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© 1999 American Society for Clinical Oncology Long-Term Outcomes After Function-Sparing Surgery Without Radiotherapy for Soft Tissue Sarcoma of the Extremities and TrunkFrom the Center for Sarcoma & Bone Oncology and Divisions of Radiation Oncology, Surgical Oncology, Biostatistics, Medical Oncology, and Pathology, Dana-Farber Cancer Institute/Brigham and Women's Hospital, Harvard Medical School, Boston MA. Address reprint requests to Samuel Singer, MD, Division of Surgical Oncology, Brigham and Women's Hospital, 75 Francis St, Boston, MA 02115; email singer{at}partners.org
PURPOSE: To define the rate of local recurrence (LR) and identify prognostic factors for LR for patients with soft tissue sarcoma (STS) treated with function-sparing surgery (FSS) without radiotherapy (RT). PATIENTS AND METHODS: Between 1970 and 1994, 242 patients with STS of the trunk and extremity presented with primary localized disease, 74 of whom were treated with FSS without RT (31%). The median tumor size was 4 cm (range, 0.5 to 31 cm). There were 40 patients with grade 1 tumors and 34 with grade 2 and 3 tumors. Median follow-up was 126 months.
RESULTS: The 10-year actuarial local control rate was 93% ± 4%. Resection margin status was a significant predictor for LR. Patients with closest histologic resection margins of less than 1 cm had a 10-year local control rate of 87% ± 6% compared with 100% for patients with closest histologic resection margins of CONCLUSION: The 7% LR rate after treatment of STS with FSS without RT reported herein is comparable to published rates following treatment where adjuvant RT is used. These results suggest there may be a select subset of patients with STS in whom carefully performed FSS may serve as definitive therapy and in whom adjuvant RT may not be necessary. However, further study is needed to carefully define this subset of patients and to identify the optimal surgical approach and technique for patients treated without RT.
BEFORE THE 1980s, amputation was frequently considered standard treatment for soft tissue sarcoma of the extremities. This practice was changed in 1982 with the report of the randomized trial from the National Cancer Institute on the treatment of extremity sarcoma, which compared amputation with function-sparing surgery and radiotherapy (RT).1 The local recurrence rate after treatment with function-sparing surgery and RT was only 15%, and there was no survival difference between the two treatment groups. At about the same time as that report, and for years following, many institutions published outcome results for series of patients treated with function-sparing surgery and RT. Reported local recurrence rates ranged from 0% to 25%, with most studies documenting local recurrence rates of  15%.2-11 Of note, these reported local recurrence rates pertained to treatment with either preoperative or postoperative RT. Published local recurrence rates after treatment with function-sparing surgery without adjuvant RT vary greatly and depend to a large extent on the type of surgery performed, ie, marginal excision, wide excision, or radical excision. Marginal excision is defined as removal of the gross tumor with no attempt to remove a cuff of normal tissue; wide excision generally refers to removal of the gross tumor with at least 2 cm of normal surrounding tissue; radical excision refers to removal of the entire compartment in which a tumor is located. Reported rates for local recurrence after marginal excision alone have been unacceptably high, ranging from 56% to 75% in some series.3,12-14 The reported rates of local recurrence after wide excision alone have varied greatly in the literature. Most institutions have reported local recurrence rates in the 30% to 35% range,6,10,11,14 whereas a few institutions have reported local recurrence rates after wide excision alone as low as 0% to 8%.12,13,15-17 To better understand the relationship between extent of surgery and local recurrence in the absence of adjuvant RT, we analyzed the long-term outcomes of patients with soft tissue sarcoma who were treated with function-sparing surgery without RT at Brigham and Women's Hospital and the Dana-Farber Cancer Institute.
