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Instructional Course Lecture   |    
Malignant Bone Tumors
C. Parker GibbsJr., MD; Kristy Weber, MD; Mark T. Scarborough, MD
The Journal of Bone & Joint Surgery.  2001; 83:1728-1745 
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Classic high-grade osteosarcoma is a highly malignant spindle-cell sarcoma of bone in which the malignant cells produce osteoid1. It is the most common primary malignant tumor of bone, excluding myeloma, and is the third most common malignant disease in adolescence after leukemia and lymphoma. However, it is still a rare tumor with only 1000 new cases per year in the United States. There appears to be no racial or ethnic influence associated with its incidence2. However, an increased prevalence has been noted in families affected with the Li-Fraumeni syndrome3 and in patients who have had retinoblastoma4 (a 40% prevalence in those with bilateral disease), have undergone radiation therapy5, or have Paget disease6.
Classic high-grade osteosarcoma has a peak prevalence in the second decade of life, with 75% of cases occurring between the ages of ten and twenty-five years1. There is a second peak in the seventh decade, which is most likely due to its association with Paget disease of bone. The male-to-female ratio is approximately 1.5:1. Osteosarcoma can occur in any bone but is most common in the metaphyses of long bones, with 80% to 90% of the tumors occurring in those locations, and it often extends into the epiphysis. Specifically, its most frequent locations are the distal femoral metaphysis (35%), the proximal tibial metaphysis (20%), and the proximal humeral metaphysis (10%), all areas of rapid skeletal growth1. Occasionally, the tumor is found in the diaphysis of long bones and, more rarely, in the flat bones.

Clinical Presentation

Pain is the most prevalent presenting symptom in osteosarcoma, occurring in 85% of patients7. It is probably due to microfractures through the involved areas of the bone or, in severe cases, to compression or stretching of adjacent anatomic structures. The pain usually is exacerbated by activity, and only 21% of patients have pain at night. Almost 50% of patients relate the onset of symptoms to an episode of minor trauma. A palpable or visible mass is noted in about 40% of patients. Painless masses may be obscured when they arise in the pelvis or proximal part of the thigh. Less common findings include a limp, weakness, a decreased range of motion in associated joints, venous engorgement, edema, and striae. Laboratory tests are generally not helpful in the diagnosis of osteosarcoma, although elevated serum lactate dehydrogenase and alkaline phosphatase levels have been associated with a poorer prognosis8,9.

Plain Radiographic Features

Classic high-grade intramedullary osteosarcoma usually appears as a destructive lesion of the metaphysis of a long bone. It typically exhibits a mixture of lytic and blastic areas but may be exclusively one or the other. Its overall appearance is one of an aggressive process characterized by destruction of both cortical and cancellous bone and a wide (permeative) zone of transition between tumor and normal host bone. Osteosarcoma usually has an extraosseous soft-tissue mass with fluffy irregular densities indicative of neoplastic bone formation. At the proximal and distal cortical margins of the tumor, there may be triangular-shaped areas of reactive periosteal new-bone formation known as Codman triangles. These are not specific to osteosarcoma but rather are seen as a reaction to any aggressive bone process. The radiographic appearances of the other types of osteosarcoma can be quite different from that of classic osteosarcoma and are discussed below.

Staging Studies

Staging studies are part of a process to determine the local and distant extent of a tumor, thus helping to determine prognosis and management strategies10. These studies can be divided into those that determine the local extent and those that determine the distant extent of disease. Magnetic resonance imaging is the current standard technique for determining the local extent of disease in the involved bone (Figs. 1-A and 1-B). The study must include the entire bone in question. Magnetic resonance imaging is extremely accurate in defining the marrow extent of the tumor and therefore is very helpful in determining the appropriate resection level at surgery11. Sagittal or coronal images of the entire bone visualize skip metastases (discontinuous foci of tumor in the same bone outside the reactive zone)12 that are not apparent on plain radiographs. Axial magnetic resonance images provide an accurate depiction of the extent of any soft-tissue mass and its relationship to nearby neurovascular structures. Adjacent joint involvement may also be demonstrated. Planning of a biopsy is facilitated greatly by the use of magnetic resonance imaging, as it shows the most appropriate surgical route to the tumor without unnecessary contamination of associated structures. Also, magnetic resonance imaging can define areas most likely to be viable, optimizing the chances for obtaining a diagnostic sample. Computed tomography is complementary to magnetic resonance imaging by providing better bone detail, and it is especially useful for visualization of pelvic tumors, where the fat planes allow better delineation between normal and tumor tissue.
Bone scintigraphy has an important role in staging both the local and the distant extent of osteosarcoma. It can define areas of primary involvement, skip metastases, and sites of synchronous metastases to other parts of the skeleton. Chest radiographs and computed tomography scans screen for the presence of pulmonary metastases. The lungs are the site of most metastases. Computed tomography scans of the chest can detect pulmonary nodules as small as 3 mm and finely pinpoint them should resection be necessary. Lymphatic spread is so uncommon that routine examination of lymphatics is not done.

Pathological Characteristics

Gross examination of an osteosarcoma specimen most often reveals a soft-tissue mass originating in the medullary canal and extending beyond the cortex. The inner part of the mass is usually more heavily mineralized than the periphery (in contradistinction to myositis ossificans)1. Any intra-articular extension can be appreciated during gross examination. If present, it usually occurs along the course of ligaments, such as the anterior and posterior cruciate ligaments.
Histological examination reveals frankly malignant cells producing osteoid. These cells are pleomorphic and exhibit mitotic activity. There are often areas of spontaneous tumor necrosis. The background stroma may also be predominantly fibrous or chondroid1. Communication of clinical and radiographic findings to the pathologist is essential in the diagnosis of all mesenchymal neoplasms. Without this essential information, a pathologist may mistake the reactive bone of fracture callus or periosteal new bone for that produced by the malignant cells of osteosarcoma or vice versa. This could result in a misdiagnosis and subsequent mismanagement of the patient’s disease. The less common types of osteosarcoma, such as low-grade central osteosarcoma and parosteal osteosarcoma, are much less cellular and are sometimes confused with fibrous dysplasia. Periosteal osteosarcoma is predominantly cartilaginous and must be distinguished from chondrosarcoma.

