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MR imaging of dedifferentiated chondrosarcoma
ELSEVIER
MR IMAGING OF DEDIFFERENTIATED CHONDROSARCOMA STEPHEN EUSTACE, MD, NANCY BAKER, MD, HOWARD LAN, MD, ANIL WADHWANI, MD, AND DAVID DORFMAN, MD
MR imaging of a dedifierentiated chondrosarcoma of the humerus is presented and correlated with gross and microscopic histology from the surgical specimen. The classification of chondrosarcoma and specific MR signal characteristics that suggest dedifferentiation are discussed. 0 Elsevier Science Inc., 1997 KEY WORDS:
Dedifferentiated
chondrosarcoma;
MRI;
Histology
INTRODUCTION The role of magnetic resonance imaging in staging primary and secondary tumors of bone is now widely established. In contrast, its potential role in primary bone tumor characterization is limited; plain film radiographs allowing more detailed evaluation of associated cortical destruction, periosteal reaction, and tumor matrix are significantly more valuable in this regard. Accepting that characterization of a cartilage tumor requires review of plain film radiographs, we present a potential exception, dedifferentiated chondrosarcoma, in which MR imaging clearly allows identification of two tumor components and in doing so helps to identify tumor dedifferentiation. CASE REPORT A 64-year-old male patient presented with a &month history of intractable left shoulder pain unrelieved From the Departments of Radiology and Pathology (D.D.), Boston University Medical Center (SE.) and Brigham and Women’s Hospitals (N.B., H.L., A.W.), Boston, Massachusetts. Address reprint requests to: Stephen Eustace, MD, Department of Radiology, Boston University Hospital, 88 East Newton Street, Boston, MA 02215. Received August 20, 1995; accepted September 30, 1995. CLINICAL IMAGING 1997;21:170-174 0 Elsevier Science Inc., 1997 655 Avenue of the Americas, New York, NY 10010
by anti-inflammatory medications. On examination he was noted to have marked swelling of the left upper arm and acute pain on palpation. Magnetic resonance imaging showed an extensive tumor of the proximal shaft of the left humerus with complicating pathological fracture. Signal characteristics suggested the presence of two histological components and hence cartilage tumor dedifferentiation (Figures 1A and 1B). Because of extension of tumor to the shoulder joint space and because of diffuse invasion of adjacent soft tissues, a palliative limb salvage procedure was performed with resection (Figures 2 and 3) and cadaveric grafting of the proximal humerus and associated soft tissue tumor. The resection specimen (Figures 3, 4A, 4B, and 4C) showed two components: centrally histology showed a low-grade cartilage component (Figure 4A), and peripherally histology showed a high-grade sarcomatous component (Figure 4B). A diagnosis of dedifferentiated chondrosarcoma was made.
DISCUSSION Chondrosarcomas represent lo-15% of bone tumors, occurring throughout the skeleton and occasionally within soft tissues, with a predeliction for the femur, humerus, pelvis, scapula, and ribs (l-3). In practice, chondrosarcomas may be divided into conventional and unconventional types. Conventional chondrosarcomas may be primary or secondary (arising in a preexisting cartilagenous lesion). Primary tumors arise more commonly within the medulla (central chondrosarcoma) and less frequently from the surface of bone (peripheral chondrosarcoma). The term nonconventional chondrosarcoma describes variants of the conventional tumor and includes mesenchymal, clear cell, extraskeletal myxoid,
0899-7071/97/$17.00 PI1 SO899-7071(96)00016-2
MAY/JUNE
1997
MR IMAGING OF DEDIFFERENTIATED CHONDROSARCOMA
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FIGURE 1. (A) Sagittal T-l-weighted
(TE-15, TR 500) MR study shows diffuse intramedullary tumor within the proximal shaft of the left humerus with pathological fracture and extension to adjacent soft tissues. Hypointense tumor (chondroid component) within the proximal shaft of the humerus is enveloped by isointense tumor (similar to adjacent soft tissue) (dedifferentiated component] in the metaphysis, in the midshaft, and within the adjacent soft tissues. (B) Coronal STIR (inversion recovery) image shows markedly hyperintense [thick white arrow) central chondroid matrix surrounded by less hyperintense dedifferentiated soft tissue tumor component.