Between 1970 and 1994, 418 patients with primary localized soft tissue sarcoma were evaluated at the Adult Sarcoma Program at the Dana-Farber Cancer Institute and Brigham and Women's Hospital. To meet inclusion criteria for the following analysis, patients had to have soft tissue sarcoma of the trunk or extremity and present with primary localized disease that had not been treated by amputation. Furthermore, the local treatment for all patients was surgery alone. (None of the included patients received radiotherapy as part of their initial treatment.) The following histologic diagnoses were excluded: osteosarcoma, Ewing's sarcoma/primitive neuroectodermal tumor, rhabdomysarcoma, dermatofibrosarcoma protuberans, and fibromatosis (desmoid); and the following tumor sites were excluded: retroperitoneal, intrathoracic, intra-abdominal, and head and neck. The study cohort was composed of 74 patients. Standard evaluation of patients included a history and physical examination, complete blood count, and serum chemistry analyses. Where appropriate, magnetic resonance imaging or computed tomography scan of the primary tumor site and chest computed tomography scans were also obtained. The type of surgery performed (marginal excision, wide excision, or radical excision) was ascertained from the operating surgeon's assessment and surgical intent as documented on the operative report. The primary size of the tumor and depth with respect to the fascia (superficial or deep) were recorded. For all cases, the pathology was reviewed at Brigham and Women's Hospital for histologic type and grade. In addition, measurements of tumor proximity to the closest resection margin were recorded. The above data were all retrieved from a prospectively collected database. Among the 242 patients seen at Brigham and Women's Hospital and Dana-Farber Cancer Institute who met the above criteria, 74 (31%) received local treatment with function-sparing surgery alone. As shown in Table 1, the overall percentage of patients treated with surgery alone was 58% for patients with grade 1 tumors, 32% for grade 2, and 17% for grade 3 tumors.
Patient characteristics are listed in Table 2. There were 32 men and 42 women with a median age of 45 years (range, 21 to 82 years). The histologic grade was 1 for 40 patients (54%), 2 for 11 (15%), and 3 for 23 (31%). The median tumor size was 4 cm (range, 0.5 to 31 cm). The most common histologic diagnosis was liposarcoma (23 patients), followed by malignant fibrous histiocytoma (MFH)/pleomorphic sarcoma not otherwise specified (16 patients), leiomyosarcoma (12 patients), malignant peripheral nerve sheath tumor (eight patients), spindle cell sarcoma not otherwise specified (three patients), angiosarcoma (three patients), synovial sarcoma (two patients), and extraskeletal chondrosarcoma (two patients). Five other histologic diagnoses occurred in one patient each. The most common tumor sites were the trunk and thigh (24 patients each), followed by the upper arm (eight patients), lower leg (six patients), and knee/popliteal region (five patients). The remaining sites were affected in three or fewer patients each: breast (three patients), foot/ankle (two patients), forearm (one patient), and hand (one patient). There were no significant differences in patient characteristics when patients were categorized by truncal versus extremity site (data not shown.)
Treatment
Margins were evaluated both grossly and microscopically in six dimensions (superior, inferior, medial, lateral, anterior, and posterior). The tumor's proximity to resection margins was recorded, and the closest margin was used to analyze margin status and local recurrence. The median value for the closest margin from the tumor to the inked edge of the specimen was 0.9 cm (range, 0 to 5 cm). Margins were further categorized as clear, microscopically positive, or grossly positive. A clear margin indicated that there was no tumor more than 1 mm from the edge of the inked specimen; a microscopically positive margin indicated microscopically discernible extension of tumor to within Doxorubicin-based adjuvant chemotherapy was delivered to seven patients, five patients with grade 3 tumors and one patient each with a grade 1 or 2 tumor. As stated above, none of the 74 patients received any form of radiotherapy as part of the initial management. Patients were seen in follow-up every 3 to 4 months for the first 3 years and then every 6 months. At these time points, local, regional, and distant disease status, survival, and cause of death were recorded. Local recurrence was defined as disease recurrence within the site of the initial tumor bed. Regional recurrence was defined as disease recurrence adjacent to the site of the initial tumor bed or in adjacent lymph nodes. The median follow-up for all patients was 126 months (range, 7 to 398 months); for all living patients, it was 116 months (range, 32 to 398 months). Median follow-up for living patients according to tumor grade was 121 months (range, 36 to 219 months) for grade 1, 116 months (range, 32 to 398 months) for grade 2, and 70 months (range, 42 to 231 months) for grade 3, (Table 2).