Osteosarcoma Variants

Osteosarcoma can be divided into primary and secondary types. The primary types include high-grade central (classic), low-grade central, juxtacortical or surface, and telangiectatic lesions. Secondary osteosarcomas include those associated with Paget disease, post-irradiation sarcomas, and those that "dedifferentiate" from other benign precursors, such as fibrous dysplasia and bone infarcts.
High-grade central (classic) osteosarcoma is the most common type. The typical locations are the distal aspect of the femur, the proximal aspect of the tibia, and the proximal part of the humerus. The clinical, radiographic, and pathological presentation is usually typical and does not pose a difficult diagnostic challenge.
The surface or juxtacortical osteosarcomas include parosteal, periosteal, and high-grade surface tumors. Parosteal osteosarcomas are located predominantly in the posterior aspect of the distal femoral metaphysis and have a lobulated radiodense "pasted on" appearance on plain radiographs. There may be an apparent cleavage plane between the cortex and the tumor. Some may progress to involve the medullary canal. These tumors usually occur in a somewhat older age-group (twenty to forty years old) and have a definite preponderance among females. Histological examination reveals a low-grade fibrous stroma with tumor osteoid and bone formation13. Although such tumors are most often low-grade histologically, they may evolve into high-grade malignant lesions, in which case they are called dedifferentiated parosteal osteosarcomas14. The treatment of histologically low-grade tumors is wide excision without chemotherapy. Long-term survival rates as high as 93% have been reported15.
Periosteal osteosarcoma is most commonly an intermediate-grade tumor found in the diaphysis of long bones, especially the tibia. Radiographically, it appears as a variably calcified mass in a saucer-shaped defect in the cortex of a long bone. Histologically, it is composed of intermediate-grade malignant cells producing osteoid in a predominantly chondroid background. It most often occurs in adolescence and has a metastatic rate between that of parosteal osteosarcoma and that of conventional osteosarcoma. The treatment is wide excision, and the role of chemotherapy is unclear16.
High-grade surface osteosarcoma is an extremely rare tumor that occurs in the second and third decades of life17. These tumors have a predilection for the diaphyseal surface of long bones (especially the femur), although fully one-third involve only the metaphysis. They exhibit various amounts of mineralization, which is most pronounced at the broad base of the tumor. Most tumors affect the underlying cortex by destruction or thickening, or both. Approximately one-half of the tumors infiltrate the underlying bone either grossly or histologically. Histological evaluation reveals a high-grade malignant tumor that is essentially identical to classic osteosarcoma. Treatment is wide surgical excision, and chemotherapy is thought to be beneficial. The metastatic rate is similar to that of classic high-grade osteosarcoma.
Telangiectatic osteosarcoma is a high-grade osteosarcoma that is often seen to be purely destructive on plain radiographs. It is hemorrhagic, and often there is little tissue present. It can be confused with benign lesions, especially an aneurysmal bone cyst1. It is similar to classic high-grade osteosarcoma with respect to patient demographics, treatment, and outcome.
The most common secondary osteosarcomas are associated with Paget disease of bone or arise in a bone that has had previous irradiation. Both types are aggressive, destructive lesions of bone with highly anaplastic cell populations. Both have a dismal prognosis, usually with a rapid progression to distant metastasis. The use of chemotherapy may be beneficial, but there are limited data. In addition, the patients with these secondary osteosarcomas are usually more than fifty years old and do not tolerate the chemotherapy as well as younger patients do.

Treatment of Classic High-Grade Osteosarcoma

Surgery alone was the treatment for patients with classic high-grade osteosarcoma before 1970, and 80% of the patients died with metastatic disease. During the next two decades, great strides were made in the treatment of classic high-grade osteosarcoma so that, currently, approximately 70% of patients with the disease survive and limb-sparing surgery is possible in about 90% of patients. Modern therapy for osteosarcoma begins with accurate clinical staging, the final step of which is biopsy10. The current standard of treatment is multiagent preoperative (neoadjuvant) chemotherapy combined with wide resection or amputation followed by postoperative (adjuvant) chemotherapy.
The history of the development of the use of chemotherapy for osteosarcoma is an interesting one. In 1974, the New England Journal of Medicine published reports on two chemotherapy trials that claimed marked improvement in the survival of patients with osteosarcoma when surgery was followed with adjuvant chemotherapy18,19. This finding seemed to set the stage for the accepted use of adjuvant therapy in the treatment of osteosarcoma. However, an alternate theory, attributing the apparent increase in survival not to the chemotherapy but to a change in the natural history of the disease, was espoused. A randomized trial was then done to compare surgery combined with adjuvant high-dose methotrexate therapy and surgery without chemotherapy. The study, which was published in 1984, showed identical five-year survival rates of 42% in the two groups, supporting the theory of a change in the natural history of the disease20. In response to this intriguing data, two prospective, randomized studies were begun to answer definitively the question of the efficacy of chemotherapy in the treatment of osteosarcoma. One was performed at the University of California at Los Angeles, and the other was a multi-institutional study. Both studies21,22 showed substantial differences between the treatment groups with respect to two-year survival rates. The patients treated with surgery and adjuvant chemotherapy had a two-year survival rate of >60%, whereas those treated with surgery alone had a two-year survival rate of <20%.
In the 1970s, Rosen et al. showed a dramatic increase in survival of patients treated with preoperative (neoadjuvant) chemotherapy23. One of the arguments for neoadjuvant chemotherapy was that it prevented the development of resistant clones in a tumor with a rapid doubling time. Postponing the institution of chemotherapy until after surgery might allow spontaneous mutations to occur, resulting in resistant clones. The second argument was that preoperative chemotherapy would kill the microscopic metastases (that could eventually kill the patient) already present in the majority of patients at the same time that it was treating the primary tumor. Neoadjuvant chemotherapy may also shrink the primary tumor and sterilize microscopic tumor foci in the reactive zone around it, facilitating resection and increasing the chance for limb-sparing surgery. Neoadjuvant chemotherapy also allows time for surgical planning, the fabrication of a custom tumor prosthesis, or the procurement of allograft tissue for implantation. Finally, neoadjuvant chemotherapy induces necrosis in the primary tumor, and the amount of this necrosis serves as an extremely important prognostic indicator for long-term survival. To date, however, no large studies have shown increased survival of patients receiving preoperative chemotherapy compared with those receiving postoperative therapy24. Because of these theoretical advantages, most protocols include neoadjuvant chemotherapy. The drugs that are most commonly used in combination for the treatment of osteosarcoma are doxorubicin, high-dose methotrexate, cisplatin, and, most recently, ifosfamide25.
Successful surgical management is predicated on attaining wide surgical margins. This can be accomplished either by limb-sparing resection or by amputation. There does not appear to be any significant difference in long-term survival between patients who undergo amputation and those who have a limb-sparing procedure provided that wide margins are obtained26. Limb-sparing surgery is indicated for patients in whom wide margins can be obtained without sacrificing so much tissue that the remaining limb is nonfunctional. Usually, the determining factor is the ability to spare major nerves. Major vessels need to be preserved or reconstructed. There must be adequate soft-tissue coverage either locally or in the form of flaps to ensure survival of the reconstruction. The overall reconstruction should function as well as or better than an appropriate prosthesis after an amputation. The options for reconstructing the skeletal defect include osteoarticular allograft, intercalary allograft, a metal endoprosthesis, an allograft-prosthesis composite, arthrodesis, rotationplasty, and free vascularized fibular transfer.
Current management protocols provide long-term survival rates of between 60% and 80% for patients without clinically apparent metastatic disease at presentation24,27. Patients who have clinically apparent metastases at presentation fare considerably worse, with five-year survival rates of between 10% and 20%28,29. When pulmonary metastases develop after completion of therapy and the metastases can be resected, a five-year survival rate of 20% to 40% can be expected30.

Clinical Prognostic Factors

The single most predictive factor in osteosarcoma is the presence or absence of detectable metastatic disease at presentation. As mentioned, the survival rate for patients who have metastases at the time of presentation is between 10% and 20%28,29. Those who present with bone or skip metastases fare even worse12,30. The degree of tumor necrosis after neoadjuvant chemotherapy is also an important prognostic factor. Patients who have tumors with a good response to chemotherapy (>90% tumor necrosis) have a considerably better long-term survival rate than those who have tumors with a poor response (<90% tumor necrosis)24,27,31. Large tumor size has been implicated as a negative prognostic indicator in several studies; however, inconsistent methods of determining size in these studies make it difficult to ascertain its true influence. Other poor prognostic variables reported in the literature include elevated serum lactate dehydrogenase and alkaline phosphatase levels8,9. A tumor located in the pelvis, proximal part of the femur, or proximal part of the humerus also appears to be indicative of a poor prognosis in some studies32.

