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Synovial Sarcoma: A Multivariate Analysis of Prognostic Factors in 112 Patients With Primary Localized Tumors of the Extremity

From the Departments of Surgery, Biostatistics, and Pathology, Memorial Sloan-Kettering Cancer Center, New York, NY.

Address reprint requests to Jonathan J. Lewis, MD, PhD, Memorial Sloan-Kettering Cancer Center, Department of Surgery, 1275 York Ave, New York, NY 10021; email lewisj{at}mkcc.org

	ABSTRACT

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION REFERENCES

 
PURPOSE: Synovial sarcoma is a high-grade tumor that is associated with poor prognosis. Previous studies analyzing prognostic factors are limited because of inclusion of heterogeneous cohorts of patients with nonextremity and recurrent tumors. The objective of this study was to determine independent prognostic factors of primary synovial sarcoma localized to the extremity.

PATIENTS AND METHODS: Between July 1, 1982, and June 30, 1996, 112 patients underwent surgical resection for cure at our institution and then were followed-up prospectively. Clinical and pathologic factors examined for prognostic value included age, sex, tumor site and location, depth, size, microscopic status of surgical margins, invasion of bone or neurovascular structures, and monophasic or biphasic histology. The end points analyzed were the time to first local recurrence that was not preceded by a distant recurrence, time to any distant recurrence, and time to disease-related mortality. These end points were modeled using the method of Kaplan and Meier and analyzed by the log-rank test and Cox regression.

RESULTS: The median duration of follow-up among survivors in this cohort of 112 patients was 72 months. The 5-year local-recurrence, distant-recurrence, and mortality rates were 12%, 39%, and 25%, respectively. Tumor size 5 cm (P = .001; relative risk [RR] = 2.7; 95% confidence interval [CI], 1.5 to 5.2) and the presence of bone or neurovascular invasion (P = .04; RR = 2.3; 95% CI, 1.0 to 5.3) were independent adverse predictors of distant recurrence. Tumor size 5 cm (P = .003; RR = 2.3; 95% CI, 1.4 to 6.3) and the presence of bone or neurovascular invasion (P = .03; RR = 2.7; 95% CI, 1.0 to 6.5) were also independent adverse predictors of mortality.

CONCLUSION: The natural history of primary synovial sarcoma of the extremity is related to tumor size and invasion of bone and neurovascular structures.

	INTRODUCTION

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SYNOVIAL SARCOMA is a soft tissue sarcoma that has been the subject of much controversy. Despite numerous case reports and several relatively large series, debate still exists about (1) the cell type represented by the tumor, (2) the actual biologic behavior, (3) whether adolescents with synovial sarcoma have more favorable biologic behavior, (4) prognostic factors for this disease, (5) and whether adjuvant chemotherapy is useful in treating patients.

Considering that synovial sarcoma comprises only approximately 13% to 17% of the mere 6,000 cases of soft tissue sarcomas per year in the United States,¹ it is not surprising that this disease is poorly understood. Few studies have included more than 100 patients with synovial sarcomas. Definitive conclusions from even larger studies have been difficult to make because of inclusion of a heterogeneous group of patients with varying histologic subtypes, truncal and extremity locations, locally recurrent tumors, synchronous metastases, and specimens with inadequate surgical resections.

More recently, specific genetic alterations (t(X;18) (p11.2;q11.2)) and fusion transcripts that are unique to synovial sarcoma^2,3 have been identified, and pathologic criteria for the diagnosis of synovial sarcoma have been defined. Refinements in the oncologic techniques have also been important in standardizing care of these patients and have enabled the natural history of this disease to be better understood.⁴

The aim of our study was to determine independent prognostic factors that govern the natural history of this disease. We performed univariate and multivariate analyses of clinical and pathologic factors in a homogenous cohort of 112 patients with localized primary extremity synovial sarcoma. These patients all underwent surgical resection with curative intent at Memorial Sloan-Kettering Cancer Center (MSKCC) and were then followed-up prospectively.