and dedifferentiated forms as in the described case (a-9). The dedifferentiated form comprises approximately 10% of all chondrosarcomas (5). With the exception of primary chondrosarcomas, most chondrosarcomas occur in elderly patients, more commonly males, presenting with pain and swelling as in our own patient (l-3). On the basis of histology, chondrosarcomas are divided into grade 1 tumors, characterized by small nuclei, grade z tumors, characterized by moderate sized nuclei, and grade 3 tumors with larger nuclei, high mitotic rate, and hypercellularity. Grade 1 tumors are more indolent, while grade 3 tumors are aggressive and associated with a particularly poor prognosis (10, 11).
Dahlin and Beabout (12) have defined dedifferentiated chondrosarcoma as a tumor that is composed of a histologically grade 1 chondrosarcoma in association with a contiguous high-grade malignant tumor (such as a fibrosarcoma, osteogenic sarcoma, or malignant fibrous histiocytoma) (13-16). Unlike simple grade 1 chondrosarcomas, prognosis for patients with the dedifferentiated form is extremely poor, presumably reflecting the high-grade soft tissue component, 19 of 21 patients conforming to these criteria dying within 1 year in one study (5). The exact mechanism of tumor dedifferentiation is currently unclear. Dahlin and Beabout suggest that a dedifferentiated chondrosarcoma represents direct transformation of a well-differentiated cartilagenous
172
EUSTACE
CLINICAL IMAGING VOL. 21, NO. 3
ET AL.
tumor into a mesenchymal high-grade lesion (12). Tetu et al. suggest that dedifferentiated chondrosarcoma is derived from two separate clones of cells each with the ability to differentiate into separate lines with different histological characteristics and different levels of maturation (17). In contrast Sanerkin and Woods have suggested that dedifferentiation represents transformation within the dense fibrotic tissue reaction at the margin of the cartilage component and that the cartilage component remains uninvolved in the dedifferentation (18). Capanna et al. (5) in a review of 46 patients with chondrosarcoma identified two forms of dedifferentiated tumor, the first arising out of a low-grade tumor conforming to the classic criteria of Dahlin and
FIGURE 3. Corresponding surgical specimen, in concordance with MR image, shows two cellular patterns. Focal chondroid tumor centrally (white arrows) is surrounded by more densely cellular tumor proximally, distally, and within adjacent soft tissues.
FIGURE 2. Anteroposterior radiograph shows a pathological fracture through a permeative destructive lesion of the proximal shaft of the humerus with associated soft tissue mass.
Beabout, and the second arising out of a high-grade cartilagenous lesion. On radiographs, the former did not expand or destroy cortex (Figure l), while the latter enlarged and distorted the parent bone. As in our own case, classic group 1 lesions were often complicated by pathological fracture (Figures 4A and 4B). In either type, two patterns of dedifferentiation were observed. In one, dedifferentiation was focal and limited, and in the second, the dedifferentiation was diffuse and circumferential, encasing and destroying the original cartilagenous tumor. In the reported case, MR imaging clearly demonstrated the presence of two histological components with differing tion
of the
signal patterns. tumor,
gested the presence
Within
MR signal of c&age,
the central
por-
characteristics sughypointense on T-l
MAY/JUNE
1997
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173
and markedly hyperintense on T-Zweighted imaging. Peripherally, signal characteristics suggested soft tissue abnormality, isointense to muscle on T-l, hyperintense on T-z-weighted imaging yet less hyperintense than the adjacent markedly hyperintense cartilage (Figures 3A and 3B). Pathological fracture, lack of bone expansion, and two clearly defined histological components conform to the classic description of a type 1 dedifferentiated chondrosarcoma (12). Circumferential encasement of the cartilage component by soft tissue sarcoma conforms to the second pattern of dedifferentiation described by Capanna et al. (5). In summary, we present and review MR appearances and histopathology of a patient with a type 1 dedifferentiated chondrosarcoma and emphasize characteristic signal patterns at magnetic resonance imaging that suggest the diagnosis prior to surgical resection.
