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© 1999 American Society for Clinical Oncology Desmoid Tumor: Prognostic Factors and Outcome After Surgery, Radiation Therapy, or Combined Surgery and Radiation TherapyFrom the Departments of Radiation Oncology and Surgical Oncology, University of Texas M.D. Anderson Cancer Center, Houston, TX. Address reprint requests to Dr. Gunar K. Zagars, Department of Radiation Oncology (Box 97), M.D. Anderson Cancer Center, 1515 Holcombe Blvd, Houston, TX 77030.
PURPOSE: To evaluate the therapeutic value of resection and the potential benefits of and indications for adjuvant and definitive radiation therapy for desmoid tumors. MATERIALS AND METHODS: We performed a retrospective review of 189 consecutive cases of desmoid tumor treated with surgical resection, resection and radiation therapy, or radiation therapy alone. Treatment was surgery alone in 122 cases, surgery and radiation therapy in 46, and radiation therapy alone in 21. Median follow-up was 9.4 years. RESULTS: Overall, 5- and 10-year actuarial relapse rates were 30% and 33%, respectively. Uncorrected survival rates were 96%, 92%, and 87% at 5, 10, and 15 years, respectively. For the patients treated with surgery, the actuarial relapse rates were 34% and 38% at 5 and 10 years, respectively. Among 78 patients with negative margins, the 10-year recurrence rate was 27%, whereas 40 margin-positive patients had a 10-year relapse rate of 54% (P = .003). Tumors located in an extremity also had a poorer prognosis than did those in the trunk. For patients treated with radiation therapy for gross disease, the 10-year actuarial relapse rate was 24%. For patients treated with combined resection and radiation therapy, the 10-year actuarial relapse rate was 25%. The addition of radiation therapy offset the adverse impact of positive margins seen in the surgical group. CONCLUSION: Wide local excision with negative pathologic margins is the treatment of choice for most desmoid tumors. Function-sparing resection is appropriate because adjuvant radiation therapy can offset the adverse impact of positive margins. Unresectable disease should be treated with definitive radiation therapy.
DESMOID TUMOR, ALSO KNOWN as aggressive fibromatosis or musculoaponeurotic fibromatosis,1 is a monoclonal2,3 fibroblastic proliferation arising in musculoaponeurotic structures. Histologically, these tumors consist of spindle-shaped cells in a collagenous matrix and lack the pleomorphic, atypical, or hyperchromatic nuclei of malignancy.1 Although desmoid tumors do not metastasize, they are locally invasive and their propensity for recurrence after conservative resection is well documented. Recent surgical series report recurrence rates of 39% to 79%.4-9 Because the histologic features of these tumors are uniform from case to case, they do not serve as a guide to potential outcome. Most surgical reports emphasize the difficulty in achieving adequate resection margins, while maintaining acceptable function and cosmesis, as the major factor contributing to high rates of relapse.5,6,9-13 However, few reports clearly document the significance of negative versus positive resection margins,12,14,15 and some authors have denied that margin status is an important determinant of outcome,16,17 emphasizing instead the variability in biologic behavior, including a potential for quiescence and even spontaneous regression, as a critical factor.15,17-20 This has confounded the definition of optimal surgical management and clouded the potential role of radiation therapy as adjuvant or definitive treatment in select patients. Although some reports claim that there is little or no benefit from radiation therapy for this disease,9,16,17,21 many studies have found external-beam radiotherapy to be helpful in the management of desmoid tumors.15,22-29 A significant factor that has limited the attempted generalizations concerning management has been the small number of cases available for analysis, reflecting the relative rarity of this disease. Few series have 100 or more patients9,12,15; typically, patient numbers range between 20 and 40,6,8,21,25-27,30 with patients often treated in a number of ways, resulting in wide confidence intervals around the estimated outcome and its dependence on potential prognostic factors. This retrospective review of consecutive patients treated at the University of Texas M.D. Anderson Cancer Center (MDACC) was undertaken to evaluate the therapeutic value of resection and the potential benefits of and indications for adjuvant and definitive radiation therapy and to define factors that influence local tumor control.