Molecular and Genetic Considerations

Cytogenetics

Ewing sarcoma and many soft-tissue sarcomas demonstrate consistent cytogenetic abnormalities, such as reciprocal chromosomal translocations, that are important in the diagnosis and pathogenesis of the disease. In classic high-grade osteosarcoma, no consistent chromosomal alteration with diagnostic, therapeutic, or prognostic importance has been found to date. In fact, the karyotypes are often bizarre, containing multiple aberrations that are highly inconsistent between tumors. This finding has led to the use of molecular methods to identify events that may be important in the pathogenesis of osteosarcoma.

Tumor Suppressor Genes

A tumor suppressor gene is any gene that by its loss of function contributes to the pathogenesis or progression of a tumor. This can occur at the level of the gene or at the level of the protein for which it codes. Often, tumor suppressors function as cell-cycle regulators. The hallmark of a putative suppressor gene is loss of the genetic material coding for a protein that is important in the regulation of the cell cycle or its proliferation. Studies on loss of heterozygosity (loss of one allele on a chromosome) have shown allele loss on chromosome arms 17p, 13q, 3q, and 18q in >50% of osteosarcomas studied33. These findings suggest the existence of putative suppressor genes in these regions33. The known tumor-suppressor gene p53 and the retinoblastoma (Rb) gene are the most frequently mutated in osteosarcoma (mutated in 25% to 80%) and are localized to chromosome arm 17p and 13q, respectively33-35. Kruzelock et al. recently localized a novel putative tumor-suppressor gene on chromosome arm 3q in osteosarcoma36.
The p53 gene product functions as a cell-cycle regulator and has the ability to induce apoptosis (programmed cell death). It can cause the cell to pause during the cell cycle to repair genetic damage, or it can cause apoptosis in the cell if repair of this damage is not possible. A defect in this gene or its protein might then allow a mutated cell to proliferate without control, propagating DNA damage to its progeny. Loss of p53 function in osteosarcoma has been demonstrated to occur by several mechanisms, including point mutation, gross loss of genetic material, and inhibition of its protein function by the murine double-minute 2 (MDM2) gene product37,38. Although it is one of the most commonly altered genes in osteosarcoma, little association with disease progression or prognosis has been demonstrated.
The retinoblastoma (Rb) gene was the first characterized tumor-suppressor gene. It acts as a negative transcriptional regulator of genes involved in the cell-cycle progression from G1 to S phase. Loss of this function allows cells to progress through the cell cycle unchecked. Allele loss of the Rb gene has been reported in approximately 50% to 60% of osteosarcomas33,36. A recent study has demonstrated that loss of heterozygosity at the Rb locus on chromosome arm 13q is a predictor of poor outcome in patients with osteosarcoma35.

Oncogenes

The effect of oncogenes on tumorigenesis is different from that of tumor suppressors in that mutation of a normal proto-oncogene to an oncogene confers a gain of function, as opposed to a loss, driving the cell toward a malignant phenotype. C-myc is a proto-oncogene transcription factor found to be overexpressed in many human cancers. C-fos is another transcription factor implicated in many cell processes including cell-cycle progression. It is also involved in osteoblast and chondrocyte differentiation. In a recent study39, both c-myc and c-fos were shown to be overexpressed in osteosarcoma, especially in pulmonary metastases. Seven of thirty-eight patients showed an overexpression of both c-fos and c-myc, and these patients had a significantly lower rate of disease-free survival than did patients with overexpression of only one of the two transcription factors (p < 0.05) .
Her2/erbB-2 is a cellular proto-oncogene that encodes the human epidermal growth-factor receptor 2 (Her2). Overexpression of this oncogene induces malignant transformation of rodent fibroblasts and has been implicated in decreased survival of patients with breast carcinoma. Recently, two studies have shown overexpression in approximately 40% of the osteosarcomas and a correlation with decreased event-free survival and histological response to neoadjuvant chemotherapy40,41. With the development of additional prospective studies, the presence of the Her2/erbB-2 receptor eventually may emerge as a significant prognostic indicator. It may also become a treatment target, with use of recombinant anti-Her2 monoclonal antibody for tumors positive for overexpression. Phase-II trials are currently under way.
The MDM2 gene codes for a p53 binding protein and is located on chromosome arm 12q13, a region that is often amplified in a variety of sarcomas. It has the ability to inhibit the transcriptional activity of p53, providing an alternative pathway of p53 inactivation. MDM2 has been found to be amplified in approximately 4% to 7% of osteosarcomas38. It is marginally associated with locally recurrent and metastatic disease but cannot be used currently as a prognostic marker38.
The MDR1 (multidrug resistance) gene codes for an adenosine triphosphate-dependent cellular efflux pump (p-glycoprotein) that actively transports doxorubicin (among other drugs) out of the cell. It would make sense that cells overexpressing MDR1 would be relatively resistant to doxorubicin, an important agent in the treatment of osteosarcoma. Indeed, several large, retrospective, immunohistochemical analyses of p-glycoprotein expression in osteosarcoma have shown a highly significant correlation between low survival rates and p-glycoprotein expression (p < 0.001)42,43. However, other studies have not demonstrated this finding40. Recently, in a large, prospective multi-institutional study of MDR1 mRNA levels in osteosarcoma, Wunder et al. demonstrated no correlation between MDR1 gene expression and prognosis44. Although the logic behind the theory that MDR1 confers a resistant phenotype upon osteosarcoma cells is attractive, its true effect remains somewhat controversial.