	PATIENTS AND METHODS

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Between July 1, 1982, and June 30, 1996, 126 patients with primary extremity synovial sarcoma were surgically treated and prospectively followed-up by the Department of Surgery at MSKCC. Of these 126 tumors, three were locally recurrent. The histologic results in all 126 cases were rereviewed by two pathologists (C.R.A. and J.M.W.). The diagnosis was confirmed either by a typical histologic examination (in most biphasic synovial sarcomas) or in conjunction with immunohistochemical techniques (in all monophasic synovial sarcomas). Immunohistochemical studies for epithelial differentiation, including epithelial membrane antigens and keratins (CAM5.2 and AE1:AE3) were performed in all 78 cases of synovial sarcomas without clear-cut biphasic histologic/glandular differentiation (100%) and in 14 of 34 biphasic synovial sarcomas (41%). The biphasic tumors were positive for all three epithelial markers. Fifty-eight out of 78 cases without glandular differentiation showed immunoreactivity for at least one epithelial marker. The synovial sarcoma diagnosis in the remaining 20 cases with negative immunohistochemistry was confirmed by reverse transcriptase polymerase chain reaction detection of SYT-SSX fusion transcript (n = 10), electron microscopy (n = 5), and an additional battery of immunostains (n = 20). These 20 cases were determined to be completely negative for S-100 protein and muscle markers (smooth muscle actin, common muscle actin), to rule out other high-grade spindle cell sarcomas, such as malignant peripheral sheath tumor or leiomyosarcoma. The ultrastructural studies did not show any evidence of fibroblastic differentiation of the tumor cells, excluding the possibility of a high-grade fibrosarcoma diagnosis. Eleven of the original 126 tumors were different types of tumors and were excluded, leaving 112 localized primary synovial sarcomas for analysis.

The following patient, tumor, and pathologic factors were examined for prognostic importance for times to local recurrence without previous distant metastases, any distant recurrence, and disease-specific mortality: (1) patient age and sex, (2) tumor depth and anatomic site (upper- v lower-extremity and proximal v distal), and (3) tumor size, microscopic status of surgical margins, invasion of a bone or neurovascular structures, and monophasic or biphasic histologic appearance.

All patients were treated with either limb-sparing resection or amputation. Adjuvant chemotherapy and/or radiotherapy were given based on evaluation of prognostic factors or as part of clinical trials. Thus any treatment difference observed may not reflect true difference in effectiveness, and including them could lead to a misleading conclusion. Therefore treatment factors, such as the type of operation, adjuvant chemotherapy, and adjuvant radiation, were recorded but not analyzed.

The following definitions were used.⁵ A tumor was considered to be a localized primary malignancy if it was previously untreated or a biopsy had been performed at the time of presentation and if there was no evidence of metastasis. Locally recurrent disease was defined as tumor recurrence at a site previously ( 3 months) resected for synovial sarcoma. The depth of tumor was evaluated relative to the investing muscle fascia, with tumors characterized as superficial or deep. A tumor was classified as upper-extremity site if it was at or beyond the shoulder joint and lower-extremity site if it was in the groin or leg. Truncal tumors were excluded from this analysis. Distal location of the lower- and upper-extremity tumors was defined as below the knee and below the elbow joint, respectively. Tumor size was defined as the maximum dimension at pathologic analysis. Tumors were defined as small (< 5 cm) and large ( 5 cm). A tumor was considered as invading bone or a neurovascular structure if there was either gross or microscopic involvement by tumor at operation or subsequent pathologic examination. Bone invasion was defined as invasion of tumor through periosteum and breaching cortex. Neurovascular invasion was defined as invasion into the perineurium of a nerve or through the intima of large veins or arteries. The tumors were divided into two histologic subtypes, biphasic and monophasic, based on the presence or absence of glandular differentiation. Using a two-grade system, all tumors were classified as high-grade sarcomas. Although the existence of lower-grade tumors is still debatable, we consider synovial sarcoma as a fully malignant sarcoma, based not only on histologic grounds (increased cellularity, mitotic activity, and so on), but also on biologic behavior, with a high incidence of distant pulmonary metastases.⁶ Adjuvant irradiation or chemotherapy was defined as treatment within 3 months of the first operation and before a recurrence.