We retrospectively analyzed the medical records of all 189 patients treated with surgical resection, surgical resection and radiation therapy, or radiation therapy alone for desmoid tumors between 1965 and 1994, inclusive, at MDACC. In each case, the histologic diagnosis was confirmed at our institution. Full histories were obtained from all patients, and all patients underwent complete physical examinations, routine blood tests, and chest radiography and other radiographic work-ups as appropriate and possible during the years encompassed by this review. There were 108 women and 81 men. Patients' ages ranged from 1 to 81 years, with a mean and median of 31 and 29 years, respectively. There were no significant differences in age between female (mean age, 33 years) and male (mean age, 30 years) patients. Tumors were in the head and neck in 19 cases (10%), in the trunk in 111 (59%), in an upper extremity (distal to the axilla and shoulder) in 35 (19%), and in a lower extremity (distal to the inguinal crease and gluteal fold) in 24 (13%). Lesions of the head and neck were in the neck in 13 cases (68%). Lesions of the trunk were in the shoulder region (19 cases), anterior abdominal wall (18 cases), back (15 cases), axilla (14 cases), pelvis (14 cases), buttock (10 cases), chest wall (eight cases), retroperitoneum or mesentery (eight cases), flank (three cases), and intrathoracic cavity (two cases). Lesions of the upper extremity were in the upper arm (19 cases), forearm (13 cases), hand (two cases), and elbow region (one case). Lesions of the lower extremity were in the thigh (10 cases), leg (five cases), foot (five cases), knee region (three cases), and ankle region (one case). Seven patients (4%) had Gardner's syndrome,31 and their desmoids were in the anterior abdominal wall (three cases), on the back (two cases), in the mesentery (one case), and on the chest wall (one case). Clinical or pathologic tumor sizes were documented in 186 cases and ranged from 1 to 28 cm in largest linear dimension (mean, 8.4 cm; median, 7.0 cm). Fifty-seven tumors were 5 cm or smaller and 129 were larger than 5 cm. Forty-four tumors exceeded 10 cm in the largest dimension. Mean tumor sizes (SD) by anatomic site were as follows: head and neck, 6.9 cm (3.6 cm); trunk, 9.3 cm (5.4 cm); upper extremity, 6.7 cm (3.8 cm); and lower extremity, 7.5 cm (4.5 cm). The only statistically significant differences in size were between lesions of the trunk and lesions of the upper extremity. Tumor size in females (mean, 8.5 cm) was not significantly different from that in males (mean, 8.2 cm). One hundred four patients (55%) presented after one (54 patients) or more (50 patients) local recurrences after earlier attempts at definitive treatment outside our institution. Eighty-five patients (45%) presented with previously untreated disease. The primary focus of this review was on the outcome after the first definitive treatment at our institution. Surgical resection was the preferred treatment for all resectable desmoid tumors, and 122 patients (65%) underwent resection only—119 for gross disease and three for suspected microscopic residual disease after inadequate resection immediately before referral. Forty-six patients (24%) underwent combined resection and radiation therapy; 38 received postoperative radiation therapy and seven received preoperative radiation therapy. The use of adjuvant radiation therapy was at the discretion of the responsible physicians and was more often used if the patient had had a previous recurrence, in which circumstance radiation therapy was added to resection in 33%. Radiation therapy was added to resection in only 14% of patients with a first presentation. A second factor determining the use of adjuvant radiation therapy was the status of the resection margins. Among the 164 patients in whom all gross disease was resected, 91 (55%) had negative resection margins and only 13 of these (14%) received adjuvant radiation therapy, whereas 73 (45%) had positive resection margins and 33 of these (45%) received adjuvant radiation therapy. In 21 cases, the tumor was judged to be unresectable and radiation therapy was used as definitive treatment for gross disease. In summary, 122 patients were treated with resection, 46 patients with resection and radiation therapy, and 21 patients with definitive radiation therapy for gross disease. Twelve patients—10 in the surgical group and one each in the other two groups—received doxorubicin-based chemotherapy as previously described.32 Selected patient and tumor characteristics according to treatment modality are shown in Table 1.
