SKELETAL METASTASES FROM SOFT-TISSUE SARCOMAS

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1 INCIDENCE, PATTERNS, AND RADIOLOGICAL FEATURES HIDEKI YOSHIKAWA, TAKAFUMI UEDA, SHIGEKI MORI, NOBUHITO ARAKI, SHIGEYUKI KURATSU, ATSUMASA UCHIDA, TAKAHIRO OCHI From Osaka Medical Centre for Cancer and Cardiovascular Diseases and Osaka University Medical School, Osaka, Japan We reviewed 277 patients with soft-tissue sarcoma (STS) treated between 1975 and 1995 to study the incidence, distribution, time of appearance, and radiological findings of skeletal metastases. Of these, 28 (10.1%) had metastases within a mean period of 18.6 months after admission. The incidence of skeletal metastases differed among the histological subtypes of sarcoma; alveolar soft-part sarcoma, dedifferentiated liposarcoma, angiosarcoma, and rhabdomyosarcoma tended to show higher incidences. The regional bones close to the primary tumour were affected in 13 (46.4%) of the 28 patients, and the axial bones in 18 (64.3%). Radiologically, the metastatic bony lesions predominantly showed osteolytic changes, and there were pathological fractures in 21 of 44 lesions. J Bone Joint Surg [Br] 1997;79-B: Received 28 October 1996; Accepted 17 March 1997 Soft-tissue sarcomas (STS) often recur and have distant metastases. They spread via the bloodstream rather than by lymphatics. 1 Lung metastases are most common and most life-threatening and the pattern, surgical treatment and prognosis have been reported. 2,3 Bone, lymph nodes, liver, brain and subcutaneous tissue are involved much less often. 4-8 H. Yoshikawa, MD, Chief of Musculoskeletal Tumour Surgery T. Ueda, MD, Musculoskeletal Tumour Surgeon S. Mori, MD, Musculoskeletal Tumour Surgeon Department of Orthopaedic Surgery, Osaka Medical Centre for Cancer and Cardiovascular Diseases, 1-3-3, Nakamichi, Higashinari-ku, Osaka 537, Japan. N. Araki, MD, Musculoskeletal Tumour Surgeon S. Kuratsu, MD, Musculoskeletal Tumour Surgeon A. Uchida, MD, Chief of Musculoskeletal Tumour Surgery T. Ochi, MD, Professor of Orthopaedic Surgery Department of Orthopaedic Surgery, Osaka University Medical School, 2-2, Yamadaoka, Suita 565, Japan. Correspondence should be sent to Dr H. Yoshikawa British Editorial Society of Bone and Joint Surgery X/97/47372 $2.00 Bony metastases may cause intractable pain, pathological fractures, and paresis if the vertebrae are involved. Because of the increased survival rate of patients with STS it is important to deal with skeletal metastases effectively to improve well-being and quality of life. Knowledge of the clinical features of skeletal metastases in each subtype of STS is essential for their early detection and the management of patients with these lesions. There have been several epidemiological reports of the incidence of skeletal metastases from STS, 4,5,8 but few have described the clinical characteristics and the metastatic pattern in the skeleton. Our aim was to identify the characteristics of skeletal metastases from STS and to correlate the sites of the primary tumour with the bones involved. PATIENTS AND METHODS Between 1975 and 1995 we treated 277 patients with STS. There were 147 males and 130 females with a median age of 42 years (7 to 85). Primary tumours were found in the upper limb in 41 patients, the lower limb in 160, the trunk in 65 and elsewhere in 11. The histological variation is shown in Table I. At admission a full diagnostic examination was performed which included physical examination, radiography, tomography of the chest, and a bone scan followed by radiography of all bones with abnormal scintigraphy. All the patients were seen at least every month for the first year after surgery, at three-monthly intervals up to five years, and six-monthly up to ten years. A full physical examination was performed at each visit with chest radiography. Full lung tomography and bone scans were routinely performed every six months for the first five years of follow-up. Radiographs of specific bones were taken for the diagnosis of skeletal metastases after an abnormal bone scan or because of clinical symptoms such as pain and swelling. Patterns of bony destruction were classified into three groups: geographic, moth-eaten, or permeated. 9 Metastatic sites were divided into three groups in relation to the tumour: ipsilateral bones, contralateral bones, and axial (central) bones, which is similar to the classification used 548 THE JOURNAL OF BONE AND JOINT SURGERY