Angiogenesis

One of the most interesting topics in cancer therapy is that of anti-angiogenesis. Very little work on sarcomas has been done in this field. Anti-angiogenic agents have been shown to inhibit tumor growth and cause tumor regression in mouse models45. There are currently many anti-angiogenic agents being tested in Phase-I and II clinical trials of their effects on human cancers. Two of the targets of these trials are vascular endothelial growth factor and its receptors. Kaya et al. recently demonstrated expression of vascular endothelial growth factor in seventeen (63%) of twenty-seven osteosarcomas46. They also correlated this expression with a high prevalence of pulmonary metastasis, suggesting that expression of vascular endothelial growth factor may play a role in the metastatic cascade of osteosarcoma46. Given these findings, two drugs currently in Phase-II trials, an antivascular endothelial growth-factor antibody and a vascular endothelial growth-factor receptor inhibitor, may well prove advantageous in the treatment of osteosarcoma.
In the near future, molecular analysis may very well help to stratify patients with osteosarcoma into relative risk groups (molecular staging), allowing more tailored treatment regimens. In addition, we hope that, with further progress, highly selective targets for antisarcoma therapy without the substantial morbidity of current cytotoxic chemotherapy will be identified.
Great strides have been made in the diagnosis and treatment of Ewing sarcoma over the last three decades. With the advent of modern chemotherapy, the long-term survival rate has improved to approximately 70%47-58. Originally, treatment consisted of surgery or irradiation of the tumor, and the rate of survival was approximately 5% to 10%47,49-58. When adjuvant chemotherapy was added in the 1970s, survival improved and the treatment of the primary site became controversial. Currently, surgical resection has become the treatment of choice in the multidisciplinary management of Ewing sarcoma.
Ewing sarcoma is a malignant small-round-cell bone tumor47,48. It is the second most common primary malignant bone tumor in children and accounts for approximately 10% of all primary malignant bone tumors. The peak prevalence of Ewing sarcoma is during the second decade of life, with 80% of tumors occurring in patients who are less than twenty years old. There is a male preponderance. The tumor presents most frequently in the lower extremities and the pelvic girdle but can occur in any bone.
A great deal of progress has been made in understanding the biological mechanisms and refining the diagnosis of Ewing sarcoma. James Ewing believed that the tumor was of vascular origin and, in 1921, he called it "diffuse endothelioma of bone."59 More recently, cytogenetic as well as immunohistochemical studies have supported a neural cell origin developing into the concept of small-round-cell neuroectodermal lesions of bone and soft tissue49,60,61. This family of tumors includes Ewing sarcoma, primitive neuroectodermal tumor, atypical Ewing tumor, and Askin tumor. Cytogenetic studies have shown that these tumors share reciprocal translocations, which are identical in Ewing sarcoma and primitive neuroectodermal tumor49,60,61. Currently, the treatment of these tumors is very similar, with multidrug chemotherapy for systemic treatment and surgery and/or radiation therapy for control of the primary tumor.

Clinical and Radiographic Presentation

The most common presenting symptoms of Ewing sarcoma include pain, swelling, or a mass. Approximately 20% of patients present with a fever, which may lead to the mistaken diagnosis of infection. Laboratory studies are nonspecific but may reveal anemia, leukocytosis, or an increased erythrocyte sedimentation rate. Osteomyelitis is more common than Ewing sarcoma, and the general orthopaedic surgeon must consider both entities in the differential diagnosis. During an open or needle biopsy, Ewing sarcoma often has the appearance and consistency of pus, and it is vital to send the biopsy material for frozen section in addition to performing cultures. Pathological fractures occur in 10% of cases, and neurological compromise is possible with vertebral lesions. Patients with rib lesions often present with a malignant pleural effusion.
Any portion of any bone may be involved by Ewing sarcoma, which typically has a mottled, permeative radiographic appearance (Fig. 2). Periosteal reaction, with a laminated or "onion-skin" appearance, is common in Ewing sarcoma, but it is not pathognomonic. Frequently a large, unmineralized soft-tissue mass (best seen with magnetic resonance imaging) is associated with the osseous lesion. The magnetic resonance imaging scan is repeated after several cycles of chemotherapy to assess the response of the tumor to the neoadjuvant regimen and to help to plan definitive treatment of the primary lesion. There has been recent interest in the use of dynamic magnetic resonance imaging scans to assess more accurately the viability of the tumor before definitive local control is undertaken50. The presence and extent of metastatic disease is evaluated with a radiograph and computed tomography scan of the chest, a bone scan, and a bone-marrow aspirate. The bone scan is important, as 10% of patients have involvement of multiple bones at presentation. Studies including renal function and liver function tests and an evaluation of cardiac function are performed routinely before chemotherapy.

Pathological Characteristics

Grossly, Ewing sarcoma is a gray-white tumor with a variable amount of necrosis, hemorrhage, or cyst formation. At times, the tumor tissue may be almost liquid, mimicking purulence. Histologically, it is composed of numerous small round cells with a diffuse homogeneous growth pattern and sparse intercellular stroma (Fig. 3). The cells have ill-defined borders and a finely dispersed chromatin pattern. Mitotic activity is seldom high, and the cells are quite uniform. Atypical Ewing tumor is a histological variant in which the cells have larger, more irregular nuclei and more prominent nucleoli.
Previously, Ewing sarcoma was differentiated from other small-round-cell tumors by the presence of glycogen in the cells as seen with a periodic acid-Schiff stain51. However, current advances in cytogenetics and immunohistochemistry allow more precise diagnostic evaluations. Ewing sarcoma and primitive neuroectodermal tumor cells strongly express the p30/32 MIC2 antigen, which is a cell-surface glycoprotein encoded by the MIC2 gene49. This glycoprotein can be recognized by commercially available monoclonal antibodies, which help to differentiate Ewing sarcoma and primitive neuroectodermal tumor from lymphoma and embryonal cell rhabdomyosarcoma. The MIC2 analysis has a sensitivity of up to 95% in the diagnosis of Ewing sarcoma. There is minimal false-positive reactivity with lymphoblastic lymphoma and other tumors.
Cytogenetic studies have revealed that 85% of Ewing sarcomas and primitive neuroectodermal tumors contain the t(11;22)(q24;q12) balanced chromosomal translocation49,52,60,61. The breakpoints on chromosomes 22, 21, and 11 are the EWS, ERG, and FLI-1 genes, respectively. These translocations have been cloned and are identical in Ewing sarcoma and primitive neuroectodermal tumor. The EWS/FLI-1 or EWS/ERG fusion transcripts can be amplified by reverse transcriptase-polymerase chain-reaction60. Scotlandi et al. compared immunohistochemical studies with reverse transcriptase-polymerase chain-reaction and found that fusion transcripts analyzed by reverse transcriptase-polymerase chain-reaction were much more specific than immunostaining with use of a monoclonal antibody61. The definitive prognostic importance of these specific translocations has yet to be identified.
Ewing sarcoma and primitive neuroectodermal tumor have a number of unifying characteristics47. The translocations are highly specific for these two tumors, both express an MIC2 gene on the cell membrane, and they respond to similar drugs. Primitive neuroectodermal tumor has more characteristic histological features, with Homer-Wright rosettes in a fibrillary background, a lobular arrangement of cells, and densely clumped nuclear chromatin. In addition, electron microscopy demonstrates prominent organelles and neurosecretory granules47. Studies have shown no difference in survival between patients with Ewing sarcoma and those with primitive neuroectodermal tumor when histological criteria are used for diagnosis47, but more elaborate analyses may be able to differentiate these two lesions in terms of patient outcome.

Chemotherapy

Dramatic advances have been made in the treatment of Ewing sarcoma in the last two decades. Development of effective chemotherapy was a major breakthrough in the prevention and control of disseminated disease, which increased the five-year survival rate from 5% to 10% twenty years ago to >70% at the current time47,49-58. In 1981, the First Intergroup Ewing Sarcoma Study demonstrated that the addition of doxorubicin to the three-drug combination of vincristine, cyclophosphamide, and actinomycin D increased survival57. The Second Intergroup Sarcoma Study demonstrated that the intensity of drug dosage was important for relapse-free survival, as intermittent administration of high-dose vincristine, actinomycin D, cyclophosphamide, and Adriamycin (doxorubicin) (VACA) was found to be superior to continuous administration of a moderate dosage of the same regimen54. A combined study of the Children’s Cancer Group and the Pediatric Oncology Group showed that a more aggressive regimen, adding ifosfamide and etoposide to vincristine, actinomycin D, cyclophosphamide, and Adriamycin, improved the event-free survival rate of patients with nonmetastatic disease. The greatest effect was seen in large pelvic tumors and in patients who were less than nine years old55,56,58,62. Current studies focus on intensifying the alkylating agents and administering more intense chemotherapy over a shorter time-period.

