Skeletal Radiol (1991) 20:279 283
Transarticular invasion of joints by bone tumors: hypothesis Ibrahim Fikry Abdelwahab, M.D. 1, Theodore T. Miller, M.D. 1, George Hermann, M.D. 1, Michael J. Klein, M.D. 2, Samuel Kenan, M.D. 3, and Michael M. Lewis, M.D. 3 Departments of i Radiology, 2 Pathology, and 3 Orthopedic Surgery, Mount Sinai Medical Center, City University of New York, New York, USA
Abstract. Eight bone tumors with associated transarticular invasion of the sacroiliac joints are described. All invaded the true synovial joint and spread to the opposing bone. One tumor was benign, and the other seven were malignant. Five of the seven were primary and two were metastatic cancer. One, a myeloma, invaded the disc spaces between the fourth and fifth lumbar vertebrae and the fifth lumbar vertebra and sacrum as well as the sacroiliac joint. The right facet joints o f the two vertebrae were also invaded. After a thorough search of the literature, we find that the sacroiliac joint is the most c o m m o n joint to be invaded by tumors. This is followed by the vertebral disc spaces and, last, the facet joints. Apart from these joints, we were unable to find any radiographic documentation of other joints being transarticularly invaded by tumors. We noted that there is a direct relation between transarticular tumor spread and joints that lack mobility and that certain tumors, benign and malignant, tend to invade these joints.
Key words: Tumors of bone - Joint invasion - Computed tomography
Magnetic resonance imaging
It is a c o m m o n belief that skeletal tumors involving the end of a long bone, a vertebra, or a flat bone stop short at the articular margin or disc space and do not cross the cartilage space. Anecdotal wisdom holds that the joint space acts as a barrier to the spread of t u m o r ; this is, in fact, a commonly taught rule for differentiating tumors from infectious-inflammatory processes. We present eight cases in which tumors invaded joints, together with a review of the literature.
Materials and methods
destruction limited to one articular margin was not included because this finding is not uncommon in tumors involving the end of a bone. We reviewed our series of approximately 2000 malignant and 500 benign tumors involving the entire skeleton and found eight cases of transarticular joint invasion. These patients were referred to our orthopedic tumor service, a tertiary care referral center, from 1978 to the present. Three patients were men, and the other five were women, ranging in age from 24 to 68 years. Plain films and computed tomography (CT) examinations were performed in all cases, and bone scans were obtained in four. Magnetic resonance imaging (MRI) was performed in two patients. All eight patients underwent open biopsy, and a histopathologic diagnosis was obtained. The clinical information, joint involvement, and histologic diagnoses are summarized in Table 1 and illustrated in Figs. 1-5.
Results All results are presented as follows: Case 1. Currettage of the aneurysmal bone cyst. Case 2. The fibrosarcoma was very large and involved the spinal canal. Patient was referred to the oncology service for possible chemotherapeutic treatment. Case 3. Anterior and posterior exploration of the sacrum was done in two stages with curettage and local excision of the chondrosarcoma. Case 4. As the chondrosarcoma compressed the sciatic nerve, en bloc resection of the neoplasm was performed. Case 5. The patient with the dedifferentiated chondrosarcoma refused surgery. Case 6. Radiation therapy was performed for the multiple myeloma with marked relief of the low back pain.
We defined the transarticular invasion of a joint as involvement of the opposing bones of the joint associated with destruction of the intervening cartilage space. According to this criterion, bone
Case 7. The hepatocellular carcinoma with subsequent development of pulmonary, thoracic, and sacroiliac metastases was treated with chemotherapy.
