Tumors of cartilaginous origin represent one of the largest categories of skeletal neoplasms. It is a heterogeneous group of benign and malignant tumors composed either of pure cartilage or cartilage in combination with various amounts of myxoid, fibrous, or osseous tissue. Conventional radiography remains instrumental in the diagnosis of cartilaginous and other primary skeletal neoplasms. It provides the best opportunity to characterize the lesion and gives an initial assessment of tumor aggressiveness, size, and extent. In addition, computed tomography (CT) may detect subtle calcifications not visible on plain radiographs, and magnetic resonance (MR) imaging provides definitive local staging. MR's multiplanar imaging capability and superior soft-tissue contrast, compared to CT, allows for accurate evaluation of tumor invasion into adjacent muscles and neurovascular bundles. The extent of bone marrow involvement also is more reliably identified with MR than CT.

Considerable overlap exists in the MR appearance of histologically unrelated lesions. Most malignant tumors demonstrate low to intermediate signal intensity on T1-weighted (T1W) images, high signal intensity on T2-weighted (T2W) images, and marked enhancement following intravenous injection of gadolinium. Benign and low grade malignant tumors containing hyaline cartilage have a similar pattern but demonstrate unique characteristics that easily distinguish them from non-hyaline cartilage-containing tumors.1 This article will review basic cartilage biology and the MR imaging characteristics of the most common benign and malignant neoplasms that contain hyaline cartilage.

Cartilage biology

A basic knowledge of the different types and distribution of cartilage within the musculoskeletal system provides an insight into the imaging characteristics and location of hyaline cartilage-containing tumors. Hyaline cartilage and fibrocartilage are the two basic types found in the musculoskeletal system. They both are connective tissue of mesenchymal origin, characterized by a firm consistency and hypovascularity. Fibrocartilage is the primary constituent of synchondroses, symphyses, and menisci. Hyaline cartilage is a critical component of skeletogenesis; it also is found in physes, and it lines the articular surface of synovial joints.

The vast majority of the skeleton passes through an intermediate cartilage step during formation, a process termed enchondral ossification. The clavicle, mandible, and craniofacial bones are exceptions, as these undergo a different process called intramembranous ossification. The distribution of hyaline cartilage-containing tumors is greatly influenced by the process of ossification, with most lesions occurring in bones that are formed through enchondral ossification.

The structural differences between hyaline and fibrocartilage account for their different appearance on MR imaging. Compared to fibrocartilage, hyaline cartilage contains less collagen and more proteoglycan. The higher proteoglycan content results in higher water content. Fibrocartilage contains more collagen and less proteoglycan, therefore containing less water. On T2W images, hyaline cartilage characteristically demonstrates homogeneous increased signal intensity while fibrocartilage shows decreased signal intensity. Within tumors, hyaline cartilage grows in a lobular pattern, with or without fibrous septa, that can easily be seen on MR imaging. It may contain rings, arcs, or punctate areas of calcification that are detectable on conventional radiography, tomography, CT, or MR imaging.

Hyaline cartilage-containing tumors include osteochondroma, enchondroma, parosteal chondroma, low grade chondrosarcoma, chondroid chordoma, and chondroblastic osteosarcoma. Myxoid and chondroid are other types of cartilage encountered in these neoplasms. Myxoid cartilage is a variant of hyaline cartilage, contains prominent cystic cavities, and can be seen in some hyaline cartilage-containing tumors including chondrosarcoma, enchondroma, and parosteal chondroma. Chondroid refers to a primitive form of fibrocartilage and is typically associated with chondro-blastoma, chondromyxoid fibroma, mesenchymal chondrosarcoma, and certain osteosarcomas.

Hyaline cartilage-containing tumors

Osteochondroma-Osteochondromas are the most common benign cartilage-containing tumor.2,3 These heterogeneous tumors are composed of trabecular bone and marrow, are surrounded by a thin cortex, and are covered by a hyaline cartilage cap over the outer surface. The thickness of the hyaline cartilage is variable and dependent upon the degree of skeletal maturation and malignant transformation. Osteochondromas typically are located in the metaphyseal region of long bones and are connected to the host bone by either a broad base (sessile) or a narrow stalk (pedunculated). Osteochondromas most likely arise at the physeal periphery from reorientation of a physeal fragment, congenital perichondral deficiency or, rarely, following radiation.3,5

Osteochondromas may be discovered as an incidental finding or may present with nonspecific signs and symptoms, including a mass with or without pain, skeletal deformity, or pain caused by compression of adjacent neurologic structures. Complications include fracture through the osteochondroma, repetitive trauma to adjacent structures, and malignant transformation. The risk of malignant transformation of an isolated osteochondroma is approximately 1%. Malignancy should be suspected if there is growth of the osteochondroma after skeletal maturity or the thickness of the hyaline cartilage cap exceeds 2 to 3 cm. Malignant transformation typically results in low grade chondrosarcomas, although higher grade lesions are possible.6 If malignant transformation occurs, it usually is present in lytic regions or areas of bulky unmineralized cartilage.