Prognosis

A number of major prognostic factors have been identified in Ewing sarcoma63-69. Recognition of such factors may help to categorize this tumor according to risk status so that future treatment protocols can be modified. Patients with Ewing sarcoma in distal sites or a rib fare better than do patients with central lesions, and those with a pelvic lesion have the least favorable prognosis53,62. An initial tumor size of >8 to 10 cm, large volume, and metastatic disease at the time of diagnosis are negative prognostic indicators63,65,69. Picci et al., in a review of the experience at the Rizzoli Institute, found significantly improved survival when there was a good histological response to neoadjuvant chemotherapy (p = 0.004)67,68.

Local Control

Classically, treatment for Ewing sarcoma has been chemotherapy and radiation, with surgical resection reserved for expendable bones47,48. The newest trends, however, suggest that surgery should always be considered when the surgeon believes that the primary tumor can be removed completely. Radiation therapy is still used for tumors in anatomic sites where total resection cannot be done, when the functional deficit is unacceptable to the patient, and when an attempted resection has unacceptable margins. Additional site-specific analyses of the oncological results of resection and the long-term functional results of reconstruction are necessary before definitive recommendations can be made.
Several retrospective studies have shown that surgical excision of the primary tumor improves survival. A study from the Mayo Clinic showed a five-year survival rate of 74% for patients who had surgical excision of the primary tumor compared with 34% for those who had radiation alone for local control69. In a study of forty-six patients with Ewing sarcoma treated at Massachusetts General Hospital, 92% of those treated with surgical resection were alive at five years compared with 37% of those treated without surgical resection70. This survival advantage is maximized in patients with a pelvic tumor. One possible explanation for the increased survival rate is that surgical resection of the tumor eliminates residual clones of chemotherapy-resistant cells before they have a chance to recur locally or to metastasize. Patients treated with surgery alone or with surgery and radiation tend to have a lower recurrence rate than patients treated with radiation alone. This trend becomes more important as patients are followed for longer than five years, as it is not unusual to see late local recurrences after radiation71. Bacci et al. reported local recurrence in 36% of patients treated with radiation alone, with 14% of the recurrences occurring four years after completion of treatment53. Overall survival was improved significantly by operative treatment (p < 0.001). In another study, the local recurrence rate was 3.7% for patients managed with surgery compared with 24% for those who did not have surgical excision69. The prevalence of local recurrence is greatest in patients with a pelvic lesion. An alternative explanation for these more favorable results is a selection bias for performing surgery on smaller and more surgically resectable tumors.
With the increase in long-term survival rates as a result of modern chemotherapy, the problems of late local recurrence, functional impairment secondary to radiation complications, and radiation-induced sarcomas have been better appreciated71-74. The local recurrence rate in patients treated with radiation alone is 15% to 20%, and this adversely affects survival. The complications of radiation therapy are most pronounced in skeletally immature patients and include limb-length discrepancy, joint contracture, muscle atrophy, and pathological fracture72. The risk of radiation-induced malignant tumors is becoming more apparent with longer patient survival and is particularly high in patients who have received doses of radiation in excess of 60 Gy73,74. Tucker et al. showed that the relative risk of secondary sarcoma formation after irradiation for Ewing sarcoma increases with time74. In a group of 649 children, they found that the cumulative mean probability of secondary sarcoma formation in patients with Ewing sarcoma was 22%, second only to that in patients with retinoblastoma.
The current philosophy of treatment is to utilize neoadjuvant chemotherapy to decrease the size of the tumor, followed by wide resection for lesions in expendable or surgically reconstructible bones to avoid late chemotherapy-resistant recurrences48,65. It is not possible to identify precisely the indications for surgical resection of Ewing sarcoma; however, some general principles can be followed. First, the treatment plan needs to be individualized on the basis of the location, stage, and size of the tumor. Next, it is essential that a multidisciplinary team consisting of a medical oncologist, radiation oncologist, and orthopaedic oncologist formulate the treatment plan. The local therapy should not take precedence over, nor interfere with, systemic chemotherapy. Surgical resection should be done in all cases in which the surgeon believes that the primary tumor can be removed completely, particularly in expendable sites or surgically reconstructible sites. If an adequate margin is not achievable or is found to be inadequate (<1 cm) at the time of resection, local radiation therapy should be added. In general, a combination of surgery and radiation therapy allows use of a dose of 45 Gy, which minimizes the side effects of radiation. It is important to try to avoid complicated surgical reconstructions, which may delay the initiation of postoperative chemotherapy. When a complicated reconstruction is required, the surgeon should consider performing a temporary, less complex reconstruction first and delaying the more complex reconstruction until the entire chemotherapy regimen has been administered.
Treatment principles vary depending on the location of the primary tumor. Long-bone lesions generally can be managed by limb-sparing resection and reconstruction (Figs. 4-A and 4-B). If radiation is used in combination with surgery, metal prostheses provide a more reliable reconstruction. Intercalary allografts are prone to delayed union or nonunion at the host-graft junction, especially in patients receiving chemotherapy or radiation, and may need to be combined with an immediate or delayed vascularized fibular graft75. Limb-salvage surgery is possible in most cases, but amputation is occasionally necessary when the tumor is extremely large, a pathological fracture is unmanageable, or the lesion is in the distal aspect of the lower extremity in a very young child.
A pathological fracture through a Ewing sarcoma, which occurs in 5% to 10% of patients, poses a special problem48,76. Tumor cells disseminate in the fracture hematoma, the severity of which is related to the degree of fracture displacement. Limb-sparing in the setting of a pathological fracture may be difficult. Often the limb can be immobilized in a cast or external fixator while the patient continues preoperative chemotherapy. With a good response to chemotherapy, the fracture often heals. Magnetic resonance imaging scans are necessary before and after chemotherapy. Unlike a pathological fracture through an osteosarcoma, which necessitates resection of all anatomical areas that have been contaminated with tumor cells, it may be possible to sterilize residual contaminated areas around a pathological fracture through a Ewing sarcoma with external beam irradiation following a more conservative resection.

Problem Sites

Pelvis

Ewing sarcoma in the pelvis is particularly difficult to manage because of the large tumor volume and complex anatomy62,65,77,78 (Fig. 5). The overall prognosis for such patients is poor. Radiation is not completely effective for local control, but the role of surgery for pelvic tumors remains controversial. Complete resection of the primary tumor may improve local control, increase disease-free survival, and eliminate the possibility of postradiation sarcoma. In a study from Massachusetts General Hospital, the addition of surgery was not a favorable prognostic factor, but other series have suggested better local control following surgical resection of pelvic lesions53,62,70,78. Frassica et al. reported that 20% of 181 patients with Ewing sarcoma evaluated over a sixteen-year period had involvement of the pelvic ring77. Nine patients were excluded from the study, and the remaining twenty-seven patients were categorized into three groups according to the type of local treatment and whether they had metastases at the time of initial presentation. The surgically treated group had better overall survival, with a low rate of local recurrence. These retrospective studies must be interpreted with caution as they involve limited numbers of patients; however, there seems to be a trend for prolonged survival and a decreased risk of local recurrence in patients treated with surgery for local tumor control. The functional outcome after surgery needs to be measured against the risk of local recurrence and the development of a secondary malignant tumor after radiation.

