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The Journal of Bone and Joint Surgery 78:141-9 (1996)
© 1996 The Journal of Bone and Joint Surgery, Inc.

Instructional Course Lecture

Instructional Course Lectures, The American Academy of Orthopaedic Surgeons - Chondrosarcoma: a Review*{dagger}

DEMPSEY S. SPRINGFIELD, M.D.{ddagger}, MARK C. GEBHARDT, M.D.{ddagger}, BOSTON, MASSACHUSETTS and MICHAEL H. MCGUIRE, M.D.§, OMAHA, NEBRASKA

An Instructional Course Lecture, The American Academy of Orthopaedic Surgeons


   Introduction
Top
 Introduction
References
 
Chondrosarcoma is a malignant tumor of cartilage-producing cells35. It is subdivided in a variety of ways, including by histological grade, by whether it is primary or secondary, and by whether it is peripheral or central; among these, the single most prognostic sub-classification is the histological grade. In addition, there are a few specific histological subtypes of chondrosarcoma: clear-cell, mesenchymal, base of the skull, and soft-parts chondrosarcoma.

Chondrosarcoma is most often separated into three histological grades: low (grade 1), medium (grade 2), and high (grade 3). The higher the grade, the more likely it is that the tumor will metastasize. Grading is based on the tumor's histological appearance, with tumors that most resemble normal cartilage being low-grade (grade 1) and having the least risk of metastasizing, and those that have the most abnormal-appearing cartilage being high-grade (grade 3) and having a higher risk of metastasizing (Figs. 1 and 2). A type of chondrosarcoma that has a higher risk of metastasizing than a grade-3 chondrosarcoma is the uncommon, so-called dedifferentiated chondrosarcoma7,24. This chondrosarcoma is believed to arise from a benign cartilage lesion or a low-grade chondrosarcoma. On histological examination, it has areas of malignant spindle cells that cannot be recognized as being of cartilaginous origin, adjacent to areas of neoplastic chondrocytes surrounded by a hyaline-cartilage matrix. The dedifferentiated chondrosarcoma is the most malignant of the chondrosarcomas and has an extremely high risk of distant metastasis. A review of the experience at the Mayo Clinic with dedifferentiated chondrosarcoma found that only eight of seventy-eight patients who had such a lesion survived for more than five years after the initial diagnosis12. This finding is consistent with the four and five-year survival rates reported in other studies3,8.



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  		Photomicrograph of a low-grade chondrosarcoma. The most important finding suggestive of the malignant nature of this lesion is how the cartilage tumor has surrounded pre-existing trabeculae of bone. Benign cartilage tumors such as enchondroma will not do this. The cellularity of the lesion is not markedly greater than that of an active enchondroma (x 10).

 


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  		Photomicrograph of a high-grade chondrosarcoma. As in Fig. 1, the cartilage tumor has surrounded normal trabeculae. The lesion is clearly producing a cartilage matrix but has markedly increased cellularity and enlarged nuclei, both typical of high-grade chondrosarcoma. Dedifferentiated chondrosarcoma (not shown) also has areas of malignant spindle cells without cartilage matrix production (x 10).

 
There is also a group of cartilage tumors that are best thought of as premalignant, or borderline, chondrosarcomas4. A lesion of this type that arises within the medullary canal will be more cellular than a typical enchondroma and may have slight cellular atypia. Such a lesion is called an atypical enchondroma by some pathologists and a so-called grade-1/2 chondrosarcoma by others. A premalignant cartilage lesion that arises from the surface of the bone may either be large, arising from the periosteum (periosteal chondroma), with atypical cartilage cells but no frankly malignant changes, or, more commonly in an adult, it may be an osteocartilaginous exostosis with an enlarging cartilaginous cap that is thicker than one centimeter. The histological features of the chondrocytes in the thick cartilaginous cap are benign, but it is thought that an osteocartilaginous exostosis should not enlarge in an adult (after the age of thirty years) and that growth indicates excessive biological activity. A premalignant lesion has no measurable risk of metastasizing, but its clinical behavior is locally aggressive, and it has a risk of progressing into a definitive chondrosarcoma with metastatic potential13.