Statistics
Patterns of Failure All patients were assessable for local, regional, and distant recurrence as well as survival. Among the 74 patients, four experienced a local recurrence, for a crude local control rate of 95%. There was one local recurrence each in the groups of patients with grade 1 tumors and grade 2 tumors and two local recurrences among those with grade 3 tumors. The single local recurrence in the grade 1 group occurred in a patient who presented with a 3-cm fibrosarcoma of the scapular region treated by wide excision. The closest histologic resection margin was 0.5 cm. The recurrence occurred at 35 months and was salvaged by a second wide excision and 69.4 Gy of postoperative external-beam RT. The patient ultimately died at 164 months from a papillary adenocarcinoma of the ovary. The single local recurrence in the grade 2 group occurred in a patient with a 3-cm MFH of the calf treated with initial wide excision that resulted in a closest histologic resection margin of 0.5 cm. At 5 months, he developed both a local and regional recurrence in the soft tissues of the leg as well as the fibula. He underwent an above-knee amputation and was alive without disease at 157 months. Two patients in the grade 3 group experienced local recurrences. The first patient had a 9-cm MFH of the anterior chest wall excised with a microscopically positive margin. (He did not receive RT because of prior mediastinal RT for a seminoma 13 years earlier.) He developed a local and regional recurrence of the chest wall and mediastinum at 2 months and died of disease at 12 months. The final patient had a 2-cm leiomyosarcoma of the popliteal region treated with an excision that achieved a 0.5-cm histologic margin. She developed a local recurrence at 25 months that was treated with excision and 60 Gy of external-beam RT. She developed a second local recurrence at 80 months that was salvaged with another excision and 45 Gy delivered via brachytherapy. She remains alive without disease at 129 months. Three patients in the series developed a regional recurrence. The details of two patients are described above. The patient with a 3-cm grade 2 MFH of the leg experienced a synchronous local recurrence in the calf and regional recurrence in the fibula. The patient with a 9-cm grade 3 MFH of the chest wall developed a synchronous local and regional recurrence of the chest wall and mediastinum. The third patient experienced an isolated regional recurrence. She had a 6.5-cm grade 3 leiomyosarcoma of the chest wall. She underwent a wide resection, and the closest histologic resection margin was 0.3 cm. (She did not receive adjuvant RT because she had received prior RT for breast cancer.) Her disease recurred in the axilla at 8 months. The recurrence was resected, and she remains alive without disease at 97 months. Overall, nine patients (12%) experienced a distant recurrence as a first site of failure. Distant recurrences as first site of relapse were seen for two patients (5%) with grade 1 tumors and seven patients (30%) with grade 3 tumors. The sites of distant recurrence included the lung (three patients), liver (one patient), retroperitoneum (one patient), and calf (one patient) and were unknown in three patients. The median time to distant recurrence has not yet been observed. At the time of the last distant recurrence (14.6 years), 76% of patients remained free of distant disease progression. Eight of the nine patients who developed a distant recurrence died of sarcoma. (One patient with a grade 1 tumor of the thigh experienced a metastasis to the lung at 9 months and was still alive at 82 months' follow-up.)
Local Control Analysis
When the assessment of competing risks was performed,22,23 the local cause-specific probabilities for the whole patient group at 5 years and 10 years were 4% and 6%, respectively (compared with 4% and 7% by the Kaplan-Meier method). Detailed analysis of predictors for local recurrence also provided results similar to those of the Kaplan-Meier method. The relationship between resection margin status (< 1 cm v
Survival For all patients, the actuarial overall survival rate was 89% (±4%) at 5 years and 73% (±6%) at 10 years. Survival according to grade shows the 5-year and 10-year actuarial survival rates were 100% and 87% (±6%) for patients with grade 1 tumors, 100% (at both 5 and 10 years) for patients with grade 2 tumors, and 65% (±10%) and 37% (±12%) for those with grade 3 tumors. The difference between these rates is statistically significant (P < .0001). Statistically significant survival differences were also seen favoring T1 tumors (< 5 cm) and superficial tumors. The 5-year and 10-year survival rates for T1 tumors were 97% (±2%) and 79% (±7%), respectively, compared with 77% (±8%) and 66% (±10%) for T2 tumors (P = .02). Superficial tumors were associated with 5-year and 10-year survival rates of 96% (±4%) and 90% (±7%), respectively, compared with 86% (±5%) and 64% (±8%) for deep tumors (P = .02).