Proximal Part of the Femur

The appropriate treatment to achieve local control of Ewing sarcoma of the proximal part of the femur is still a subject of debate, and the long-term durability of proximal femoral reconstructions is not known. Currently, the two most popular options are proximal femoral replacement prostheses and allograft-prosthetic composite reconstructions (Figs. 6-A, 6-B, 6-C, 6-D, and 6-E). In Ewing sarcoma, the outcome of these reconstructions should be compared with that of irradiation following conventional treatment, which also has limitations. The cases of sixteen patients with Ewing sarcoma of the proximal part of the femur who were treated in the modern chemotherapy era were reviewed76. Local control involved radiation alone in fourteen patients (two patients who were treated with prophylactic internal fixation were excluded), and the most notable orthopaedic problem was a pathological fracture, which occurred in eleven patients. The fractures were divided nearly equally between those occurring early and those occurring late. Possible factors contributing to early fractures include extensive infiltration of the bone with sarcoma cells, technical errors in the biopsy technique, and poor compliance with protected-weight-bearing precautions. In the late phase of treatment, the bone is weakened by infiltration of tumor cells and the osteonecrotic effects of radiation. While structural demands on the proximal part of the femur make it a difficult site to reconstruct reliably following resection, the same structural demands result in a high rate of pathological fracture when radiation is the primary local treatment. Currently, the two treatment options are a resection of the lesion after neoadjuvant chemotherapy or prophylactic intramedullary fixation after completion of radiation and chemotherapy.

Spine

Fortunately, only 3.5% of patients with Ewing sarcoma have spinal involvement, and this rate decreases to 1% if the sacrum is excluded48,79. Although primary lesions of the spine are rare, metastasis of Ewing sarcoma to the spine is common in the terminal stages. In a retrospective study of thirty-six patients with Ewing sarcoma of the spine, twenty-one (58%) presented with neurological deficits79. The most common location was the lumbar or lumbosacral spine. All patients were treated with radiation and chemotherapy. Of the patients with neurological deficits, the majority had improvement after decompressive laminectomy. The five-year survival rate was 33%, and there was no difference in the disease-free survival rate between patients with a primary lesion of the sacrum and those with a tumor in the mobile spine, although other studies have found that sacral lesions portend a worse prognosis80. Local recurrence occurred in approximately one-half of the patients. Anterior spinal procedures have gained widespread popularity in the last decade and have a growing role in the treatment of Ewing sarcoma, particularly with the high prevalence of late kyphosis following conventional radiation therapy. Because complex surgical procedures for Ewing sarcoma of the spine frequently are performed in a staged fashion, it may be prudent to complete chemotherapy and radiation preoperatively so that the postoperative recovery and possible complications of vertebral resection and reconstruction do not interfere with systemic treatment.
In summary, considerable strides have been made in the treatment of Ewing sarcoma as currently about 70% of patients are long-term survivors47,49-58. A multidisciplinary team approach is necessary to combine chemotherapy, surgery, and/or radiation in the care of the patient. New developments in molecular biology and cytogenetics have allowed a more accurate diagnosis to be made and may have prognostic implications in the future. Modern multidrug chemotherapy is the mainstay of current treatment. Historically, local control of the tumor was achieved with radiation, but an important role for surgery is evolving with improved limb-salvage techniques. Surgical resection of the tumor in reconstructible bones is often a reasonable option, decreasing the risk of local recurrence and the development of radiation-induced sarcoma. The treatment plan must be individualized on the basis of the location, stage, and size of the tumor. Future studies will focus on the treatment of patients with metastatic disease, as their overall survival remains poor.
Chondrosarcoma of bone is the third most common primary malignant bone tumor following osteosarcoma and Ewing sarcoma. Chondrosarcoma can arise de novo (primary) or secondary to a preexisting benign cartilaginous lesion (for example, exostosis, enchondroma, or, rarely, synovial chondromatosis). Chondrosarcomas can be classified according to the relationship to the underlying bone (peripheral compared with central), as primary or secondary, or by histological type.

Pathological Characteristics

The histological classification of cartilaginous tumors poses a great diagnostic challenge to the musculoskeletal pathologist81-87. The difficulty lies in differentiation between benign active and low-grade malignant cartilaginous lesions. These tumors look similar histologically, and there are no markers that clearly allow distinction. The most difficult distinction is between enchondromas and low-grade central chondrosarcomas. Because of the similarity, clinical and radiographic criteria must be used to separate a benign enchondroma from a low-grade malignant cartilaginous neoplasm. The identification and classification of high-grade, dedifferentiated, clear-cell, and mesenchymal chondrosarcoma require extensive knowledge and yet are less controversial.
Cartilaginous tumors usually can be classified as benign, borderline (grade 1/2), low-grade malignant, or high-grade malignant. Low-grade chondrosarcomas can be distinguished from enchondromas histologically on the basis of cortical destruction or permeation of cancellous bone or the development of a soft-tissue mass. High-grade chondrosarcomas typically show severe cytologic atypia and a high mitotic rate.

Radiographic Characteristics

Cartilaginous neoplasms, which are difficult to classify on the basis of histological findings, can frequently be identified by their radiographic appearance (Table I). Enchondromas typically are metaphyseal in location and do not have an extraosseous soft-tissue mass, cortical destruction, or periosteal reaction. In contrast, low-grade central chondrosarcomas cause a periosteal reaction, may destroy the cortex, and often have an extraosseous soft-tissue mass (Figs. 7-A, 7-B, 7-C, 7-D, and 7-E); these lesions are usually seen in patients who are older than thirty years of age. The development of a thickened cartilaginous cap (>2 cm) is a sign of malignant transformation from an osteocartilaginous exostosis to a secondary chondrosarcoma. Mesenchymal chondrosarcomas and dedifferentiated chondrosarcomas usually have a more aggressive radiographic appearance. Clear-cell chondrosarcomas frequently present as a destructive lesion in the epiphyseal portion of a long bone.

Chondrosarcoma Secondary to Exostosis

Chondrosarcomas arise from <1% of osteocartilaginous exostoses. Exostoses stem from an outgrowth of the physis due to a defect in the perichondral node of Ranvier that surrounds it. They can occur singly or multiply in the genetic syndrome of multiple hereditary exostoses. The classic radiographic feature of an exostosis is that of an osseous stalk arising from the metaphysis of a bone covered with a cartilaginous cap. The cartilaginous cap is analogous to the physeal plate. The histological organization of the cap, with columns of chondrocytes, resembles that of the physis, albeit in a disorganized fashion. During growth, the cartilaginous cap proliferates, enchondral ossification takes place, causing the stalk to grow, and the exostosis enlarges. At the time of skeletal maturity or shortly thereafter, the cartilaginous cap becomes quiescent and the exostosis stops growing. Histologically, the cap becomes less active and thin (usually <1 cm). When a secondary chondrosarcoma develops, the cartilaginous cap begins to grow uncontrollably and the cap thickens (>2 cm). These secondary sarcomas are almost always histologically low-grade and slow-growing, and patients are at a low risk for metastases. Metastatic disease occurs in approximately 1% to 10% of patients with multiple hereditary exostoses and rarely in patients with solitary exostoses. If not treated surgically, the lesions can attain enormous size and cause local morbidity or even death. Rarely, they dedifferentiate into a highly malignant dedifferentiated chondrosarcoma. Treatment consists of surgical resection, with wide surgical margins. Education of patients with multiple hereditary exostoses and their families is important to facilitate early recognition and diagnosis.

