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Annals of Surgical Oncology 9:346-354 (2002)
© 2002 Society of Surgical Oncology

ORIGINAL ARTICLES

Initial Results of a Trial of Preoperative External-Beam Radiation Therapy and Postoperative Brachytherapy for Retroperitoneal Sarcoma

Julia J. Jones, MD, MSc, Charles N. Catton, MD, Brian O’Sullivan, MB, Jean Couture, MD, Ryan L. Heisler, MSc, MD, Rita A. Kandel, MD, PhD and Carol J. Swallow, MD, PhD

From the University of Toronto Sarcoma Group, Princess Margaret Hospital and Mount Sinai Hospital, Toronto, Ontario, Canada.

Correspondence: Address correspondence and reprint requests to: Carol J. Swallow, MD, PhD, FRCS(C), Mount Sinai Hospital, 600 University Ave., Suite 1224, Toronto, ON, M5G 1X5, Canada; Fax: 416-586-8392; E-mail: cswallow@ mtsinai.on.ca.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Background: Surgical resection alone does not cure the majority of patients with retroperitoneal sarcoma (RPS). We evaluated the effects of preoperative external-beam radiotherapy (XRT) and postoperative brachytherapy (BT) combined with complete surgical resection.

Methods: Fifty-five patients with primary or locally recurrent RPS judged to be resectable were entered onto a trial of combined therapy and observed prospectively. Forty-six patients underwent complete gross resection with curative intent. Of these, 41 patients completed preoperative XRT and 23 patients received BT. Outcome measures were treatment toxicity, overall survival, and disease-free survival (DFS).

Results: Preoperative XRT was very well tolerated and was associated with Radiation Therapy Oncology Group acute toxicity scores of <=2 in all patients. Acute postoperative and BT-related toxicity resulted in modified RTOG scores of >=3 in 39.1% (18 of 46) of patients. Late toxicity was associated with death in 4.3% (2 of 46) and with life-threatening illness in 2.2% (1 of 46) of patients, all of whom had been treated with BT to the upper abdomen. The 2-year overall survival and DFS for resected RPS were 88% and 80%, respectively. Significantly better 2-year DFS was achieved in patients with primary RPS and in those with low-grade tumors (93% and 95%, respectively).

Conclusions: The initial results of combined therapy are promising. Although preoperative XRT was very well tolerated, BT to the upper abdomen was associated with substantial toxicity. Our current protocol includes selective application of BT to the lower abdomen only.

Key Words: Retroperitoneal sarcoma • External-beam radiotherapy • Brachytherapy • Survival analysis


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Retroperitoneal soft tissue sarcoma (RPS) is a rare disease that almost invariably presents at an advanced stage. Although complete surgical resection represents the only hope of cure, resection of these large tumors is often technically complex and challenging.1–6 Despite complete gross surgical resection, RPS has a predilection to recur locally, that is, within the retroperitoneum and the peritoneal cavity. Several recent studies indicate that resection alone results in local control rates of 35% to 50% at 5 years.7,8 Furthermore, failure to control local disease, rather than distant metastatic disease, causes death in the majority of patients with RPS.1,3,9,10

Postoperative external-beam radiotherapy (XRT) has been used by several sarcoma groups in an effort to reduce local recurrence rates and improve disease-free survival (DFS) in patients with RPS. Unfortunately, no clear lasting benefits have been demonstrated.8,11 The failure of surgery alone or combined with adjuvant postoperative XRT to prevent local recurrence has prompted an interest in new strategies for adjuvant therapy, including preoperative XRT, intraoperative radiotherapy, postoperative brachytherapy (BT), and neoadjuvant chemotherapy.12 Preoperative XRT with the tumor in situ offers several potential advantages: it allows for more accurate radiation planning, minimizes toxicity to contiguous organs, in particular small bowel, and allows for the delivery of high-dose radiation to very large volumes. In addition, preoperative XRT may decrease the risk of tumor implantation at the time of resection by sterilizing the operative field of microscopic tumor emboli. BT can potentially be used in conjunction with conventional XRT to escalate the dose to the tumor bed, specifically targeting areas at high risk of local recurrence.