The surgical strategy for desmoid tumors was to obtain tumor-free margins of 1 to 5 cm, using limb- and function-preserving approaches. If this was not in the immediate vicinity of functionally important neurovascular structures, an attempt was still made to obtain tumor-free but closer margins by dissecting in the immediate perineural or perivascular tissue planes. However, four patients underwent major resections: two had forequarter amputations, one had a hemipelvectomy, and one had most of his small bowel resected because of a mesenteric desmoid. The difficulty in achieving negative resection margins was reflected in the finding that among 164 patients in whom all gross disease was resected, 73 (45%) had microscopically positive resection margins. The radiation therapy techniques used for these patients have been described33,34 and will not be reiterated in detail. Radiation was delivered with megavoltage (60Co or higher) or electron beams, using techniques appropriate to each site. Postoperative radiation was delivered to a dose of approximately 60 Gy, with the first 50 Gy encompassing the surgical bed and a 5- to 8-cm margin and the final 10 Gy delivered through smaller fields to the surgical bed. Preoperative radiation was delivered to a dose of approximately 50 Gy, encompassing the tumor with a 5- to 8-cm margin. Definitive radiation for gross tumor was delivered to a dose of approximately 55 Gy.
Follow-up time for all 172 patients alive at last contact ranged from 2 to 377 months, with mean and median times of 11.1 and 9.4 years, respectively. Only seven patients were followed for less than 3 years. Disease relapse was scored if there was clinical-radiographic evidence of tumor regrowth. Actuarial curves for local control and survival were calculated using the Kaplan-Meier method35 and tests of significance were based on the log-rank statistic. Rothman's method36 was used to derive 95% confidence intervals (CIs) for actuarial percentages. Multivariate analysis was done with the proportional hazards model, using the log-linear relative hazard function of Cox.35 The expected survival curve for the patients was calculated from U.S. vital statistics data37 and was adjusted for the age and sex of each patient. The significance of differences between proportions was tested with the
Overall Outcome Fifty-eight (31%) of the 189 patients developed recurrence of their disease after treatment at MDACC. The actuarial freedom from recurrence is illustrated in Fig 1 and was 70% at 5 years (95% CI, 63% to 77%) and 67% at 10 years (95% CI, 60% to 74%). Time to relapse varied between 3 and 113 months after treatment (median, 23 months). The cumulative time to recurrence in the 58 patients whose disease relapsed is shown in Fig 2. More than 90% of recurrences were evident by 5 years and only four patients developed recurrence after 5 years. Univariate analysis of factors potentially correlated with local control in all 189 patients is summarized in Table 2. The only factor clearly related to outcome was patient age. Younger patients had higher relapse rates than did older patients. This effect was pronounced in patients younger than 30 years. Forty-two patients older than 40 years had a 10-year relapse rate of 25% (95% CI, 14% to 40%), 43 patients between 31 and 40 years also had a 10-year relapse rate of 25% (95% CI, 13% to 43%), 57 patients between 21 and 30 years had a 10-year relapse rate of 35% (95% CI, 24% to 48%), and 37 patients 20 years or younger had a 10-year relapse rate of 45% (95% CI, 31% to 59%). There was a trend, although not significant, for relapse to occur more often if the disease had already relapsed more than once. There was no evidence that anatomic site of the primary tumor affected outcome. In particular, comparison between extremity and nonextremity locations yielded 10-year relapse rates of 42% (95% CI, 29% to 55%) and 28% (95% CI, 21% to 37%), respectively (P = .104). Multivariate Cox proportional hazards regression revealed that only age (  30 v > 30 years) (P = .015) and treatment (surgery v radiation therapy v combined) (P = .036) were independently correlated with local control. The number of prior recurrences (> 1 v 1) was of borderline significance (P = .075). Outcomes by treatment strategy are summarized in Fig 3.