2 549 Table I. Incidence of skeletal metastases from soft-tissue sarcomas Skeletal metastasis Number of Diagnosis cases Number Percentage Malignant fibrous histiocytoma Liposarcoma 49 (4)* 2 (2)* 4.1 (50)* Synovial sarcoma Malignant schwannoma Rhabdomyosarcoma Leiomyosarcoma Fibrosarcoma Alveolar soft-part sarcoma Clear-cell sarcoma Extraskeletal Ewing's sarcoma Epithelioid sarcoma Angiosarcoma Extraskeletal myxoid chondrosarcoma Mesenchymal chondrosarcoma Unclassified sarcoma Total * parentheses: dedifferentiated liposarcoma Figure 1a Case 18. Radiograph showing a metastatic lesion in the humerus from a synovial sarcoma of the right foot. There is an osteolytic metastasis with pathological fracture of the humerus. Figure 1b Case 19. Radiograph showing an osteolytic metastasis in the left femur from a malignant schwannoma of the left upper arm, with a pathological fracture. Fig. 1a Fig. 1b for renal carcinomas. 10 In addition, bones close to the primary tumour were categorised as regional bones. A metastasis was not diagnosed if there was direct invasion of bone by the primary sarcoma. The median follow-up period for survivors was 76 months (12 to 248) from the date of the first admission to September 25, RESULTS Incidence of skeletal metastases. Of the 277 patients, 28 (10.1%) were diagnosed clinically and radiologically as having a skeletal metastasis; 18 of these had histological confirmation by biopsy or radical surgery. Table I shows the incidence of skeletal metastases from different histological types of STS. Alveolar soft-part sarcoma (55.6%), dedifferentiated liposarcoma (50%), angiosarcoma (50%) and rhabdomyosarcoma (26.7%) tended to show a higher incidence of bony metastases, followed by malignant schwannoma (10.7%), malignant fibrous histiocytoma (8.1%), synovial sarcoma (7.5%) and leiomyosarcoma (7.7%). Two of 14 unclassified sarcomas developed skeletal metastases. During the follow-up period there were no skeletal metastases from liposarcoma (except the dedifferentiated type), fibrosarcoma, clear-cell sarcoma, extraskeletal Ewing s sarcoma, epithelioid sarcoma, extraskeletal myxoid chondrosarcoma or mesenchymal chondrosarcoma. Radiological findings. All 44 bony lesions evaluated by plain radiographs were predominantly osteolytic (Fig. 1); VOL. 79-B, NO. 4, JULY 1997

3 550 H. YOSHIKAWA, T. UEDA, S. MORI, ET AL Table II. Clinical characteristics of 28 patients with skeletal metastases from soft-tissue sarcomas Age Primary Time to skeletal Solitary or Time to lung Case (yr) Gender site Histology* metastases (mth) multiple metastases (mth) 1 48 M R thigh MFH 66 M M L leg MFH 21 M M R leg MFH 4 M M R knee MFH 19 S F R thigh MFH 44 S None 6 71 F R knee MFH 30 S F L thigh ASPS 0 M F R buttock ASPS 0 M M R buttock ASPS 42 S F R thigh ASPS 0 S F L thigh ASPS 20 S F L buttock RMS 10 M F R thigh RMS 8 S M R groin RMS 36 M None F L hand RMS 2 S M R forearm Synovial 36 M M L popliteal Synovial 13 M M R foot Synovial 0 M M L upper arm M schwan 23 S M L groin M schwan 8 M F L leg M schwan 28 M M L thigh Dedif lipo 19 S M R thigh Dedif lipo 4 M F L leg Angiosa 26 S F L leg Angiosa 15 M None F L thigh Unclass 6 M M L thigh Unclass 16 M F L thigh LMS 24 S 24 * MFH, malignant fibrous histiocytoma; ASPS, alveolar soft-part sarcoma; RMS, rhabdomyosarcoma; M schwan, malignant schwannoma; Dedif lipo, dedifferentiated liposarcoma; Angiosa, angiosarcoma; Unclass, unclassified sarcoma; LMS, leiomyosarcoma S, solitary, M, multiple metastases Table III. Relationship between primary and metastatic sites in 28 patients with skeletal metastases Metastatic site Case Primary site Ipsilateral Contralateral Axial (central) 1 R thigh R scapula Th3 2 L leg L femur*, L ilium* L3 3 R leg Th5,6,11,12 4 R knee R ilium* 5 R thigh R femur* 6 R knee L5 7 L thigh L femur (multiple)* 8 R buttock L femur