Diagnosis of osteochondroma can be readily made with conventional radiography and rests upon demonstrating continuity of the host bone marrow cavity and cortex with that of the osteochondroma. The lesion can easily be identified as arising from the surface of bone pointing away from an adjacent joint. The lobular growth pattern of hyaline cartilage is recognized by the bulbous or lobular gross morphologic appearance to the end of the osteochondroma. However, the extent and pattern of mineralization within the hyaline cartilage can be overlooked at MR, though it is well demonstrated on CT. This degree of mineralization varies with cap thickness, and MR has been found to be superior in assessment of hyaline cartilage cap thickness and demonstration of the relationship of adjacent structures (figure 1). The cap typically is only several millimeters thick and will demonstrate low to intermediate signal intensity on T1W images, high signal intensity on T2W images, and no

or slight peripheral enhancement following intravenous injection of gadolinium.7 Both MR and CT display equally well the continuity of the osteochondroma marrow and cortex with that of the parent bone.

The risk of malignant transformation is higher in patients with hereditary multiple osteochondromatosis (15 to 20%). This disorder is transmitted as an autosomal dominant trait and results in multiple sessile and pedunculated osteochondromas distributed in a bilateral symmetric pattern. The polyostotic metaphyseal involvement can result in marked growth disturbances.

Enchondroma-Enchondromas are the second most common cartilage-containing neoplasms and, unlike osteochondromas, are composed of pure hyaline cartilage.2,3 They are benign, usually solitary intramedullary tumors which most likely arise from the physis as dysplastic, hypercellular hyaline cartilage nodules.8 Enchondromas even-tually separate themselves from the physis and reside within the metaphysis. This process may be of variable duration, resulting in enchondromas of variable size. A widespread, long-standing process could explain the abnormalities encountered in Ollier's disease, while a limited, localized process would result in a solitary enchondroma.

Enchondromas often are discovered incidentally or following pathologic fracture. Although pain associated with long bone enchondromas may be due to secondary chondrosarcoma, it must be distinguished from a pathologic fracture or adjacent joint or soft-tissue abnormality. Malignant transformation is a more worrisome complication of enchondroma. The age of the patient and duration of symptoms are important clues in determining the likelihood of malignant transformation. An adult patient with gradually increasing pain over a long duration in the region of a presumed enchondroma should be seriously considered to have a possible chondrosarcoma.

The distribution and radiographic appearance of enchondromas have been well described. They typically are centrally located within the medullary canal and have a predilection for the short tubular bones, proximal femur, and proximal humerus. Enchondromas usually are metaphyseal in location and demonstrate geographic destruction with a lobulated contour. There may be a variable amount of mineralization present, which would appear as small, punctate ring or arc-like densities and reflect dystrophic calcifications within small cartilage nodules or fragments of lamellar bone that encase the nodules. Focal areas of cortical endosteal scalloping also may be present. If the enchondroma arises within a small tubular bone (such as the phalanx, rib, or fibula), the bone may show expansion due to its small size.

MR of enchondroma shows low to intermediate signal intensity on T1W and prominent areas of high signal intensity on T2W images. CT and MR both are superior to conventional radiography for visualizing cortical destruction and associated soft-tissue mass, both ominous signs that indicate malignant transformation. Matrix calcifications identified on MR imaging are depicted as low signal intensity foci and are more apparent on gradient echo sequences. Normal marrow fat may be present interspersed between the cartilage nodules, a finding that indicates benignancy (figure 2). The use of intravenous gadolinium may be useful in distinguishing enchondromas from low grade chondrosarcomas;9,10 enchondromas typically show a peripheral enhancement pattern while chondrosarcomas demonstrate a septal enhancement pattern.

Chondrosarcoma-Chondrosarcomas are classified according to their site of origin and presence of a prior lesion. These tumors are termed central if they arise within the medullary canal, peripheral or exostotic if they arise from an osteochondroma, and juxtacortical if they arise from the surface of bone. Chondrosarcomas also are divided into primary or secondary categories, based upon the absence or presence of a preexisting lesion. Conventional chondrosarcomas are easily classified using these criteria. Nonconventional chondrosarcomas, however, require additional categories that reflect their unique pathologic features. This group includes dedifferentiated, mesenchymal, clear cell, and extraskeletal chondrosarcomas (table 1).

The majority of chondrosarcomas are central (either primary or secondary) or peripheral. As a group, they are slow growing, low grade lesions. Patients typically present with a history of gradually increasing pain which is often worse at night. Local swelling or a palpable mass may be present. These symptoms may be present for many years prior to diagnosis.