Central Chondrosarcoma

Central chondrosarcoma can arise secondary to an enchondroma or de novo within a bone. Chondrosarcomas are almost always associated with pain, while enchondromas rarely are. Because pain is often associated with other musculoskeletal conditions (for example, rotator cuff arthropathy), the difficult clinical problem is ascertaining whether the pain reported by the patient is due to the apparent bone lesion or to some other problem. When the lesion has no radiographic signs of chondrosarcoma but seems to be the cause of pain, classification as a painful enchondroma, a borderline chondrosarcoma, or "chondrosarcoma in situ" can be difficult. Treatment of these lesions varies, with expectant observation, intralesional curettage, and resection all being acceptable options. There is a low risk of local recurrence or metastasis of these controversial lesions. On the other hand, central chondrosarcomas that have all or some of the classic radiographic and clinical characteristics of a frank sarcoma—namely, cortical destruction, periosteal reaction, and a soft-tissue mass—will behave more like a true malignant tumor. These true central chondrosarcomas are typically low to medium-grade histologically, with a prevalence of metastatic disease of approximately 30%. Treatment is surgical resection. Chemotherapy or radiation therapy is indicated infrequently. For the more rare high-grade central chondrosarcomas, aggressive surgery with radical surgical margins or amputation is sometimes necessary for local control.

Clear-Cell Chondrosarcoma

Clear-cell chondrosarcoma, described by Unni et al. in 1976, is a rare variant of chondrosarcoma with a characteristic histological appearance and a specific anatomic predilection88,89. The histological appearance of clear-cell chondrosarcoma is a combination of immature chondroid matrix surrounding chondrocytes with a characteristic clear cytoplasm. Clear-cell chondrosarcoma arises primarily in the epiphyses of the long bones after skeletal maturity. Because of the similar anatomic distribution of clear-cell chondrosarcoma and chondroblastoma, careful histological distinction is necessary. Histologically, the differential diagnosis primarily includes other tumors that contain a clear cytoplasm, such as renal cell carcinoma, clear-cell sarcoma, mucinous adenocarcinoma, and the physaliferous cells of a chordoma. Immunohistochemical stains can help to distinguish between clear-cell chondrosarcoma and the other diagnoses. The prognosis for patients with clear-cell chondrosarcoma is intermediate, between those associated with low-grade and high-grade chondrosarcomas. Metastases occur most often in the lung but can occur in bone and may appear years later. Treatment is wide local excision. Chemotherapy and radiotherapy are indicated.

Dedifferentiated Chondrosarcoma

Dedifferentiated chondrosarcomas, first described by Dahlin and Beabout in 1971, occur when a benign or low-grade malignant lesion transforms into a highly malignant variety of sarcoma90,91. The diagnosis is made histologically when a high-grade sarcoma is found in conjunction with either an underlying benign or a lower-grade malignant cartilaginous bone tumor. The most common type of high-grade sarcoma is an osteosarcoma followed by malignant fibrous histiocytoma. These tumors tend to be radiographically, histologically, and clinically aggressive. The prognosis is quite poor, with few survivors two years after diagnosis and a five-year survival rate of only 10% to 15%. Treatment usually consists of either palliation with radiotherapy or radical ablative surgery. The role of chemotherapy has not been established.

Mesenchymal Chondrosarcoma

Mesenchymal chondrosarcoma is a rare variety of chondrosarcoma. Approximately 70% arise in bone, and 30% develop in soft tissue. The tumor consists of an immature cartilaginous matrix and aggregates of primitive mesenchymal cells. Since the mesenchymal component often predominates, the lesions are sometimes confused with Ewing sarcoma, lymphoma, or hemangiopericytoma. The most common anatomic areas of occurrence are the maxilla, mandible, vertebrae, and ribs. The radiographic features are usually a destructive lesion in bone with stippled calcification. Treatment is primarily surgical excision. Irradiation is indicated when the tumor cannot be completely excised. Adjuvant chemotherapy may improve overall survival.

Molecular and Genetic Considerations

Like osteosarcoma, chondrosarcoma has few consistent cytogenetic findings, with the exception of the t(9;22) (q22;q12) translocation, which is found in approximately 25% of extraskeletal myxoid chondrosarcomas. The translocation forms a fusion gene EWS/TEC that in turn codes for a protein that is a member of the orphan nuclear receptor family. It is thought that this receptor helps to control cellular proliferation and differentiation by modulating the response to specific growth factors or by interfering with the signaling pathway of retinoic acid92. Cytogenetic changes seen in high-grade bone chondrosarcomas are of a numerical, as opposed to a structural, type. Losses of chromosomes 10, 6, and 13 are often seen, and gains of chromosomes 7 and 20 are occasionally noted.
Collagenase activity is responsible, in part, for the ability of tumor cells to degrade and migrate through surrounding tissue. Recent in vitro studies93 have shown that increased collagenase activity and matrix metalloproteinase-1 gene expression, relative to its inhibitor, correlate directly with invasive potential and inversely with the level of differentiation in human chondrosarcoma cell lines. Collagenase activity may increase the ability of tumor cells to migrate in vivo, resulting in a poorer prognosis for patients with chondrosarcoma. Other proteases have been implicated in the progression of chondrosarcoma as well. Hackel et al. showed that overexpression of cathepsin B correlated significantly with increased rates of local recurrence in a study of 114 patients with chondrosarcoma (p = 0.006)94.

Treatment and Prognosis

The treatment of chondrosarcoma is primarily surgical since the response to chemotherapy and radiotherapy is relatively low95. Radiation therapy may be of benefit for the local control of chondrosarcoma or for palliation. Chemotherapy has been reported to be effective in the treatment of mesenchymal chondrosarcoma. The role of chemotherapy in the treatment of dedifferentiated or high-grade chondrosarcoma is unclear. The risk of local recurrence is related to the surgical margin obtained at the time of resection. Low-grade tumors have a high rate of local recurrence with intralesional margins. Wide or radical surgical margins are often necessary to gain local control of high-grade chondrosarcomas. The prognosis is related to the histological grade, the surgical stage, the subtype of chondrosarcoma, and, as found recently, to molecular markers. Future advances in the diagnosis and treatment of cartilaginous tumors are likely to result from their molecular characterization, allowing better prediction of clinical behavior. This should lead to better treatment and hopefully will solve the problem of differentiating between benign and low-grade cartilaginous neoplasms.
 
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+Fig. 1-A:Figs. 1-A and 1-B A ten-year-old boy with osteosarcoma in the knee. Fig. 1-A Anteroposterior radiograph of the knee, showing a bone-forming destructive lesion.
 
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+Fig. 1-B:Figs. 1-A and 1-B A ten-year-old boy with osteosarcoma in the knee. Fig. 1-B Axial magnetic resonance image revealing a soft-tissue mass and bone involvement. A biopsy revealed classic osteosarcoma.
 
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+Fig. 2:Anteroposterior radiograph of the femur in a nineteen-year-old woman, revealing a Ewing sarcoma. Note the periosteal reaction with a typical "onion skin" appearance. A pathological fracture occurred through the lesion.
 