Sacrum 9 R buttock Th12 10 R thigh L femur 11 L thigh L femur* 12 L buttock L femur* Skull, spine (multiple) 13 R thigh L4 14 R groin R femur*, R ilium* L scapula Th3,7,8, skull 15 L hand L3 16 R forearm R humerus*, R rib L tibia, L ilium 17 L popliteal L ilium*, L rib C5,6 18 R foot R tibia*, R humerus* Mandible 19 L upper arm L femur 20 L groin L ilium* C6 21 L leg L humerus Th8, L5 22 L thigh Th6,7 23 R thigh R rib (multiple) L rib (multiple) Skull, C4 24 L leg L scapula 25 L leg L tibia*, L calcaneus*, L talus* 26 L thigh L ilium* C5 27 L thigh Skull (multiple) 28 L thigh L rib * considered as metastasis to regional bone THE JOURNAL OF BONE AND JOINT SURGERY

4 551 (p < 0.01). Of these 19 patients, 13 with ipsilateral metastases were categorised as having metastases to regional bones (Fig. 2), and five of these (cases 4,5,7,11,25) had metastases only to ipsilateral bones without contralateral or axial lesions. Fig. 2 Case 7. MRI of the left thigh with an alveolar softpart sarcoma. The primary tumour is in the anterior thigh (white arrows) and the metastatic lesions are within the distal femur (black arrows). This was categorised as metastasis to regional bone. six were geographic, 20 were moth-eaten, and 18 had a permeative pattern. Sixteen lesions were within the medulla of the bones and 28 showed erosion or destruction of the cortex of the bone. There was little evidence of periosteal reaction such as perpendicular spiculation, Codman s triangle, or onion-skinning. In 21 lesions, there was a pathological fracture (Fig. 1). Patterns of skeletal metastases. Table II summarises the clinical characteristics of the 28 patients with skeletal metastases. This includes four patients (cases 7, 8, 10, 18) with skeletal metastases at admission. The mean interval between admission and skeletal metastasis was 18.6 months (0 to 66). Twelve patients showed a solitary metastasis and 16 had multiple metastases. Isolated bony metastases occurred in three patients (cases 5, 14, 25) (11%). The remaining 25 patients (89%) also had lung metastases. In 14 of these the lung was the first site, followed by bone, but in four patients a skeletal metastasis was detected first, before a lung metastasis. The other seven patients developed metastases almost simultaneously in bone and lung. Table III shows the distribution of bony metastases and the relationship between primary and metastatic sites. Eighteen patients (64%) had axial metastases, including those in the skull. The spine was the most common single site (16/28, 57%). Nineteen patients (68%) developed metastases to ipsilateral bones while only five (18%) had metastases to contralateral bones; this difference is statistically significant DISCUSSION Skeletal metastasis from STS and its clinical implications have received little attention, probably because they spread via the circulation and are therefore considered to represent a terminal stage of the condition. Advances in the management of patients with disseminated tumours have led to increased survival and quality of life, 11 and there have been many improvements in imaging and in the implants used for stabilising pathological fractures. Radical local excision and endoprosthetic replacement are being commonly used for the management of isolated skeletal metastases. 12 The orthopaedic management of patients with skeletal metastases from sarcoma is therefore important even when there is a limited survival period. Analysis of our data indicates that the probability of skeletal metastasis depends on the histological type of the primary sarcoma. Alveolar soft-part sarcoma was most often associated with skeletal metastasis (five of nine, 55.6%). This is a characteristically slow-growing tumour with a long-term survival despite frequent lung and skeletal metastases at the first presentation. 13 The high incidence of skeletal metastases may be partly due to the long duration of the disease before the clinical appearance of the primary tumour. Half of our dedifferentiated liposarcomas developed skeletal metastases, but we saw none in conventional liposarcomas. Liposarcoma may acquire a metastatic attraction to bone as dedifferentiation occurs. The distribution of skeletal metastases varied with histological subtypes, but the spine was the most common site, as noted in other reports. 