The 58 patients whose disease relapsed underwent a variety of salvage treatments, including resection, radiation therapy, chemotherapy, and combinations of these treatments. Follow-up from the time of relapse to last contact in these 58 patients was 1 to 261 months (median 9 years). Within the constraints of this follow-up, salvage treatments seem to have been successful in 43 of these patients (74%). The final, apparently curative treatments in these 43 patients were further conservation resection (24 patients), combined resection and radiation therapy (11 patients), amputation (five patients), radiation therapy alone (two patients), and hemipelvectomy (one patient). Thus, the disease seems to have been ultimately eradicated in 174 (92%) of the 189 patients. There were no deaths directly attributable to desmoid tumor in this series, and the overall uncorrected survival rates were 96% (95% CI, 92% to 98%), 92% (95% CI, 86% to 95%), 87% (95% CI, 79% to 92%), and 87% (95% CI, 79% to 92%) at 5, 10, 15, and 20 years, respectively. This survival experience was not significantly different from that expected for a matched normal cohort (Fig 1).
Outcome After Resection
Multivariate analysis identified two significant variables, each with two categories. Outcomes in the four resulting groups are summarized in Table 4. Patients with nonextremity lesions with negative resection margins constituted a favorable-outcome group, with long-term disease control achieved in 82%. In this group, patients older than 30 years had a 10-year freedom from relapse of 87%. At the other end of the outcome spectrum were patients with extremity lesions and positive margins, whose relapse rate exceeded 80%. Patients with extremity lesions and negative margins as well as patients with nonextremity lesions with positive margins had similar intermediate outcomes, and just less than one half achieved long-term disease-free status with their first resection at our institution.
Salvage therapy was successful in 31 of the 43 patients in this surgical group whose disease relapsed. Thus, the disease seems to have been eventually eradicated in 110 (90%) of these 122 patients. The uncorrected survival rates were 94% (95% CI, 88% to 97%) at 5 and 10 years and 86% (95% CI, 75% to 92%) at 15 and 20 years.
Outcome After Radiation Therapy
The time course of tumor regression for the 16 patients whose disease never relapsed was reasonably well documented in 10 patients. Six patients achieved complete regression at 6 to 51 months (median, 12 months), and in four patients the tumor, although present at last contact, had regressed significantly at 67 to 81 months after radiation therapy (median, 75 months). The remaining six patients were clinically free of disease at last contact (median follow-up, 135 months), but the time to achieve complete regression could not be retrospectively ascertained. Among the five patients whose disease relapsed, one had little response to treatment and the disease was scored as relapsed at 3 months. Three patients did achieve complete regression of their tumors at 2, 2, and 20 months. One patient's tumor seemed to show some regression, but regrowth was evident within 2 years. All five patients in this group whose disease relapsed underwent successful salvage treatment, and the 5-,10-, and 15-year survival rates were 95% (95% CI, 77% to 99%).
Outcome After Surgery Combined With Radiation Therapy
In this cohort of patients, the status of the resection margin was not a significant determinant of outcome, and addition of radiation therapy to resection seemed to offset much of the adverse impact of positive resection margins observed in the group treated with surgery alone. Comparing the outcome for patients with margin-negative resections according to the use of adjuvant radiation therapy did not reveal any significant differences in local control: the 10-year recurrence rates for patients treated with surgery alone and patients treated with both surgery and radiation therapy were 27% (95% CI, 18% to 38%) and 15% (95% CI, 4% to 42%), respectively (P = .442). However, patients with margin-positive resections fared better if radiation therapy was added: the 10-year recurrence rates for patients treated with surgery alone and patients treated with combined surgery and radiation therapy were 54% (95% CI, 37% to 69%) and 31% (95% CI, 15% to 53%), respectively (P = .007). Salvage treatment was successful in 7 of the 10 patients in this group whose disease relapsed, and the 5-, 10-, and 15-year survival rates were 100%, 85% (95% CI, 67% to 94%), and 85% (95% CI, 67% to 94%), respectively.