The clinical behavior of these borderline cartilage lesions is the most important factor in deciding how they should be treated clinically, and it is important for the surgeon to ascertain this activity before a biopsy is done. The pathologist should also rely on this clinical information in determining how best to classify the tumor. The best means of determining a specific lesion's activity is by careful clinical observation. For example, if an adult has a painful intramedullary cartilage lesion that has enlarged and caused endosteal erosion, most pathologists will classify it as at least a grade-1/2 or even as a grade-1 chondrosarcoma, even if not all of the histological criteria of malignancy are present. On the other hand, if the patient has some radiographic findings but no symptoms and the lesion has not increased in size, even if there is minimum endosteal erosion the pathologist will not call the lesion a chondrosarcoma unless it meets all of the histological criteria for a malignant cartilage tumor. Before doing a biopsy of a suspected lesion, one should be sure that its clinical activity is known.

Chondrosarcoma is also subdivided into primary and secondary types. Primary chondrosarcomas arise de novo and are not associated with a pre-existing lesion. Secondary chondrosarcomas, on the other hand, arise from a pre-existing benign cartilage lesion, which could be an enchondroma, an osteocartilaginous exostosis (Figs. 3-A, 3-B, and 3-C), a chondromyxofibroma, a synovial chondromatosis, a periosteal chondroma, or even a chondroblastoma. Only patients with multiple heritable osteocartilaginous exostoses or with multiple enchondromas (Ollier disease) have a recognized risk for the development of secondary chondrosarcoma, and the precise prevalence of secondary chondrosarcoma in patients who have either of these two disorders is not known. The total number of patients with either multiple osteocartilaginous exostoses or multiple enchondromas is unknown, so the denominator needed in the ratio to determine the prevalence is unavailable. The prevalence of malignant degeneration in patients with multiple enchondromas has been the subject of analysis; Schwartz et al. reported that the prevalence of secondary chondrosarcoma in patients who have Ollier disease is about 25 per cent at the age of forty years, as estimated from life-table analysis of thirty-seven patients34. Of greater concern was their finding, also noted by others, that patients with Maffucci disease (multiple enchondromas and hemangiomas) have a 100 per cent risk of development of a malignant tumor (sarcoma or carcinoma) during their lifetime, as determined by life-table analysis, even though only four of the seven patients in the series reported by Schwartz et al. had such a lesion at the time of their evaluation20,34.



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  		Figs. 3-A, 3-B, and 3-C: A secondary chondrosarcoma from an osteocartilaginous exostosis in a thirty-five-year-old patient. The patient had noticed the mass for years, but it had enlarged recently. Fig. 3-A: Lateral radiograph. The large cartilaginous cap cannot be seen.

 


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  		Fig. 3-B: Sagittal proton-density magnetic resonance image. The cartilaginous cap can be seen as an intermediate-intensity signal mass extending from the ossified portion of the osteocartilaginous exostosis and displacing the biceps femoris (repetition time, x 1800; echo time, x 20).

 


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  		Fig. 3-C: Sagittal T2-weighted magnetic resonance image. The cartilaginous cap is now a bright signal mass, which is typical of cartilage on T2-weighted images (repetition time, x 1800; echo time, x 80).

 
Secondary chondrosarcomas arising from an osteocartilaginous exostosis have a better prognosis than other chondrosarcomas, and they rarely metastasize27. In fact, the only metastases from chondrosarcomas arising from a solitary osteocartilaginous exostosis have been from those with a high histological grade or a dedifferentiated component13. An enlarging osteocartilaginous exostosis in an adult should be resected, not because of its metastatic potential but because of its local effect and its small risk of developing into a dedifferentiated chondrosarcoma33. The resection should be complete, and the cartilaginous cap should not be violated during the resection because cutting into the cap will increase the risk of local recurrence35.

Another way to subdivide chondrosarcomas is by their location in or on the bone (central or peripheral)35. Central chondrosarcomas arise from within the medullary canal, and peripheral chondrosarcomas arise from the surface of the bone. For all practical purposes, only secondary chondrosarcomas need to be subdivided into central or peripheral; primary chondrosarcomas are virtually always central. The majority of peripheral chondrosarcomas are secondary to an osteocartilaginous exostosis, and central chondrosarcomas that are secondary almost always arise from an enchondroma. The treatment and prognosis of central secondary chondrosarcomas are identical to those of primary chondrosarcomas.

As mentioned earlier, there are a few additional specific histological subtypes of chondrosarcoma. They are uncommon and include clear-cell chondrosarcoma, mesenchymal chondrosarcoma, chondrosarcoma of the soft parts, and chondrosarcoma of the base of the skull.