Statistical Analysis
The end points analyzed were time to the first local recurrence that was not preceded by a distant recurrence, time to any distant recurrence, and time to disease-related mortality. The choice of studying only local recurrences without any prior distant recurrence was based on the fact that once distant recurrence occurs, the prognosis becomes significantly worse. Therefore local recurrences preceded by distant metastases are of less interest and importance than those that appeared as the first sign of disease progression. On the other hand, because distant recurrence is the only precursor to tumor-related deaths in extremity soft tissue sarcomas, any distant recurrence is of interest. All time intervals were calculated from the time of initial surgery at MSKCC. In two cases, the times of surgery were missing and were replaced by the times of admission. Deaths that were confirmed to be caused by the disease were treated as an end point for disease-specific mortality; others were censored. All time-to-event end points were modeled using the method of Kaplan and Meier⁷ and analyzed by the log-rank test. Significant factors by log-rank test (P < .30) were analyzed for independent prognostic importance by the Cox proportional hazards regression⁸ using a stepwise procedure. For local recurrence, Cox regression was not performed, because there were only 11 observed events. The proportional hazards model requires any factor in the model to have at least one event observed in every level of the factor. As a result, tumor depth, which had no observed death and only one distant recurrence in the superficial group, was omitted in the Cox regression analyses. In the Cox regression analyses, any observation with missing information on any one of the factors in the final Cox model was omitted from the analysis. This left 109 patients in the Cox regression analyses of distant recurrence and survival. The results of the Cox model analysis are reported with relative risks (RRs) and 95% confidence intervals (CIs). Because of the modest size of this cohort, no interactive effects were studied.

	RESULTS

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Follow-Up and Clinical and Pathologic Characteristics of the Patients
The median follow-up among survivors in this cohort of 112 patients with synovial sarcoma was 72 months, with a range of 1 to 181 months (Table 1). The median age of patients was 35 years, with a range of 16 to 70 years. There were 59 female and 53 male patients. Most patients (n = 87; 78%) underwent resection by limb-sparing procedures. Surgical margins were microscopically positive in 15 cases. Fifty-two patients received adjuvant irradiation. Brachytherapy was administered to 32 patients, external-beam irradiation was used to treat 14 patients, and combined external-beam irradiation and brachytherapy were administered to six patients. Forty-two patients received adjuvant chemotherapy, with regimens consisting of single-agent doxorubicin for 25 patients and multiagent chemotherapy for 17 patients. The most common chemotherapeutic agents used in patients receiving multiagent drug regimens were doxorubicin (n = 12), dacarbazine (n = 8), cyclophosphamide (n = 7), and ifosfamide (n = 7).

Local Recurrence
The actuarial 5-year local recurrence rate was 12% (Table 2). By univariate analysis, the only significant adverse factor was proximal site (P = .005).

View larger version (12K): [in this window] [in a new window]   Fig 1. Distant recurrence rate based on no risk factors (n = 54), one risk factor (either tumor size 5 cm or bone/neurovascular invasion [n = 52]), or two risk factors (tumor size 5 cm and bone/neurovascular invasion [n = 6]). P = .0002.

View larger version (12K): [in this window] [in a new window]   Fig 2. Tumor-related mortality based on no risk factors (n = 54; 5-year tumor-related mortality rate, 14%), one risk factor (either tumor size 5 cm or bone/neurovascular invasion [n = 52; 5-year tumor-related mortality rate, 34%]), or two risk factors (tumor size 5 cm and bone/neurovascular invasion [n = 6; 5-year tumor-related mortality rate, 60%]). P = .0009.