We evaluated the effect of preoperative XRT and postoperative BT in a cohort of prospectively observed patients with RPS who were resected for cure. We hypothesized that preoperative XRT and postoperative BT, in conjunction with complete gross resection, could be administered safely with minimal morbidity and could positively affect the control of disease in patients with RPS. The preliminary results of a trial of combined therapy are described. In this initial report, our primary outcome measure was treatment toxicity. Overall survival (OS) and DFS were evaluated at the 2-year time point.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
From June 1, 1996, to October 5, 2000, 83 patients with a diagnosis of RPS were referred to Princess Margaret Hospital, Toronto, Canada. Clinicopathologic, treatment, and outcome data were recorded in a prospective database at the time of referral. All outside pathology specimens were reviewed internally. Patient variables included age at diagnosis, sex, and presentation status (primary or recurrent). Tumor variables included maximum diameter, histological subtype, histological grade (low or high), and location of tumor.

Patients with primary or recurrent RPS in situ deemed to be potentially resectable on imaging studies and with no evidence of distant metastatic disease were eligible for a trial of combined therapy consisting of preoperative XRT, complete surgical resection, and postoperative BT. Of the 83 patients referred, 14 had recently undergone resection at an outside institution, 9 were found to have distant metastases, 3 were deemed technically unresectable, and 2 refused therapy. These 28 patients were excluded from the trial (Fig. 1). The remaining 55 patients gave informed consent and were entered onto a trial of combined-modality therapy. The protocol was approved by the University of Toronto Ethics Review Board.



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  		FIG. 1. Management of patients entered on the trial of combined therapy. This flow diagram illustrates the management of patients presenting to Princess Margaret Hospital, Toronto, with retroperitoneal sarcoma (RPS) from June 1, 1996, to October 5, 2000. Numbers of patients undergoing complete gross resection, external-beam radiation (XRT), and brachytherapy (BT) are indicated.

 
Patients were excluded from preoperative XRT if they had previously received XRT to the same site. Preoperative XRT was designed with a conformal external-beam plan by using three-dimensional treatment-planning techniques. A decision to proceed with BT was based on the intraoperative assessment. Patients who received BT had a single plane of afterloading BT catheters placed on the surgical resection bed at the end of the surgical extirpation. The site for catheter placement was selected for its close proximity to the tumor and the risk of residual microscopic disease at that site. One-centimeter intercatheter spacing was used, and catheters were brought out through separate stab wounds in the skin. The parallel orientation of the catheters was maintained with absorbable sutures to secured Vicryl mesh.13 Three to eight catheters were placed. Closed suction drainage catheters were also inserted to prevent weeping of serous fluid around the catheter exit sites. Exit sites were locally treated with topical polymyxin B and bacitracin. Our protocol was modified partway through the study because of our perception that BT was associated with a high rate of severe duodenitis when applied to the upper abdomen. Therefore, in the latter half of the trial, BT was administered in a selective fashion; we applied it to patients with close margins along structures in the lower abdomen.

BT was given as a planar implant at a dose rate of .5 Gy/hour at a depth of .5 cm by using an afterloading iridium-192 pulsed dose rate BT unit. All plans were optimized to correct for the geometry of misplaced catheters. BT was delayed until the patient recovered from the surgery with evidence of gastrointestinal (GI) function (postoperative days 7–14).

The acute toxicity of preoperative XRT was recorded with the Radiation Therapy Oncology Group (RTOG) toxicity score at each outpatient visit during treatment and every 2 weeks after completion of the XRT up to the time of surgery. Operative mortality was defined as death occurring up to 30 days after resection. The acute treatment toxicity after surgery, with or without BT (referred to as acute postoperative toxicity), was recorded at the maximum point during the 3 months after completion of treatment. Chronic treatment-related toxicity (referred to as late toxicity) was measured at each follow-up visit after completion of therapy. Modified RTOG scores were used to measure both acute postoperative toxicity and late toxicity.

Fifty-five patients were observed until death or February 28, 2001. The median follow-up time was 16 months for the 55 patients entered onto the trial and 19 months for the 46 patients who were resected with curative intent. Patients were followed with clinic visits, chest x-ray, and computed tomographic scans of the abdomen/pelvis every 4 months for 2 years after completion of therapy and every 6 months thereafter. For all patients whose disease recurred, recurrence was first identified on imaging studies before the development of any symptoms or signs on physical examination. The time to recurrence and DFS were measured according to changes in serial imaging studies compared with the postoperative baseline.

Local recurrence was defined as disease recurrence in the abdomen (retroperitoneal, peritoneal cavity, or intra-abdominal lymph nodes) but not within the liver parenchyma. Systemic recurrence was defined as recurrent disease within the liver parenchyma or at an extra-abdominal site.