The clinical features of desmoid tumors in our patients were consistent with those generally reported.1,9,12,16,17 This disease is more common among women than men, it can occur at any age, and it can arise in a variety of sites but it most frequently occurs in the limb girdles. The lesion tends to be bulky at presentation. A small fraction of patients have Gardner's syndrome, and a significant proportion of patients with desmoid tumor have had at least one recurrence before referral to a tertiary care center. The overall 10-year actuarial recurrence rate of 33% determined in our study is similar to that given in most recent reports.5,8,9,11,12,15,25,39 Despite the absence of mitotic figures in histopathologic specimens, when these tumors recur they do so fairly quickly; the median time to recurrence in our study was 23 months. More than 90% of recurrences were evident by 5 years (Fig 2). Although some studies report even shorter times to relapse and suggest that the outcome at 2 years can serve as an end point,7-9,21,26 our data do not support this. It is necessary to follow these patients for a prolonged time because occasional relapses will first become evident after 5 years.12,15,30,39 Despite the fact that the disease recurred in one third of the patients in our review after initial treatment at MDACC, it was ultimately eradicated in 92% of patients. The uncorrected long-term survival was not significantly inferior to that expected for an age- and sex-matched cohort from the general U.S. population (Fig 1). However, in some series there was occasional desmoid-related mortality,5,9,12,30 and sometimes the clinical course can be rough, as in the case of the patients in our series who required debilitating resections either initially or as salvage treatment. Wide local resection, advocated nearly 100 years ago,40 remains the treatment of choice for most patients with desmoid tumors. Nevertheless, there are little data and agreement with regard to what constitutes an adequate wide margin. Typically, these tumors lack pseudoencapsulation10 and have nonpalpable extensions along muscle bundles and fascial planes, precluding reliable intraoperative clinical estimation of their extent. Despite this, attempts have been made in a number of reports to define the optimal operative procedure by evaluating outcome according to the type of resection—designated variously as simple excision, local excision, wide excision, adequate resection, inadequate resection, radical local excision, and so on—without evaluating the actual pathologic margin.5,7,9,10,17,18 Yet, as our data show, it is the actual status of the microscopic surgical margin that best determines the risk of local recurrence (Fig 4). In multivariate analysis, margin status was the single most significant determinant of recurrence in patients treated with surgery. Other studies that addressed pathologic margin status had similar findings: recurrence rates for margin-positive versus margin-negative resections have been reported as 43% v 15%,21 47% v 15%,14 68% v 12%,23 and 42% v 22%.15 Margin-negative resections are not necessarily wide. We classified negative microscopic surgical margins strictly as negative, regardless of the absolute margin of normal tissue around the lesion. In some cases, the tumor was within a few millimeters of the edge of the specimen but it was not possible to quantitate the degree of closeness in this retrospective review. One study, however, found that when tumors with negative margins were subdivided into those with close (< 1 mm) and wider (> 1 mm) margins, there was no difference in outcome.15 Thus, it seems that an appropriate resection for desmoid tumors is one that achieves negative, even if close, microscopic surgical margin. Unfortunately, the achievement of histopathologically negative margins does not assure eradication of this disease. In our series, the recurrence rate after margin-negative resection was 27%. Another recent study found a 22% recurrence rate after margin-negative resection.15 Recurrence rates as high as 68% have been reported in this circumstance.6 Clearly, occult tumor clonogens are left in situ in a significant proportion of margin-negative tumor beds. Determinants of local recurrence other than margin status have been poorly studied and reports are conflicting. In our series, a major prognostic factor was tumor location; extremity lesions had a significantly higher risk for recurrence than did lesions of the trunk, regardless of margin status (Table 4). Whereas some studies12 have not found anatomic site to be a determinant of outcome, at least three other studies have found a preponderance of recurrences among extremity lesions.5,24,27 The reasons for this phenomenon are unclear, but it was not evident among patients receiving radiation therapy (Tables 4 and 5), which suggests a particular difficulty in achieving adequate resection for extremity desmoid tumors.