In this series of 74 patients with soft tissue sarcoma treated with function-sparing surgery without RT, the 10-year actuarial local recurrence rate was 7% and the 10-year overall survival rate was 73%. Histologic resection margin status less than 1 cm was the only statistically significant predictor for local recurrence. Among the four patients who developed a local recurrence, two underwent successful salvage therapy with further function-sparing surgery and radiotherapy, one underwent salvage treatment consisting of an amputation due to regionally advanced disease, and one died of synchronous locally and regionally recurrent disease involving the chest wall and mediastinum. In this series of patients treated with function-sparing surgery without RT, the low local recurrence rate of 7% is comparable to reports from four other institutions. Rydholm et al12,15 from Lund, Sweden, have reported local recurrence rates of 5% and 7% following treatment with wide excision alone. These reports included patients with tumors that were both subcutaneous and intramuscular, high and low grade, and of varying sizes. Rydholm et al emphasize that tumor location and surgical technique are critically related to the risk of local recurrence. They advocate that surgery alone for the treatment of sarcoma may be applied selectively if surgery is carefully performed according to the following principles. Subcutaneous tumors require resection of a "cuff of fat tissue around the tumor and inclusion of the deep fascia beneath the tumor"; intramuscular tumors require "no (prior) open biopsy and an unbroken muscle fascia or (resection of) a thick muscle cuff around the tumor."15 They do not advocate surgery alone for extramuscular tumors. In an earlier report, Rydholm and Rooser25 showed a 27% local recurrence rate for tumors not confined to a muscle compartment (extracompartmental), deep or subcutaneous tumors that had grown through the deep fascia, and deep tumors resected without a fascial boundary surrounding the entire specimen. Markhede et al13 reported a series of 82 patients treated in Goteborg, Sweden, with function-sparing surgery alone. The local recurrence rate was 8% for 63 patients treated with a wide excision compared with 74% for 19 patients treated with marginal excision. This study included high-grade tumors, and most tumors were more than 5 cm in size. Karakousis et al16 showed a 10% local recurrence rate among 116 patients treated with wide excision at Roswell Park Cancer Institute between 1977 and 1992. The majority of tumors in this study were high grade and larger than 5 cm. The fourth study was reported by Gibbs et al17 from the University of Chicago. It included 62 patients with subcutaneous soft tissue sarcomas, 47% of which were high grade and 32% of which were larger than 5 cm. The median follow-up time for living patients was 56 months. Among 35 patients treated with wide excision alone (including removal of deep fascia and 1 cm of underlying muscle), there were no local recurrences.
In contrast with the above reports of local recurrence rates of
Among the 74 patients treated with surgery alone in the current study, only six had positive resection margins and 68 (92%) had negative margins. None of the six patients with a positive resection margin experienced a local recurrence, and all of the recurrences occurred among patients with a closest histologic resection margin of less than 1 cm. Thus, it seems that the minimum margin necessary for acceptable local control is in the order of 1 cm. Specifically, the 10-year local recurrence rate for patients with histologic margins of less than 1 cm was 13%, compared with 0% for those with margins of No statistically significant differences in the risk of local recurrence were found for tumor grade, tumor stage, or depth. This is not surprising, because with only four local recurrence events, statistical power is limited. It may be that subsequent studies with larger patient numbers will show some of these factors to be important. Furthermore, as expected, the present study did show statistically significant differences for all of these factors as predictors for survival. Although not statistically significant, there was a 10-percentage point difference in local recurrence rates between low- and high-grade tumors. The 10-year local recurrence rate was 2% for grade 1 tumors compared with 12% for grade 2 and 3 tumors (P = .2). The nature of the relationship between grade and the risk of local recurrence remains an unanswered question. Some authors have found a significant correlation13,17 whereas others have not.7,11,14 It is widely believed that adjuvant RT should be delivered before or after function-sparing surgery for all high-grade and many low-grade soft tissue sarcomas.5,29-31 (RT is generally recommended for low-grade tumors that are larger than 5 cm, have close resection margins, or are locally recurrent.) This dogma is based on thoughtful analyses of hundreds of patients over many years, but perhaps it is time to re-examine the indications for adjuvant RT following function-sparing surgery. The 10-year local recurrence rate of 7% after function-sparing surgery without RT in this study is comparable to reported rates from several institutions for function-sparing surgery and RT.5-11,16 When designed and executed carefully, RT can be delivered safely and result in good function.32,33 However, treatment with RT is not without morbidity, which can include edema, fibrosis, limited mobility, impaired wound healing, pain, and second tumors,8,9,34-37 as well as cost and inconvenience. It would be advantageous to the patient to omit RT from the treatment of soft tissue sarcoma, but only if such an omission does not result in a significantly increased local recurrence rate and corollary loss of function (ie, amputation) or