavbek ES, Saglam S, et al. A phase II study of cisplatin, ifosfamide and epirubicin combination chemotherapy in adults with nonmetastatic and extremity osteosarcomas. Oncology. 2008;72(34): Rashid M, Hafeez S, Zia ul Islam M, et al. Limb salvage in malignant tumours of the upper limb using vascularised fibula. J Plast Reconstr Aesthet Surg. 2008;61(6): Khuu H, Moore D, Young S, Jaffe KA, Siegal GP. Examination of tumor and tumor-like conditions of bone. Ann Diagn Pathol. 1999;3(6): Arch Pathol Lab Med Vol 136, May 2012 Telangiectatic Osteosarcoma Sangle & Layfield
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