REFERENCES 1. Dahlin DC, Unni KK. Chondrasarcoma (primary, secondary,
dedifferentiated and clear cell). In Dahlin DC, Unni K (eds):
Bone Tumors: ed. Springfield:
General Aspects Thomas, 1986,
and Data on 8542 pp. 227-259.
cases,
4th
2. Schajowicz
F. Cartilage forming tumors. In Schajowicz F. (ed): Tumors and Tumorlike Lesions of Bone and Joints. New York: Springer-Verlag. 1981. pp. 160-204.
3. Mirra JM. Intramedullary cartilage and chondroid producing tumors. In Mirra JM (ed): Bone Tumors: Clinical, Radiologic. and Pathologic Correlations. Philadelphia: Lea & Febiger. 1989, pp. 439-690. 4. Varma DGK, Ayala AG. Carrasco CH. Edeiken J. Chondrosarcoma: MR imaging relation. Radiographics X992:12:687-704.
Guo SQ. Kumar R, with pathologic cor-
5. Capanna R, Bertoni F, Bettelli G. Picci P, Bacchini P, Present D, Giunti A, Campanacci M. Dedifferentiated chondrosarcoma. J Bone Joint Surg 1988;7OA:69-79. 6. Nakashima Y, Unni KK, Shives TC, Swee Mesenchymal chondrosarcoma of bone and view of 111 cases. Cancer 1986;57:2444-2453.
RG, Dahlin DC. soft tissue: a re-
7. Bjornssen J, Beabout JW. Unni K. Sim FH. Dahlin DC. Clear cell chondrosarcoma of bone: observations in 47 cases. Am J Surg Path01 1984:8:223-230. FM, Shiraki MS. Extraskeletal myxoid chondrosar8 Enzinger coma, an analysis of 34 cases. Hum Pathol 1972:3:421-435. 9 Campannaci drosarcomas.
FIGURE 4. (A) Histology from central tumor shows abundant cartilage cells with low-grade mitotic activity. (B) Histology from peripheral tumor component shows densely packed fibrous tissue containing abundant mitoses typical of a high-grade soft tissue sarcoma. (C) Histology shows abrupt transition from one histological type to the other. Soft tissue sarcomatous element (left), low-grade chondrosarcomatous element (right).
10
M. Bertoni F, Capanna R. Dedifferentiated Italian J Orthop Traumat 1979;5:331-341.
chon-
Evans HL. Ayala AG. Romsdahl MM. Prognostic factors in chondrosarcoma of bone: a clinicopathologic analysis with emphasis on histologic grading. Cancer 1977;40:818-831.
DJ, Lunke RJ. Taylor WF, Dahlin DC, Medley BE. 11 Pritchard Chondrosarcoma: a clinicopathologic and statistical analysis. Cancer 1980;45:149-157. 12 Dahlin DC, Beabout JW. Dedifferentiation drosarcomas. Cancer 1971:28:461-466.
of low grade
13
Jaworski RC. Dedifferentiated chondrosarcoma, tural study. Cancer 1984;53:2674-2678.
14
Johnson
S, Tetu
B, Ayala
AG. Chawla
chon-
an ultrastruc-
SP. Chondrosarcoma
174
EUSTACE
ET AL.
with additional mesenchymal component (dedifferentiated chondrosarcoma): a clinicopathologic study of 26 cases. Cancer 1986;58:278-286. 15. Kahn LB. Chondrosarcoma with dedifferentiated foci: a comparative and ultrastructural study. Cancer 1976;37:1365-1375. 16. McCarthy EF, Dorfman HD. Chondrosarcoma of bone with dedifferentiation: a study of 18 cases. Hum Pathol 1982;13:36-40.
CLINICAL IMAGING VOL. 21. NO. 3
17. Tetu B, Ordonez NG, Ayala AG, MacKay B. Chondrosarcoma with additional mesenchymal component (dedifferentiated chondrosarcoma): an immunohistochemical and electron microscopic study. Cancer 1986;58:287-298. 18. Sanerkin NG, Woods CG. Fibrosarcomata and malignant fibrous histiocytomata arising in relation to enchondromata. J Bone Joint Surg 1979;61B:366-372.