11 It is generally agreed that the high incidence of vertebral metastases from carcinoma is due to involvement of the paravertebral venous plexus, as proposed by Batson. 14 A similar pattern of haematogenous spread to the spine is also likely from STS. In addition, the high incidence of metastases to the ipsilateral bones, especially to the regional bones, may be considered as a phenomenon equivalent to a skip lesion in an osteosarcoma. 15 This is believed to occur through a plexus of valveless emissary veins with multiple anastomoses around the joints and long bones. 16,17 Sarcoma cells appear to metastasise to the regional bones in this manner. This is similar to the spread of uterine cervical cancer to the pelvis 18 or of renalcell carcinoma to the lumbar spine. 10 Careful examination of the bones close to the primary STS may therefore be useful for the early detection of skeletal metastases. Metastatic lesions from STS showed an exclusively osteolytic destruction with a permeative or moth-eaten pattern. Since these patterns indicate rapid destruction of bone, 9 pain due to pathological fracture, impending fracture VOL. 79-B, NO. 4, JULY 1997

5 552 H. YOSHIKAWA, T. UEDA, S. MORI, ET AL or instability of the spine may rapidly follow seeding to bone. In our series almost half of the metastatic bony lesions produced pathological fractures. Consequently, surgical intervention may be more often required for STS metastases than those with an osteoblastic or mixed pattern such as prostatic or breast carcinomas. We hope that our findings will help the earlier detection of skeletal metastases of STS and the selection of the appropriate orthopaedic management. This study was supported in part by a grant from the Japanese Ministry of Health and Welfare. 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. REFERENCES 1. Enzinger FM, Weiss SW. Soft tissue tumors. 3rd ed. St Louis: Mosby- Year Book Inc, 1995: Putnam JB, Roth JA, Wesley MN, Johnston MR, Rosenberg SA. Analysis of prognostic factors in patients undergoing resection of pulmonary metastases from soft tissue sarcomas. J Thorac Cardiovasc Surg 1984;87: Ueda T, Uchida A, Kodama K, et al. Aggressive pulmonary metastasectomy for soft tissue sarcomas. Cancer 1993;72: Gustafson P. Soft tissue sarcoma: epidemiology and prognosis in 508 patients. Acta Orthop Scand 1994;65: Huth JF, Eilber FR. Patterns of metastatic spread following resection of extremity soft-tisue sarcomas and strategies for treatment. Semin Surg Oncol 1988;4: Potter DA, Glenn J, Kinsella T, et al. Patterns of recurrence in patients with high-grade soft-tissue sarcomas. J Clin Oncol 1985;3: Potter DA, Kinsella T, Glatstein E, et al. High-grade soft tissue sarcomas of the extremities. Cancer 1986;58: Vezeridis MP, Moore R, Karakousis CP. Metastatic patterns in softtissue sarcomas. Arch Surg 1983;118: Mirra JM, ed. Bone tumors: clinical, radiologic and pathologic correlations. Philadelphia: Lea and Febiger, Arkless R. Renal carcinoma: how it metastasizes. Radiology 1964;84: Galasko CSB. Skeletal metastases. London: Butterworths & Co. Ltd, 1986: Harrington KD. Orthopaedic management of extremity and pelvic lesions. Clin Orthop 1995;312: Lieberman PH, Brennan MF, Kimmel M, et al. Alveolar soft-part sarcoma: a clinicopathologic study of half a century. Cancer 1989;63: Batson OV. The vertebral vein system. Am J Roentgenol 1957;78: Enneking WF, Kagan A. The implications of skip metastases in osteosarcoma. Clin Orthop 1975;111: Oni OOA, Stafford H, Gregg PJ. An investigation of the routes of venous drainage from the marrow of the human tibial diaphysis. Clin Orthop 1988;230: Kato F, Bassett FH, Silver D. Arteriography of the nutrient artery and blood flow of the canine tibia. J Bone Joint Surg [Am] 1970;52-A: Ratanatharathorn V, Powers WE, Steverson N, et al. Bone metastasis from cervical cancer. Cancer 1994;73: THE JOURNAL OF BONE AND JOINT SURGERY

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