	DISCUSSION

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION REFERENCES

 
Meaningful clinical evaluation of synovial sarcomas began in 1942, with Haagenson and Stout.⁹ In an extensive review of 104 cases of synovial sarcoma, they established pathologic criteria for this disease and reported that only three of 104 patients survived for 5 years. They also found that most tumors were unassociated with synovial tissues and required a biphasic histologic appearance (spindle and epithelioid cells) for the diagnosis. Pack and Ariel¹⁰ from Memorial Hospital reported in 1950 on 60 patients with synovial sarcoma who, despite a high incidence of pulmonary metastases (65%), had a 24% overall 5-year survival rate after resection. The authors demonstrated that both surgical technique and adjuvant radiation were significant factors for improvement in survival. Simple excision, which was associated with a 63% local recurrence rate in their series, was subsequently abandoned.

During the last 40 years, there have been many studies to determine prognostic factors in this disease. Anatomic site,¹¹ tumor size,^4,12-17 patient age,^4,10,12,14 microscopic margins,¹⁷ and histologic subtype (monophasic v biphasic)^11,18 have all been reported to be significant determinants of outcome for patients with synovial sarcoma. Most of these studies were difficult to evaluate for a variety of reasons. Some studies included patients who underwent noncurative surgery by simple excision or biopsy^{4,10,15-17,19} or included unfavorable tumor types, such as epithelioid and clear-cell sarcomas,^10,11,13 which are not forms of synovial sarcoma. Although recurrent and metastatic synovial sarcomas^13,14,20 have a worse prognosis than primary and localized tumors, many studies included these patients.^13,15,17 In addition, few studies evaluated the significance of various prognostic factors in a multivariate fashion,¹³ and it is unclear whether any studies were prospective in design.

Our study consisted of a consecutive series of patients who underwent surgical resection with curative intent at a single institution and were then prospectively followed-up. Patients who presented with recurrent or metastatic tumors were excluded from analysis.

Although patient age has been commonly noted as a significant variable affecting outcome, we were unable to show any statistical differences between patients 25 years of age or younger and those older than 25 years in recurrence or survival. We also attempted to model age in its original, continuous scale and used a four-category system (< 20 years, 20 to 30 years, 30 to 40 years, and > 40 years). Although we have shown that older patients have a higher propensity of developing distant recurrence and risk of dying of disease, this was not statistically significant in the Cox model (P = .13, 0.07, respectively, for distant recurrence and disease-specific survival). Similarly, age was not a factor that predicted local recurrence. Younger patients with synovial sarcoma have been reported to have better survival; however, there is no biologic rationale for this observation. Synovial sarcomas appear the same histologically, independent of age. Reported differences in survival based on age are probably the result of differences in other factors in these age groups, which cannot be determined because none of these were multivariate analyses.

A recent analysis of a selected cohort of patients³ has suggested that the SYT-SSX gene fusion product affects prognosis. The present sequential series was completed before this study, and the fusion product analysis was available for only a minority of these patients. The significance of the fusion product awaits elucidation and confirmation.

In contrast to early historical series^10,19 that reported exceedingly high local-recurrence rates, only 11 (10%) in our series experienced local recurrence as a first recurrence, and 16 (15%) overall had experienced local recurrence at last follow-up. This improvement in local control may be related in part to improved surgical techniques. In these previous series, a large percentage of patients underwent simple tumor excision, and local-recurrence rates ranged from 50% to 60%. In addition, the use of adjuvant irradiation may account for our improved results, because approximately 50% of patients were irradiated. Patients with synovial sarcoma with positive microscopic margins or upper-extremity lesions had higher local-recurrence rates. Previous studies documented the significance of a positive microscopic margin in patients with extremity sarcomas.^5,17,21

Distant metastasis is a major clinical challenge. Overall, 39% of the patients in our series developed distant metastasis as first recurrence and 25% died of their disease. By multivariate analysis, we determined that tumor size greater than 5 cm and tumor invasion of bone, nerve, or vascular structures are independent adverse prognostic factors for development of metastasis and tumor-related mortality. These two adverse prognostic factors were associated with 29 of 43 distant metastases and with 22 of 31 tumor-related deaths. Large tumor size, as previously noted, has been implicated as an adverse prognostic variable in patients with synovial sarcoma as well as in those with soft tissue sarcoma in general.⁵ From our study, tumor invasion of bone and/or neurovascular structures has emerged as a significant prognostic factor for patients with extremity sarcoma of this histologic subtype. One study of children with synovial sarcoma with both localized and metastatic disease at presentation also suggested the prognostic significance of tumor invasion of contiguous structures.¹⁶