MR IMAGING OF DEDIFFERENTIATED CHONDROSARCOMA STEPHEN EUSTACE, MD, NANCY BAKER, MD, HOWARD LAN, MD, ANIL WADHWANI, MD, AND DAVID DORFMAN, MD
MR imaging of a dedifierentiated chondrosarcoma of the humerus is presented and correlated with gross and microscopic histology from the surgical specimen. The classification of chondrosarcoma and specific MR signal characteristics that suggest dedifferentiation are discussed. 0 Elsevier Science Inc., 1997 KEY WORDS:
Dedifferentiated
chondrosarcoma;
MRI;
Histology
INTRODUCTION The role of magnetic resonance imaging in staging primary and secondary tumors of bone is now widely established. In contrast, its potential role in primary bone tumor characterization is limited; plain film radiographs allowing more detailed evaluation of associated cortical destruction, periosteal reaction, and tumor matrix are significantly more valuable in this regard. Accepting that characterization of a cartilage tumor requires review of plain film radiographs, we present a potential exception, dedifferentiated chondrosarcoma, in which MR imaging clearly allows identification of two tumor components and in doing so helps to identify tumor dedifferentiation. CASE REPORT A 64-year-old male patient presented with a &month history of intractable left shoulder pain unrelieved From the Departments of Radiology and Pathology (D.D.), Boston University Medical Center (SE.) and Brigham and Women’s Hospitals (N.B., H.L., A.W.), Boston, Massachusetts. Address reprint requests to: Stephen Eustace, MD, Department of Radiology, Boston University Hospital, 88 East Newton Street, Boston, MA 02215. Received August 20, 1995; accepted September 30, 1995. CLINICAL IMAGING 1997;21:170-174 0 Elsevier Science Inc., 1997 655 Avenue of the Americas, New York, NY 10010
by anti-inflammatory medications. On examination he was noted to have marked swelling of the left upper arm and acute pain on palpation. Magnetic resonance imaging showed an extensive tumor of the proximal shaft of the left humerus with complicating pathological fracture. Signal characteristics suggested the presence of two histological components and hence cartilage tumor dedifferentiation (Figures 1A and 1B). Because of extension of tumor to the shoulder joint space and because of diffuse invasion of adjacent soft tissues, a palliative limb salvage procedure was performed with resection (Figures 2 and 3) and cadaveric grafting of the proximal humerus and associated soft tissue tumor. The resection specimen (Figures 3, 4A, 4B, and 4C) showed two components: centrally histology showed a low-grade cartilage component (Figure 4A), and peripherally histology showed a high-grade sarcomatous component (Figure 4B). A diagnosis of dedifferentiated chondrosarcoma was made.
DISCUSSION Chondrosarcomas represent lo-15% of bone tumors, occurring throughout the skeleton and occasionally within soft tissues, with a predeliction for the femur, humerus, pelvis, scapula, and ribs (l-3). In practice, chondrosarcomas may be divided into conventional and unconventional types. Conventional chondrosarcomas may be primary or secondary (arising in a preexisting cartilagenous lesion). Primary tumors arise more commonly within the medulla (central chondrosarcoma) and less frequently from the surface of bone (peripheral chondrosarcoma). The term nonconventional chondrosarcoma describes variants of the conventional tumor and includes mesenchymal, clear cell, extraskeletal myxoid,
0899-7071/97/$17.00 PI1 SO899-7071(96)00016-2
MAY/JUNE
1997
MR IMAGING OF DEDIFFERENTIATED CHONDROSARCOMA
171
FIGURE 1. (A) Sagittal T-l-weighted
(TE-15, TR 500) MR study shows diffuse intramedullary tumor within the proximal shaft of the left humerus with pathological fracture and extension to adjacent soft tissues. Hypointense tumor (chondroid component) within the proximal shaft of the humerus is enveloped by isointense tumor (similar to adjacent soft tissue) (dedifferentiated component] in the metaphysis, in the midshaft, and within the adjacent soft tissues. (B) Coronal STIR (inversion recovery) image shows markedly hyperintense [thick white arrow) central chondroid matrix surrounded by less hyperintense dedifferentiated soft tissue tumor component.