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+Fig. 3:Photomicrograph of a typical Ewing sarcoma, showing small, round, uniform cells with scant cytoplasm (magnification, 60).
 
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+Fig. 4-A:Figs. 4-A and 4-B A seventeen-year-old girl with Ewing sarcoma in the right femur. Fig. 4-A Anteroposterior radiograph showing a scalloped appearance of the medial cortex with surrounding periosteal reaction.
 
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+Fig. 4-B:Figs. 4-A and 4-B A seventeen-year-old girl with Ewing sarcoma in the right femur. Fig. 4-B With a magnetic resonance imaging scan used as a guide to the intramedullary extent of the tumor, a wide resection followed by reconstruction with an intercalary allograft was performed.
 
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+Fig. 5:Axial computed tomography scan revealing a large soft-tissue mass on the right side of the pelvis of a patient with Ewing sarcoma.
 
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+Fig. 6-A:Figs. 6-A through 6-E A nineteen-year-old man with Ewing sarcoma in the proximal aspect of the femur. Fig. 6-A Anteroposterior radiograph showing periosteal reaction along the medial and lateral cortices.
 
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+Fig. 6-B:Figs. 6-A through 6-E A nineteen-year-old man with Ewing sarcoma in the proximal aspect of the femur. Fig. 6-B Coronal magnetic resonance image, made prior to chemotherapy, revealing a large circumferential soft-tissue mass and extensive intramedullary signal changes indicating the intraosseous extent of the tumor.
 
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+Fig. 6-C:Axial magnetic resonance image made prior to chemotherapy, revealing a large circumferential soft-tissue mass and involvement of the intramedullary canal.
 
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+Fig. 6-D:The soft-tissue mass greatly decreased in size following neoadjuvant chemotherapy.
 
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+Fig. 6-E:Postoperative anteroposterior radiograph of the proximal part of the femur after wide resection and reconstruction with use of an allograft-prosthesis composite.
 
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+Fig. 7-A:Figs. 7-A through 7-E A forty-five-year-old woman who had pain in the left hip. Fig. 7-A A plain radiograph revealing a destructive lesion in the proximal part of the femur, with cortical destruction and a soft-tissue mass.
 
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+Fig. 7-B:A technetium-99 bone scan showing a marked increase in uptake in the proximal part of the left femur and no other apparent lesions.
 
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+Fig. 7-C:Magnetic resonance imaging confirmed that the tumor involved the medullary cavity of the femur and extended into the soft tissue.
 
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+Fig. 7-D:Computed axial tomography scan showing the amount of bone destruction and the soft-tissue extension.
 
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+Fig. 7-E:Histological findings were consistent with an intermediate-grade chondrosarcoma.
 
Anchor for JumpAnchor for JumpTABLE I:  Radiographic Differentiation Between Enchondroma and Low-Grade Chondrosarcoma
*The differentiation between enchondromas and low-grade chondrosarcomas is one of the more difficult distinctions in musculoskeletal oncology. The distinction is made primarily on the basis of radiographic criteria since the histological features are indistinguishable.
Feature*EnchondromaChondrosarcoma
Cortical destructionAbsentUsually present
Soft-tissue massAbsentUsually present
Periosteal reactionAbsentUsually present
Endosteal scallopingSometimes presentFrequently present
CalcificationCommonCommon
Medullary fillingUnusualCommon
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+Fig. 1-A:Figs. 1-A and 1-B A ten-year-old boy with osteosarcoma in the knee. Fig. 1-A Anteroposterior radiograph of the knee, showing a bone-forming destructive lesion.
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+Fig. 1-B:Figs. 1-A and 1-B A ten-year-old boy with osteosarcoma in the knee. Fig. 1-B Axial magnetic resonance image revealing a soft-tissue mass and bone involvement. A biopsy revealed classic osteosarcoma.
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+Fig. 2:Anteroposterior radiograph of the femur in a nineteen-year-old woman, revealing a Ewing sarcoma. Note the periosteal reaction with a typical "onion skin" appearance. A pathological fracture occurred through the lesion.
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+Fig. 3:Photomicrograph of a typical Ewing sarcoma, showing small, round, uniform cells with scant cytoplasm (magnification, 60).
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+Fig. 4-A:Figs. 4-A and 4-B A seventeen-year-old girl with Ewing sarcoma in the right femur. Fig. 4-A Anteroposterior radiograph showing a scalloped appearance of the medial cortex with surrounding periosteal reaction.
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+Fig. 4-B:Figs. 4-A and 4-B A seventeen-year-old girl with Ewing sarcoma in the right femur. Fig. 4-B With a magnetic resonance imaging scan used as a guide to the intramedullary extent of the tumor, a wide resection followed by reconstruction with an intercalary allograft was performed.
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+Fig. 5:Axial computed tomography scan revealing a large soft-tissue mass on the right side of the pelvis of a patient with Ewing sarcoma.
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+Fig. 6-A:Figs. 6-A through 6-E A nineteen-year-old man with Ewing sarcoma in the proximal aspect of the femur. Fig. 6-A Anteroposterior radiograph showing periosteal reaction along the medial and lateral cortices.
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+Fig. 6-B:Figs. 6-A through 6-E A nineteen-year-old man with Ewing sarcoma in the proximal aspect of the femur. Fig. 6-B Coronal magnetic resonance image, made prior to chemotherapy, revealing a large circumferential soft-tissue mass and extensive intramedullary signal changes indicating the intraosseous extent of the tumor.
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+Fig. 6-C:Axial magnetic resonance image made prior to chemotherapy, revealing a large circumferential soft-tissue mass and involvement of the intramedullary canal.
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+Fig. 6-D:The soft-tissue mass greatly decreased in size following neoadjuvant chemotherapy.
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+Fig. 6-E:Postoperative anteroposterior radiograph of the proximal part of the femur after wide resection and reconstruction with use of an allograft-prosthesis composite.
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+Fig. 7-A:Figs. 7-A through 7-E A forty-five-year-old woman who had pain in the left hip. Fig. 7-A A plain radiograph revealing a destructive lesion in the proximal part of the femur, with cortical destruction and a soft-tissue mass.
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+Fig. 7-B:A technetium-99 bone scan showing a marked increase in uptake in the proximal part of the left femur and no other apparent lesions.
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+Fig. 7-C:Magnetic resonance imaging confirmed that the tumor involved the medullary cavity of the femur and extended into the soft tissue.
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+Fig. 7-D:Computed axial tomography scan showing the amount of bone destruction and the soft-tissue extension.
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+Fig. 7-E:Histological findings were consistent with an intermediate-grade chondrosarcoma.
Anchor for JumpAnchor for JumpTABLE I:  Radiographic Differentiation Between Enchondroma and Low-Grade Chondrosarcoma
*The differentiation between enchondromas and low-grade chondrosarcomas is one of the more difficult distinctions in musculoskeletal oncology. The distinction is made primarily on the basis of radiographic criteria since the histological features are indistinguishable.
Feature*EnchondromaChondrosarcoma
Cortical destructionAbsentUsually present
Soft-tissue massAbsentUsually present
Periosteal reactionAbsentUsually present
Endosteal scallopingSometimes presentFrequently present
CalcificationCommonCommon
Medullary fillingUnusualCommon
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