Clear-cell chondrosarcoma, originally reported by Unni et al. in 1976, is thought to be the malignant counterpart of a benign chondroblastoma36. Clear-cell chondrosarcomas are most common in the proximal part of the humerus and the proximal part of the femur, involve the epiphyseal center of ossification and the metaphysis, and are found most often in young adults who are twenty to fifty years old. They are usually low-grade and are treated with operative resection with a wide margin.

Mesenchymal chondrosarcoma, originally described in 1959 by Lichtenstein and Bernstein23, is even less common than clear-cell chondrosarcoma. It most commonly arises in the bone but has also been reported in the soft tissues6. It is composed of nodules of benign-appearing cartilage within a background of undifferentiated small round cells. The undifferentiated small round-cell component often has the histological appearance of a hemangiopericytoma. In a review of 111 patients with mesenchymal chondrosarcoma, Nakashima et al. reported that the five-year survival rate after wide resection was 60 per cent and the ten-year survival rate was 25 per cent29. In this group of patients, fifty-seven of whom were female and who ranged in age from four to seventy-four years, the ribs, spine, pelvis, and femur were the most common osseous sites. Mesenchymal chondrosarcoma is treated with a wide operative resection.

Chondrosarcoma can occur in the soft tissues, and when it does it is called a soft-parts chondrosarcoma5,9,32. It is treated like other soft-tissue sarcomas. It is a rare tumor, and little is known about its natural history.

Chondrosarcoma may arise at the base of the skull11,28. This lesion is treated with curettage and irradiation because of the anatomical limitations of operative resection. The patient presents with neurological deficits, and orthopaedists are rarely involved in the treatment. The lesion may be confused with chordoma of the clivus, as there is overlap in the presentation, radiographic appearance, histological characteristics, and treatment.

Combination of the data from Dahlin6 and Campanacci2 for typical, primary, central chondrosarcoma provides an indication of the demographics of the tumor (Fig. 4). There were 763 patients in their combined series; 463 patients (61 per cent) were male, and 300 (39 per cent) were female. Thirty-two patients (4 per cent) were less than twenty years old, and 355 (47 per cent) were between forty and seventy years old. Almost every bone has been reported to have had at least one chondrosarcoma, but the most common sites are the pelvis (24 per cent) and the proximal part of the femur (16 per cent)2,6. The other common sites are the ribs, the distal part of the femur, the proximal part of the humerus, the proximal part of the tibia, and the scapula.



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  		The age and sex of the patients and the anatomical distribution of the chondrosarcomas, on the basis of the data of Dahlin6 and Campanacci2.

 
The most common clinical presentation of a chondrosarcoma is in a man between fifty-five and seventy years old who is in otherwise excellent health but who has pain in the hip or buttock. The patient usually has had the pain for three months or more, and often a limp has recently developed. The pain is progressive but not debilitating. It may interfere with sleep, and it is not relieved with rest. It is not uncommon for the patient to seek the advice of a sports-medicine orthopaedist, as these patients often notice that their tennis or golf game is suffering. The patient with a pelvic or proximal femoral chondrosarcoma may complain of pain in the distal part of the thigh or the knee, and, as is the case with children complaining of knee pain, it is important to remember that pelvic and hip lesions can present with such distal symptoms.

During the physical examination, abnormalities are usually noted, but the findings are subtle. The patient will have a mildly antalgic gait. The range of motion of the adjacent joint or joints may be reduced slightly. There is usually mild atrophy of the affected extremity. The remainder of the physical examination is normal.

The laboratory findings for patients with chondrosarcoma should be normal. Occasionally there will be an increase in the erythrocyte sedimentation rate, but the remainder of the serum and urine values are normal.

The radiographic findings depend on the type of chondrosarcoma, but a primary, central chondrosarcoma can usually be recognized by its typical appearance on a plain radiograph. The lesion usually arises in the metaphysis, although it can arise in the diaphysis of a long bone. There is a combination of bone destruction, often with small intralesional calcifications, and a periosteal reaction. The cortex is rarely completely destroyed but is irregularly thinned, and there is a circumferential periosteal reaction (Fig. 5). The intralesional calcifications are best seen on a computed tomography scan. A dedifferentiated chondrosarcoma has a more aggressive radiographic appearance, indicating its rapid growth rate and destructive capabilities, and often there is an extraosseous component (Figs. 6-A, 6-B, and 6-C).



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  		Anteroposterior radiograph showing a chondrosarcoma of the humeral shaft. Marked cortical destruction has taken place over an extended period of time, with a reasonably well developed periosteal reaction that seems to contain the lesion. There is calcification within the lesion suggestive of the cartilage matrix. The appearance of the lesion is most consistent with a medium or high-grade chondrosarcoma.