and dedifferentiated forms as in the described case (a-9). The dedifferentiated form comprises approximately 10% of all chondrosarcomas (5). With the exception of primary chondrosarcomas, most chondrosarcomas occur in elderly patients, more commonly males, presenting with pain and swelling as in our own patient (l-3). On the basis of histology, chondrosarcomas are divided into grade 1 tumors, characterized by small nuclei, grade z tumors, characterized by moderate sized nuclei, and grade 3 tumors with larger nuclei, high mitotic rate, and hypercellularity. Grade 1 tumors are more indolent, while grade 3 tumors are aggressive and associated with a particularly poor prognosis (10, 11).
Dahlin and Beabout (12) have defined dedifferentiated chondrosarcoma as a tumor that is composed of a histologically grade 1 chondrosarcoma in association with a contiguous high-grade malignant tumor (such as a fibrosarcoma, osteogenic sarcoma, or malignant fibrous histiocytoma) (13-16). Unlike simple grade 1 chondrosarcomas, prognosis for patients with the dedifferentiated form is extremely poor, presumably reflecting the high-grade soft tissue component, 19 of 21 patients conforming to these criteria dying within 1 year in one study (5). The exact mechanism of tumor dedifferentiation is currently unclear. Dahlin and Beabout suggest that a dedifferentiated chondrosarcoma represents direct transformation of a well-differentiated cartilagenous
172
EUSTACE
CLINICAL IMAGING VOL. 21, NO. 3
ET AL.
tumor into a mesenchymal high-grade lesion (12). Tetu et al. suggest that dedifferentiated chondrosarcoma is derived from two separate clones of cells each with the ability to differentiate into separate lines with different histological characteristics and different levels of maturation (17). In contrast Sanerkin and Woods have suggested that dedifferentiation represents transformation within the dense fibrotic tissue reaction at the margin of the cartilage component and that the cartilage component remains uninvolved in the dedifferentation (18). Capanna et al. (5) in a review of 46 patients with chondrosarcoma identified two forms of dedifferentiated tumor, the first arising out of a low-grade tumor conforming to the classic criteria of Dahlin and
FIGURE 3. Corresponding surgical specimen, in concordance with MR image, shows two cellular patterns. Focal chondroid tumor centrally (white arrows) is surrounded by more densely cellular tumor proximally, distally, and within adjacent soft tissues.
FIGURE 2. Anteroposterior radiograph shows a pathological fracture through a permeative destructive lesion of the proximal shaft of the humerus with associated soft tissue mass.
Beabout, and the second arising out of a high-grade cartilagenous lesion. On radiographs, the former did not expand or destroy cortex (Figure l), while the latter enlarged and distorted the parent bone. As in our own case, classic group 1 lesions were often complicated by pathological fracture (Figures 4A and 4B). In either type, two patterns of dedifferentiation were observed. In one, dedifferentiation was focal and limited, and in the second, the dedifferentiation was diffuse and circumferential, encasing and destroying the original cartilagenous tumor. In the reported case, MR imaging clearly demonstrated the presence of two histological components with differing tion
of the
signal patterns. tumor,
gested the presence
Within
MR signal of c&age,
the central
por-
characteristics sughypointense on T-l
MAY/JUNE
1997
MR IMAGING OF DEDIFFERENTIATED CHONDROSARCOMA
173
and markedly hyperintense on T-Zweighted imaging. Peripherally, signal characteristics suggested soft tissue abnormality, isointense to muscle on T-l, hyperintense on T-z-weighted imaging yet less hyperintense than the adjacent markedly hyperintense cartilage (Figures 3A and 3B). Pathological fracture, lack of bone expansion, and two clearly defined histological components conform to the classic description of a type 1 dedifferentiated chondrosarcoma (12). Circumferential encasement of the cartilage component by soft tissue sarcoma conforms to the second pattern of dedifferentiation described by Capanna et al. (5). In summary, we present and review MR appearances and histopathology of a patient with a type 1 dedifferentiated chondrosarcoma and emphasize characteristic signal patterns at magnetic resonance imaging that suggest the diagnosis prior to surgical resection.