Address reprint requests to: I. Fikry Abdelwahab, M.D., Box 1234, Department of Radiology, Mount Sinai Medical Center, One Gustare L. Levy Place, New York, NY 10029-6574, USA
Case 8. Chemotherapy was the treatment empioyed for the adenocarcinoma of the lung that metastasized to the right sacroiliac region. 9 1991 International Skeletal Society
I.F. Abdelwahab et al. : Transarticular invasion
Table 1. Patient characteristics and clinical information
Transarticular joint invasion
Plain films, bone scan, CT, MRI
Right SIJ (Fig. 1)
Aneurysmal bone cyst
Plain films, CT
Left SIJ (Figs. 2, 3)
Plain films, bone scan, CT
Right SIJ (Fig. 4)
Plain films, CT
Plain films, CT
Plain films, CT
Right SIJ, right facet joints, and disc spaces of the fourth and fifth lumbar vertebrae (Fig. 5)
Plain films, CT, MRI
Metastatic bone disease from hepatocellular carcinoma
l-year history of intermittent back pain with occasional radiation of pain down the right leg 2-year history of pain and discomfort in left buttock and thigh 1-year history of low back pain and radiculopathy down the right leg 6-month history of right-sided sciatica 2-year history of left-sided sciatica Several years of low back pain with recent exacerbation in the preceding 3 months Liver transplant for hepatocellular carcinoma. Follow-up CT scan 1 year later revealed metastatic disease of the lungs, thoracic spine, and pelvis 6-month history of lower back and right buttock pain
Plain films, bone scan, CT
Metastatic bone disease from adenocarcinoma of the right lung
A l t h o u g h we searched the literature to the best o f our ability, we did n o t find any evidence that the topic o f radiographically demonstrable joint space invasion by bone t u m o r had ever been directly addressed. O u r search, therefore, included large reviews o f b o t h benign and malignant b o n e t u m o r s and occasional relevant case reports. Since it is n o t possible to investigate every article, there m a y be instances o f transarticular invasion that were missed. In addition, m a n y articles, a l t h o u g h mentioning joint space invasion,'did n o t provide e n o u g h illustrations or description to prove their point and were
therefore n o t included in our discussion. Conversely, several authors did n o t discuss joint space invasion by tumor, yet some o f their illustrations vividly d e m o n strated this process. The sacroiliac joint is f o r m e d by the o p p o s i n g surfaces o f the sacrum and ilium. These surfaces are irregular and allow interdigitation o f the two bones. This interlocking o f the joint contributes to its strength and m a r k edly restricts its motion. A thick layer o f hyaline cartilage covers the articular surface o f the sacrum, whereas a thinner layer o f fibrous cartilage covers the articular surface o f the ilium. The joint has a complete fibrous capsule a n d is lined by a synovial membrane. Only the
I.F. Abdelwahab et al. : Transarticular invasion
Fig. 1. Case 1. CT scan of the pelvis and sacrum showing an expanding lucent lesion invading the right sacroiliac joint and involving the opposing sides of the sacroiliac joint Fig. 2. Case 2. Anteroposterior view of the left side of the pelvis demonstrating a lucent lesion involving the major part of the left iliac bone and crossing the left sacroiliac joint to involve the left side of sacrum Fig. 3. Case 2. CT scan of the pelvis revealing a lesion in the left iliac bone that expands and permeates the major part of the bone. The tumor involves the adjacent sacrum with destruction of the left sacroiliac joint Fig. 4. Case 3. CT scan of the pelvis demonstrating the destructive lesion, with heavily calcified matrix, invading the right sacroiliac joint Fig. 5. Case 6. CT scan of the pelvis revealing the destruction of the right iliac bone and sacrum with sacroiliac joint invasion. Note the huge, intrapelvic, soft-tissue mass lower one-half to two-thirds of the space between the sacrum and ilium represents the true synovial joint. The superior aspect of the space is ligamentous and is not part of the synovial joint . Pelvic tumors that invade the sacroiliac joint m a y arise primarily in the iliac bone or sacrum. Occasionally, the exact bony origin of the t u m o r can be difficult to determine, especially when the t u m o r is equally large on both sides of the joint. CT and M R I now permit evaluation of t u m o r size and extent as well as the presence of a soft-tissue component, if any, and involvement of the joint space. C h o r d o m a is the m o s t c o m m o n primary malignant t u m o r of the sacrum, and the sacrum is the m o s t comm o n site of chordoma. Approximately 50% of chordomas in adults are located in the sacrum . C h o r d o m a can markedly expand the sacrum and destroy both its anterior and posterior margins. However, of 77 cases of c h o r d o m a of the sacrum in one series, only one invaded the sacroiliac joint (0.8%) [8, 12, 20, 22]. In contrast, vertebral chordomas, which constitute only 15% of chordomas, much more frequently invade
the intervertebral disc space. In three series of vertebral chordomas [8, 17, 23] totalling 35 cases, nine intervertebral disc spaces were invaded (26%). The spaces were narrowed, and the opposing articular margins were partially or completely destroyed. Anatomically, the intervertebral disc space has m a r k e d similarity to the sacroiliac joint. The annulus fibrosus surrounds the nucleus pulposus and is firmly attached to the vertebral endplates. It is attached to the periphery of the vertebral bodies by Sharpey's fibers which extend from the annulus fibrosus through the vertebral trabeculae to blend with the periosteum and longitudinal ligaments. Therefore, the intervertebral disc space is also a fixed tight joint that lacks mobility . Giant cell t u m o r is the second most c o m m o n primary t u m o r of the sacrum and the most c o m m o n benign one. A review of 38 cases occurring in the sacrum and throughout the body revealed invasion of the sacroiliac joint in eight cases ( 2 / % ) [14, 20, 21]. Although Levine described two cases of knee invasion and one case of ankle invasion by giant cell tumors, his cases did not meet our criteria for radiographic invasion of joints .