 


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  		Figs. 6-A, 6-B, and 6-C: A dedifferentiated chondrosarcoma of the distal part of the femur. Fig. 6-A: Radiograph showing that the lesion is mostly intramedullary and extensive; however, there is an extraosseous component, suggested by the periosteal reaction of the posterior cortex.

 


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  		Computed tomography scan showing cortical destruction, extraosseous extension posteriorly, and reactive bone. There is also a mass anterior to the femur without calcification. This pattern suggests an aggressive lesion typical of a dedifferentiated chondrosarcoma.

 


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  		Sagittal T2-weighted magnetic resonance image. The intramedullary extension is best seen as the bright signal, which is typical of cartilage. The extraosseous extension is seen on other sections (repetition time, x 2000; echo time, x 120).

 
In many ways, the presentation of a patient with a chondrosarcoma is similar to that of a patient with a metastatic carcinoma (Fig. 7). Unfortunately, the diagnosis of chondrosarcoma may not be considered, and as a result, the patient's care may be compromised. This is a trap to be avoided. Certainly, metastatic carcinoma occurs more frequently than does chondrosarcoma, and most older patients presenting with a destructive bone lesion will have a metastatic lesion. If a patient has a history of myeloma or a carcinoma, especially in the lung, breast, thyroid, kidney, or prostate, and presents with a destructive, radiolucent lesion of bone, the lesion is unlikely to be a chondrosarcoma; however, if the patient has no history of a carcinoma and the physical examination, chest radiograph, renal ultrasonogram, and laboratory findings (prostate-specific antigen, serum, and urine immunoelectrophoresis) are normal, it is wise to plan for the possibility that the lesion is a chondrosarcoma.



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  		Anteroposterior radiograph of the proximal part of the left femur of a sixty-two-year old man who had had pain in the groin for six months. He had recently had a repair of a left inguinal hernia. There is a radiolucent lesion in the intertrochanteric region, with mild reaction just distal to it. The lesion could have been metastatic; however, the patient was otherwise healthy, and an incisional biopsy proved the tumor to be a dedifferentiated chondrosarcoma with a component that was consistent with a high-grade spindle-cell sarcoma. The patient was managed with a resection of the proximal part of the femur.

 
In the majority of patients, a biopsy is necessary only to confirm what is clinically an obvious diagnosis. In this setting, a needle biopsy will provide adequate material for a specific diagnosis. Even the grade of the tumor can usually be determined with the limited tissue made available to the pathologist by this method. When the diagnosis is not obvious clinically, we recommend an open biopsy. It is often difficult to make the distinction between a benign cartilage tumor and a low-grade chondrosarcoma. An open biopsy provides the advantage of obtaining sufficient material to lessen the risk of a missed diagnosis. When an open, incisional biopsy is done, the surgeon must consider the possibility that a subsequent resection will be necessary and that the biopsy incision and all tissue exposed during the biopsy will need to be resected. Therefore, the biopsy must be planned carefully so as not to make a subsequent resection more difficult or impossible.

Some cartilaginous lesions are best treated with excisional biopsy, including those that have a clinical presentation suggesting it will be difficult for the pathologist to distinguish a benign from a malignant cartilage lesion and those for which wide-resection excisional biopsy is not associated with considerably more morbidity than a curettage. In an excisional biopsy, the surgeon must be sure that the resected lesion is completely surrounded by normal tissue. Small lesions, especially those on the surface of the bone, and those in expendable bones such as a rib or a fibula, are best suited for excisional biopsy. This technique gives the pathologist the entire specimen from which to make a diagnosis and is adequate treatment for benign aggressive cartilage lesions as well as low-grade malignant ones. Many of these small lesions cannot be definitively classified histologically, and it is very comforting for the patient and surgeon to know that they have been totally excised.

When a biopsy is done, the pathologist should always obtain a frozen section even if immediate definitive treatment is not planned. This ensures that an adequate amount of tissue has been obtained and that the material is representative and will be diagnostic.