Although local control of high-grade extremity sarcomas has improved with the use of adjuvant radiation,^22,23 this benefit has not translated into a survival advantage. Patients continue to develop distant metastases despite "curative" surgical resections and adjuvant radiation, indicating the need for effective systemic therapy. In patients with synovial sarcoma, multiple studies have examined the benefit of systemic therapy. In one study, high-dose ifosfamide was associated with a 100% response of metastases in 13 patients, with four patients having a complete response.²⁴ Although synovial sarcoma has been shown to be sensitive to chemotherapy, studies have not conclusively shown a survival benefit. In one study that examined the efficacy of adjuvant chemotherapy, 93% of patients were free of disease at a median follow-up of 37 months.²⁵ These encouraging results must be viewed as preliminary, because more than one third of these patients had favorable tumors (< 5 cm). Similarly, two German studies of multiagent chemotherapy for children with synovial sarcoma suggested an improvement in survival compared with a historic series of patients undergoing radical surgery alone.^15,26 These studies are difficult to evaluate because the efficacy of chemotherapy was not stratified by tumor size and they were performed in a nonrandomized setting. In addition, patients with recurrent and metastatic disease at presentation were included in these trials. In a recent retrospective review of patients with synovial sarcoma, a response to chemotherapy was observed; however, this did not translate into a survival benefit.¹⁷

In our series, 42 patients (37%) were treated with adjuvant chemotherapy in a nonrandomized fashion. There is no evidence of a survival benefit for adjuvant chemotherapy in the current series. Patients receiving multiagent regimens also had disease-free survival similar to that of patients receiving doxorubicin alone or no adjuvant chemotherapy. Interpretation of these results, however, is difficult, because patients did not receive therapy in a randomized fashion, nor did they receive a uniform regimen.

Despite adequate surgical resection, nearly 40% of patients were estimated to develop distant metastasis by 5 years in our series, indicating a need for development of effective adjuvant systemic therapy. To demonstrate efficacy, future studies of this uncommon tumor will need to be multi-institutional and prospective. Trials should include children and adults with large tumors ( 5 cm) or tumors with bone, nerve, or vascular invasion who have the highest risk of distant metastasis and tumor-related mortality.

	ACKNOWLEDGMENTS

 
Supported by grant no. CA-47179 from the United States Public Health Service, National Institutes of Health.

	NOTES

 
Presented in part at the Thirty-Third Annual Meeting of the American Society of Clinical Oncology, Denver, CO, May 17-20, 1997.

	REFERENCES

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION REFERENCES

 
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7. Kaplan E, Meier P: Nonparametric estimation from incomplete observations. J Am Stat Assoc 8:457-481, 1958

8. Cox DR: Regression models and life tables. J R Stat Soc B 34:187-220, 1972

9. Haagenson CD, Stout AP: Synovial sarcoma. Ann Surg 120:826-842, 1944[Medline]

10. Pack GT, Ariel IM: Synovial sarcoma (malignant synovioma): A report of 60 cases. Surgery 28:1047-1084, 1950

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19. Cadman NL, Soule EH, Kelly PJ: Synovial sarcoma: An analysis of 134 tumors. Cancer 18:613-627, 1965[Medline]

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Submitted October 25, 1999; accepted February 9, 2000.

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This Article Abstract Full Text (PDF) Purchase Article View Shopping Cart Alert me when this article is cited Alert me if a correction is posted Services Email this article to a colleague Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Save to my personal folders Download to citation manager Rights & Permissions Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Lewis, J. J. Articles by Brennan, M. F. Search for Related Content PubMed PubMed Citation Articles by Lewis, J. J. Articles by Brennan, M. F.