282 In two separate reports, Dahlin and Henderson reviewed 500 cases of chondrosarcoma throughout the body and did not mention any joint involvement [7, 11]. However, their reports were pathologically rather than radiographically oriented, and their reviews predated the advent of CT. In a more recent study, Buirski et al. reported 20 cases of chondrosarcoma of the pelvis, none of which involved the sacroiliac joint . We did find three instances of sacroiliac joint invasion by chondrosarcoma [10, 20, 25], and three of the eight tumors in our series were chondrosarcomas. In case 3, the bulk of the tumor was in the sacrum. In cases 4 and 5 the tumor arose in the iliac bone and spread to the sacrum by invading the sacroiliac joint. Interestingly, the dedifferentiated component of case 5, which was chondrogenic osteogenic sarcoma, was located chiefly in the sacrum. In a series of 11 chondrosarcomas of the sternum , 1 tumor involved the entire manubrium but did not cross the sternoclavicular joint. The sternoclavicular joint consists of a flat circular cartilaginous disc between the articular surfaces of the clavicle and sternum. The disc separates the joint into two articular cavities. Although the sternoclavicular joint appears tight, it differs from both the sacroiliac joint and the intervertebral disc space in that it is freely mobile and participates actively in the movement of the upper extremity . Two series (198 cases) of aneurysmal bone cysts throughout the body showed no evidence of joint invasion [3, 15]. We did find two isolated cases of aneurysmal bone cyst invading the sacroiliac joint [5, 16]. In 6 of 15 cases of aneurysmal bone cyst of the vertebrae, Tillman et al.  found that the lesion affected at least two adjacent vertebrae. This finding prompted them to state that involvement of adjacent vertebrae was a useful radiographic feature distinguishing aneurysmal bone cyst from other spinal tumors. Despite the high percentage of vertebral extension in this series, it cannot be determined from their report whether the tumor invaded the intervertebral disc space. It is not mentioned directly, nor did they provide enough radiographic illustrations to evaluate this point. Intervertebral disc space invasion cannot be taken for granted in their series because it is a well-known fact that aneurysmal bone cyst can involve the posterior elements of multiple adjacent vertebrae by direct extension without intervertebral disc space involvement. Although myeloma is a common primary tumor of bone in the elderly, joint invasion was not present in a combined group of 50 patients studied by CT and MRI [9, 19]. In two large series of myeloma, totalling 959 patients, there was no mention of joint involvement in the radiographic description [6, 13]. However, one of these studies predates the advent of CT and the other is clinicopathologically oriented. In our case, the myeloma not only crossed the intervertebral disc space and the sacroiliac joint, it also invaded the right facet joints at two vertebral levels. The facet joint is similar to the sacroiliac joint and the intervertebral disc space in that it is a tight synovial joint with restricted mobility. Among 13 cases of benign giant intraosseous schwannoma of the sacrum, at least three tumors invaded the
I.F. Abdelwahab et al. : Transarticular invasion Table 2. Review of transarticular invasion of joints by tumors SIJ Giant cell tumor Chondrosarcoma Metastasis Aneurysmal bone cyst Schwannoma Malignant fibrous histiocytoma Fibrosarcoma Chordoma Multiple myeloma Ewing's tumor Osteogenic sarcoma
8 6 (3) 6 (2) 3 (1) 3 1 1 (1) 1 1 (1) 1 1 32
References [14, 20, 21] [10, 20, 25] [10, 201 [5, 161  
[8, 17, 20, 231
9 1 (a)
[201  10
In parentheses are the cases we added from our series SIJ, sacroiliac joint; IDS, intervertebral disc space; F J, facet joint
sacroiliac joint, and one invaded both joints . In addition to our two cases of metastatic carcinoma of the liver and lung, we found four other instances of metastatic disease (two salivary gland tumors and two adenocarcinomas, one of the kidney and the other of the colon) [10, 20]. Scattered cases of malignant fibrous histiocytoma , Ewing's sarcoma , and osteogenic sarcoma  have also been reported. Combining our eight cases with those in the literature, we found 32 instances of invasion of the sacroiliac joint, 10 of the intervertebral disc space, and I of the facet joint, totalling 43 tumors, both malignant and benign (Table 2). The most common tumors that invaded the sacroiliac joint were giant cell tumors, chondrosarcomas, and metastatic disease. Chordomas were the most common tumors to cross the intervertebral disc space, and myeloma was the only tumor that invaded the facet joint. Some of the malignant tumors were slow growing, whereas some of the benign tumors were aggressive. Chordoma and chondrosarcoma are examples of the former; aneurysmal bone cyst and some giant cell tumors represent the latter. Other benign tumors, like giant sacral schwannomas were very slow growing. The incidence of transarticular invasion was high among certain tumors, exceeding 20% for giant cell tumors of the pelvis and chordomas of the spine. We also observed that the sacroiliac joint, intervertebral disc space, and facet joint, which lack free mobility, are the ones most commonly invaded by tumors; we were unable to find transarticular invasion of any freely mobile joint by a bone tumor. Therefore, we conclude that transarticular invasion of a joint by a tumor is directly related to the mobility of the joint and that the sacroiliac joint is the one most commonly invaded, followed by the intervertebral disc spaces, and, last, the facet joints. Why some tumors, whether benign or malignant, tend to invade these joints and why the same tumor (chordo-
I.F. Abdelwahab et al. : Transarticular invasion ma) acts differently w h e n i n v a d i n g the sacroiliac j o i n t a n d the i n t e r v e r t e b r a l disc space are still u n k n o w n .
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