compromised survival. One might even accept a slightly higher local recurrence rate by foregoing RT if the majority of patients who do develop a local recurrence could be helped by salvage therapy. We believe that a high salvage rate can be achieved with proper patient selection. Singer reported a 67% limb salvage rate in his series of unselected patients who presented to Brigham and Women's Hospital and Dana-Farber Cancer Institute with locally recurrent disease.38 Furthermore, although the topic is controversial, a local recurrence does not seem to adversely affect survival. The randomized trial from Memorial Sloan-Kettering Cancer Center, where patients received function-sparing surgery alone versus surgery plus brachytherapy, showed a 23% higher risk of local recurrence for patients with high-grade tumors treated with surgery alone compared with those who received adjuvant RT. However, with a median follow-up of 6.5 years, there was no difference in overall survival between the groups.11
Admittedly, the low local recurrence rate we report in this retrospective study is prone to potential selection bias. As shown in Table 1, 58% of patients who presented with grade 1 tumors were treated without RT compared with 20% of patients with grade 2 and 3 tumors. The median tumor size for the series is only 4 cm. (It is also important to note that 40% of the 77 patients had tumors Given the disparity of results after treatment of soft tissue sarcoma with wide excision alone,6,10,11,13-17 any change in standard treatment recommendations should be made judiciously. Potential candidates for treatment with wide excision alone include those with (1) primary presentation of disease, (2) histologic resection margins of more than 1 or 2 cm in all directions, (3) sites of disease such that a local recurrence would not preclude function-sparing salvage surgery and RT, and (4) the ability and willingness to comply with close follow-up. In cases in which the initial resection violates tissue planes, such as compartmental or fascial boundaries, it is unclear whether a subsequent re-excision that achieves acceptable histologic margins suffices for treatment because of concerns of tumor contamination during the first resection. At our institutions, we generally recommend a proper surgical re-excision combined with adjuvant RT for patients who have undergone a marginal excisional biopsy that disrupted tissue planes or when the details of the initial excision are not available for careful pathology review. Whether high grade should be a contraindication to treatment with function-sparing surgery without adjuvant RT remains an open question. Although not statistically significant, we found a higher local recurrence rate for high-grade tumors. The suitability of deep tumors for function-sparing surgery alone is also unresolved. The present study suggests that with experienced surgical technique that avoids disruption of tissue planes and achieves margins of more than 1 cm, the local recurrence rate for deep tumors is acceptably low without the addition of RT. The careful definitions put forth by Rydholm et al of adequate surgery for deep intramuscular tumors are worthy of study.15,25 It is notable that they exclude deep extracompartmental tumors from the treatment approach of surgery alone. In addition to careful surgery, meticulous and detailed reporting of pathology, as outlined by the Association of Directors of Anatomic and Surgical Pathology, is essential for appropriate treatment decision-making.39 In summary, we report a 7% 10-year actuarial local recurrence rate after treatment of soft tissue sarcoma with function-sparing surgery without RT. These results are comparable to those reported in other studies in which function-sparing surgery and adjuvant RT were used together. We believe these results suggest that adjuvant RT may not be indicated for a select (but significant) subset of patients with soft tissue sarcoma. However, further study is needed to accurately define this select subset of patients and to validate the low local recurrence rates reported here and by others.12,13,15-17 In the meantime, decisions to offer local treatment of soft tissue sarcoma with function-sparing surgery alone should be made with care by a multidisciplinary team with experience in sarcoma management.
Presented in part at the Thirty-First Annual Meeting of the American Society of Clinical Oncology, Los Angeles, CA, May 20-23, 1995.
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Gibbs CP, Peabody TD, Mundt AJ, et al: Oncological outcomes of operative treatment of subcutaneous soft-tissue sarcomas of the extremities. J Bone Joint Surg Am79:888-897, 1997 18. Cox DR. Analysis of Binary Data. London, United Kingdom: Methuen and Co, 1970 19. Wilcoxon F. Individual comparisions by ranking methods. Biometrics 1:80-83, 1945 20. Kaplan EL, Meier P: Nonparametric estimation from incomplete observations. J Am Stat Assoc53:457-481, 1958 21. Peto R, Peto J: Asymptotically efficient rank invariant test procedures (with discussion). J R Stat Soc [A]135:185-206, 1972 22. Gaynor JJ, Feuer EJ, Tan CC, et al: On the use of cause-specific failure and conditional failure probabilities: Examples from clinical oncology data. J Am Stat Assoc88:400-409, 1993 23. Gray RJ. A class of k-sample tests for comparing the cumulative incidence of a competing risk. Ann Stat 16:1141-1154, 1988
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Copyright © 1999 by the American Society of Clinical Oncology, Online ISSN: 1527-7755. Print ISSN: 0732-183X
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ABSTRACT
INTRODUCTION
1 cm (P = .04). There was no significant association between LR and tumor grade, size, site (truncal v extremity), or depth (superficial v deep). For all patients, the 10-year actuarial survival rate was 73% ± 6%. 