We defined three patient categories on the basis of margin status and tumor location. Patients with nonextremity tumors with negative resection margins had a favorable outcome, with a relapse rate of 18%; patients with extremity lesions and negative margins as well as patients with nonextremity tumors with positive resection margins fell into an intermediate prognostic category, with a relapse rate of 48%; and patients with extremity lesions and positive margins fell into an unfavorable group, with a disease relapse rate of 83%. Although younger age ( Radiation therapy is effective in controlling gross desmoid tumor. The long-term control rate in our series (76%) is consistent with that in other reports.15,25,29,39,42,43 The fact that most patients whose disease relapsed after radiation therapy responded well to salvage treatment, which often involved surgery less radical than initially planned, suggests that even when radiation therapy fails to eradicate this disease totally, it may significantly decrease the volume of viable tumor. The radiation dose appropriate for treating gross disease remains controversial. In this analysis, we found no correlation between control and doses in the range of 50 to 75 Gy. However, in a somewhat larger group of patients including some of the surgical failures in this series irradiated for salvage, we found that doses of 56 Gy at 2 Gy per fraction produced significantly higher control rates than did doses of 50 Gy.34 Doses of more than 56 Gy produced no additional improvement. At least three other studies have found a correlation between control and dose and agree that a dose exceeding 50 Gy is required to achieve control rates greater than 70%.15,26,42 Although some investigators have recommended doses of 60 Gy or more15 we were unable to show any benefits from administration of doses greater than 56 Gy, and the incidence of radiation-related complications increased significantly when such larger doses were given.34 Thus, our current recommendation for the treatment of gross desmoid tumor is to deliver 56 Gy at 2 Gy per fraction (equivalent to approximately 60 Gy at 1.8 Gy per fraction) to an area encompassing the tumor, with a 5- to 8-cm margin.34 The effectiveness of radiation therapy for gross disease makes it likely that this treatment is effective for microscopic disease as well. In the absence of randomized data, it is difficult to evaluate precisely the potential benefits of adjuvant treatment. However, the adverse impact of positive resection margins was largely offset by the addition of radiation therapy to surgery. In our analysis, patients with positive resection margins fared significantly better when radiation therapy was added. Other studies have also found that recurrence rates were decreased when radiation therapy was used after margin-positive resection.15,22 Neither in this analysis nor in other published studies was a dose-response relationship found for microscopic disease treated with doses of 50 to 60 Gy.8,15,23,24,27,42 Thus, we recommend doses of 50 Gy at 2 Gy per fraction for treatment of microscopic residual disease. A variety of systemic agents—including tamoxifen, nonsteroidal and steroidal anti-inflammatory agents, testolactone, and cytotoxic chemotherapeutic agents—have been reported to produce partial or complete tumor responses.31,32 However, the numbers of patients treated with these agents have been small, the durability of the responses have been poorly documented, and the response rates have not approached those of conventional surgery and radiation therapy. Use of such systemic treatments remains experimental or applicable to situations in which the more conventional modalities have already been tried. Surgery remains the treatment of choice. We recommend wide local excision, with the aim of achieving negative microscopic surgical margins. However, the radicality of resection should be tempered so that significant compromise of function is avoided. If margins are positive or tumor was dissected off critical structures such as vessels or nerves, consideration should be given to the use of postoperative radiation therapy. In some of these situations, especially in young patients, close follow-up may be acceptable in lieu of radiation therapy if it is estimated that salvage treatment in the event of recurrence will not compromise functional and cosmetic outcome.15 If the margins of resection are negative, there is no compelling evidence that adjuvant treatment improves outcome and such patients should be followed. Primary amputation and other radical procedures should rarely be necessary, because there is significant likelihood that radiation therapy of gross disease will eradicate conventionally inoperable desmoid tumors.
Supported in part by grant no. CA06294, awarded by the National Cancer Institute, U.S. Department of Health and Human Services
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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
2 statistic or with Fisher's exact test, and differences between means were tested with the nonparametric Mann-Whitney test.