Resection is the treatment of choice for all chondrosarcomas (Fig. 8). We prefer to do the resection in conjunction with the incisional biopsy. The biopsy is first interpreted by the pathologist, and the suspected diagnosis of chondrosarcoma is confirmed. The biopsy wound is then closed, clean drapes are applied, the surgeon and assistants change their gowns and gloves, and the resection is done with use of clean instruments. This approach reduces the risk of creating a postoperative hematoma that will spread tumor cells beyond the tissues immediately adjacent to the biopsy track. In this way, less normal tissue must be removed. For resection, a wide operative margin is suggested, as it will provide an acceptably low prevalence of local recurrence. Magnetic resonance imaging will provide the most accurate picture of the extent of a chondrosarcoma and is recommended as the examination of choice when a resection is planned (Fig. 6-C). In general, chondrosarcoma does not infiltrate the surrounding extraosseous tissues, and by resecting the involved bone and a small cuff of the muscles that originate from the involved bone an adequate margin is obtained. For some lesions, a wide operative margin can be obtained only with an amputation, but usually an adequate resection that preserves the limb can be done.



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  		Photograph of a typical low-grade chondrosarcoma of the proximal part of the humerus. The most distal white material is polymethylmethacrylate from the plug put in at the time of the biopsy. The lesion, which appears white and shiny, has permeated throughout the metaphysis and has begun to erode the lateral endosteal surface approximately halfway down the specimen. The patient was managed successfully with a wide resection of the proximal part of the humerus.

 
Irradiation can be of use in the treatment of chondrosarcoma, but only in exceptional situations15,21,22. Such a situation most commonly occurs when the primary tumor arises in the spine. Obtaining a wide operative margin of a chondrosarcoma arising in the spine is rarely, if ever, technically possible. Fortunately, the spine is an uncommon location for chondrosarcoma. After a so-called marginal resection, irradiation eliminates, or at least delays, local recurrence, but probably only in patients who have minimum residual microscopic disease15,25. Although high-dose irradiation (more than sixty gray) will arrest the growth of a chondrosarcoma for a few years, irradiation should be used only to control macroscopic disease when operative resection is not possible.

Chemotherapy plays a minimum role in the management of patients with chondrosarcoma10. In young, healthy patients (those less than sixty years old) with a dedifferentiated chondrosarcoma, adjuvant chemotherapy may be of benefit, but there are few data to support its use10,18,26,30,37. In patients who have metastatic disease, chemotherapy may slow the growth of the lesion, but cure is extremely rare.

The survival of patients who have chondrosarcoma should be determined at ten years rather than at the more common interval of five years. Although most local recurrences or pulmonary metastases occur within the first five years after the initial presentation, chondrosarcoma has a higher prevalence of recurrence, local and distant, after five years than do most sarcomas. Almost all distant metastases will be to the lungs.

The prognosis of patients with chondrosarcoma depends on the histological grade and the adequacy of the resection. Younger patients seem to have a worse prognosis1,19. Patients with a low-grade (grade-1) chondrosarcoma that has been completely resected are almost always cured of the disease16,38. Patients with a low-grade chondrosarcoma and an inadequate resection in whom a local recurrence develops will have decreased rates of survival17. Without a complete resection, the patient will almost surely die of the chondrosarcoma, regardless of the grade.

The survival rate for patients with a medium-grade (grade-2) or high-grade (grade-3) chondrosarcoma is not easily determined because of the long time required for follow-up after the initial treatment. Reports from the Rizzoli Institute14 in Bologna and from the Mayo Clinic32 showed that, while more than 80 per cent (106 of 130) of patients with a low-grade (grade-1) chondrosarcoma survived for ten years, only 31 per cent (eleven of thirty-six) of those with a high-grade (grade-3) tumor survived for ten years.

Chondrosarcoma of bone is a primary malignant tumor that should be treated with a definitive, complete, wide resection without spillage of tumor if local control is to be achieved. Patients with a low-grade (grade-1) chondrosarcoma who are managed in this manner should expect to be cured, but those with higher-grade lesions are at risk for metastasis. An operative resection that is incomplete leaves the patient with a high risk of local failure and eventual death. Adjuvant chemotherapy and irradiation rarely play a role in the treatment of chondrosarcoma of bone.


   Footnotes
 
*Printed with permission of The American Academy of Orthopaedic Surgeons. This article will appear in Instructional Course Lectures, Volume 45, The American Academy of Orthopaedic Surgeons, Rosemont, Illinois, March 1996.

{dagger}No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article.

{ddagger}Massachusetts General Hospital, 32 Fruit Street, GRB 606, Boston, Massachusetts 02114.

§Creighton University School of Medicine, 601 North 30th Street, Omaha, Nebraska 68131.


   References
Top
 Introduction
 References
 

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