Conventional chondrosarcomas generally are composed of a single confluent mass of malignant hyaline to myxoid containing cartilage. Grossly, they have a lobular morphology, reflecting the growth pattern of cartilage with variable amounts of calcification. Diagnosis of low grade tumors may be difficult based upon cytologic criteria alone. Low grade tumors are cytologically bland, lacking distinguishing features from cellular (atypical) enchondromas. However, the presence of fibrous bands at the tumor-marrow interface has been used as a criterion to separate low grade chondrosarcomas from atypical enchondromas.11 Other criteria used in the diagnosis of malignancy include cortical thickening due to invasion of the haversian system and cortical erosion with or without associated soft-tissue mass.8 In comparison, high grade tumors show cellular anaplasia, allowing diagnosis by standard histologic examination.

Radiographic features of chondrosarcoma reflect the gross morphology and mineralization of the cartilage malignancy. Low grade chondrosarcomas may have a deceiving non-aggressive appearance on conventional radiography. Fortunately, most tumors are typically large, with a lobular appearance due to their slow growth rate pattern. Central lesions can demonstrate predominately lytic destruction, cortical thickening, broad areas of cortical scalloping, symmetric expansion of bone, and minimal calcification, with or without an associated soft-tissue mass. CT easily demonstrates the cortical changes and characterizes the mineralization, and MR reveals hyperintense signal intensity on T2W images due to the rich water content within the hyaline cartilage-containing lobules. Decreased signal intensity present on these images corresponds to intervening fibrous septa or calcification. Enhancement of the fibrous septa separating the cartilage lobules is evident following intravenous gadolinium and can be a useful finding in distinguishing between benign and low grade malignant cartilage tumors.9,10 Secondary peripheral or exostotic chondrosarcomas demonstrate similar radiographic appearances, though they lack alterations of the host bone. High grade neoplasms appear less lobulated, with more necrosis and loss of the septal enhancement pattern. Fortunately, these lesions are not difficult to diagnose histologically.

Approximately 10% of primary and secondary chondrosarcomas dedifferentiate into more anaplastic high grade sarcomas (dedifferentiated chondrosarcoma). Dedifferentiation can be seen with both low and high grade chondrosarcomas. It is defined histologically by the presence of high grade malignant tissue juxtaposed to chondrosarcoma. Radiographically, the transition is apparent. A more aggressive pattern of bone destruction may be identified, permeative or moth-eaten, with cortical destruction and soft-tissue mass. There is a poorer prognosis with higher incidence of metastasis similar to high grade sarcomas.

Chondrosarcoma cells do not require a vascular supply and can easily be transplanted. Any cells deposited within the surgical field are likely to result in a local recurrence (figure 5). Great care must be taken when treating chondrosarcomas that the surgical site and bone graft donor site are not contaminated with cartilage cells.

Conclusion

Knowledge of the types and distribution of cartilage provides a foundation for understanding the imaging characteristics and location of hyaline cartilage-containing tumors. These tumors have a characteristic appearance on MR imaging. Differentiation between enchondromas and low grade chondrosarcomas can be difficult when based only on histologic findings. Correlation with the imaging appearance can be extremely helpful in arriving at a correct diagnosis. AR

References

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2. Dahlin DC, Unni KK: Bone Tumors: General Aspects and Data on 8,542 Cases, ed 4, pp 8,34. Springfield, IL, Charles C. Thomas, 1986.

3. Moser RP: Cartilagenous Tumors of the Skeleton, pp 8,34-73. Philadelphia, Hanley and Belfus, Inc., 1990.

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5. Libshitz HI, Cohen MA: Radiation-induced osteochondromas. Radiology 142:643-647, 1982.

6. Garrison RC, Unni KK, McCleod RA, et al: Chondrosarcoma arising in osteochondroma. Cancer 49:1890-1897, 1982.

7. Lee JK, Yao L, Wirth CR: MR imaging of solitary osteochondromas: Report of eight cases. AJR 149:557-560, 1987.

8. Brien EW, Mirra JM, Kerr R: Benign and malignant cartilage tumors of bone and joint: Their anatomic and theoretical basis with an emphasis on radiology, pathology and clinical biology. Skeletal Radiol 26:325-353, 1997.

9. De Beuckeleer LHL, De Schepper AMA, Ramon F: Magnetic resonance imaging of cartilaginous tumors: Is it useful or necessary? Skeletal Radiol 25:137-141, 1996.

10. Geirnaerdt MJA, Bloem JL, Eulderink F, et al: Cartilaginous tumors: Correlation of gadolinium-enhanced MR imaging and histopathologic findings. Radiology 186:813-817, 1993.

11. Mirra JM, Gold R, Downs J, Eckardt JJ: A new histologic approach to the differentiation of enchondroma and chondrosarcoma of the bones. Clin Orthop 201:214-237, 1985.

Dr. Walker and Dr. Moore are Associate Professors in the Department of Radiology at the University of Nebraska Medical Center in Omaha.