REFERENCES 1. Dahlin DC, Unni KK. Chondrasarcoma (primary, secondary,
dedifferentiated and clear cell). In Dahlin DC, Unni K (eds):
Bone Tumors: ed. Springfield:
General Aspects Thomas, 1986,
and Data on 8542 pp. 227-259.
cases,
4th
2. Schajowicz
F. Cartilage forming tumors. In Schajowicz F. (ed): Tumors and Tumorlike Lesions of Bone and Joints. New York: Springer-Verlag. 1981. pp. 160-204.
3. Mirra JM. Intramedullary cartilage and chondroid producing tumors. In Mirra JM (ed): Bone Tumors: Clinical, Radiologic. and Pathologic Correlations. Philadelphia: Lea & Febiger. 1989, pp. 439-690. 4. Varma DGK, Ayala AG. Carrasco CH. Edeiken J. Chondrosarcoma: MR imaging relation. Radiographics X992:12:687-704.
Guo SQ. Kumar R, with pathologic cor-
5. Capanna R, Bertoni F, Bettelli G. Picci P, Bacchini P, Present D, Giunti A, Campanacci M. Dedifferentiated chondrosarcoma. J Bone Joint Surg 1988;7OA:69-79. 6. Nakashima Y, Unni KK, Shives TC, Swee Mesenchymal chondrosarcoma of bone and view of 111 cases. Cancer 1986;57:2444-2453.
RG, Dahlin DC. soft tissue: a re-
7. Bjornssen J, Beabout JW. Unni K. Sim FH. Dahlin DC. Clear cell chondrosarcoma of bone: observations in 47 cases. Am J Surg Path01 1984:8:223-230. FM, Shiraki MS. Extraskeletal myxoid chondrosar8 Enzinger coma, an analysis of 34 cases. Hum Pathol 1972:3:421-435. 9 Campannaci drosarcomas.
FIGURE 4. (A) Histology from central tumor shows abundant cartilage cells with low-grade mitotic activity. (B) Histology from peripheral tumor component shows densely packed fibrous tissue containing abundant mitoses typical of a high-grade soft tissue sarcoma. (C) Histology shows abrupt transition from one histological type to the other. Soft tissue sarcomatous element (left), low-grade chondrosarcomatous element (right).
10
M. Bertoni F, Capanna R. Dedifferentiated Italian J Orthop Traumat 1979;5:331-341.
chon-
Evans HL. Ayala AG. Romsdahl MM. Prognostic factors in chondrosarcoma of bone: a clinicopathologic analysis with emphasis on histologic grading. Cancer 1977;40:818-831.
DJ, Lunke RJ. Taylor WF, Dahlin DC, Medley BE. 11 Pritchard Chondrosarcoma: a clinicopathologic and statistical analysis. Cancer 1980;45:149-157. 12 Dahlin DC, Beabout JW. Dedifferentiation drosarcomas. Cancer 1971:28:461-466.
of low grade
13
Jaworski RC. Dedifferentiated chondrosarcoma, tural study. Cancer 1984;53:2674-2678.
14
Johnson
S, Tetu
B, Ayala
AG. Chawla
chon-
an ultrastruc-
SP. Chondrosarcoma
174
EUSTACE
ET AL.
with additional mesenchymal component (dedifferentiated chondrosarcoma): a clinicopathologic study of 26 cases. Cancer 1986;58:278-286. 15. Kahn LB. Chondrosarcoma with dedifferentiated foci: a comparative and ultrastructural study. Cancer 1976;37:1365-1375. 16. McCarthy EF, Dorfman HD. Chondrosarcoma of bone with dedifferentiation: a study of 18 cases. Hum Pathol 1982;13:36-40.
CLINICAL IMAGING VOL. 21. NO. 3
17. Tetu B, Ordonez NG, Ayala AG, MacKay B. Chondrosarcoma with additional mesenchymal component (dedifferentiated chondrosarcoma): an immunohistochemical and electron microscopic study. Cancer 1986;58:287-298. 18. Sanerkin NG, Woods CG. Fibrosarcomata and malignant fibrous histiocytomata arising in relation to enchondromata. J Bone Joint Surg 1979;61B:366-372.