OS and DFS at 2 years were estimated according to the Kaplan-Meier method.14 Comparisons between OS and DFS curves grouped by presentation and histological grade were made by using log-rank analysis. OS and DFS were calculated on the basis of the time from the date of surgery to the last follow-up visit or death. For those patients who did not undergo complete gross resection (n = 9), total follow-up was calculated from the date of the first visit.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Patient Characteristics and Management
Fifty-five patients were entered onto a prospective trial of combined therapy. This study group comprised a heterogeneous group of patients typical of the referral pattern to a tertiary cancer center. We included patients who had been previously treated at other institutions by various modes of therapy, including open biopsy (n = 2), attempted resection (n = 1), previous resection followed by recurrence (n = 18), and chemotherapy (n = 1). Of the 55 patients entered onto the trial, 9 patients did not complete the protocol: 5 had local progression or developed metastases during the preoperative period, and 4 patients died of disease progression or complications of their local disease before surgery (Fig. 1). These nine patients were observed until death and are included in the analysis of all patients entered on the trial.

The clinicopathologic characteristics of the 55 cases are listed in Table 1. The median age was 59 years (range, 25–86 years). Women represented 55% (30 of 55) and men 45% (25 of 55) of the group. A total of 67% (37 of 55) of the patients presented with primary tumors, and 33% (18 of 55) presented with recurrent RPS. Tumors were classified as high grade in 64% (35 of 55) and low grade in 36% (20 of 55). The median maximum diameter of the tumor was 17 cm (range, 3–40 cm) on pretreatment imaging.


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  		TABLE 1. Clinicopathologic characteristics of 55 patients entered on the trial of combined therapy
 
Preoperative Radiation and Acute Toxicity
All patients were accurately staged and then started on the treatment protocol. Forty-one patients had preoperative XRT followed by curative resection (Fig. 1). The median preoperative XRT dose for these patients was 45 Gy (range, 42–50 Gy; n = 41). The median volume that received at least 95% of the maximum XRT dose was 7.3 L (range, .5–30.7 L). Preoperative XRT was uniformly associated with RTOG acute toxicity scores of <=2. No patients were hospitalized and none terminated radiotherapy because of acute toxicity, although one patient had to delay XRT for 1 week because of acute nausea and vomiting. A total of 24.4% (10 of 41) had an upper-GI score of 1. A total of 31.7% (13 of 41) had an upper-GI score of 2. Lower-GI/pelvic scores were 1 in 9.8% (4 of 41) and 2 in 14.6% (6 of 41) of patients. One patient had a GI score of 2.

Surgical Resection, BT, and Acute Postoperative Toxicity
Surgical resection was performed via a transabdominal approach. Resection of contiguous structures, in addition to tumorectomy, was performed in 95% of patients. No histological assessment of margins was attempted intraoperatively. Operative mortality (death within 30 days after surgery) was 2.2% (1 of 46).

Twenty-three patients received BT (Fig. 1). The median BT dose was 25 Gy (range, 7.3–30 Gy; n = 23). The median BT area was 50 cm2 (range, 24–108 cm2). Of the patients who were planned to receive BT, 2 of 23 did not complete the protocol. One patient had technical difficulties with catheter displacement, and one patient developed respiratory distress secondary to severe atelectasis. These two patients had BT terminated prematurely at 7.3 and 14.5 Gy, respectively.

Acute postoperative toxicity, which included operative morbidity and BT-related toxicity, was assessed with a modified RTOG score in the 46 patients who underwent resection. Fifteen patients had no toxicity. Eight patients had minor symptoms. Five patients had symptoms that required some medical intervention, including three patients with nausea and vomiting and one patient with delayed wound healing. Eleven patients had symptoms that necessitated readmission to hospital or prolongation of hospitalization and active therapy; the problems in this group included severe upper-GI symptoms (n = 4), chylous ascites (n = 2), and cellulitis (n = 1). Six patients had life-threatening complications that were managed successfully acutely, including two patients with severe duodenitis. One patient died of liver failure after right hepatic lobectomy in the setting of preoperative XRT to the liver.

The late toxicity scores associated with combined therapy are listed in Table 2. There were two late treatment-related deaths, each directly or indirectly related to duodenal perforation during wire-guided nasojejunal feeding tube insertion performed under fluoroscopy in patients who had duodenal strictures and who had received upper-abdominal BT.


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  		TABLE 2. Late toxicity scores for patients undergoing curative resection ± BT (n = 42; three follow-ups not complete, one postoperative death)
 
Comparison of treatment toxicity between patients who received BT and those who did not showed that four of six patients who developed grade 4 acute postoperative toxicity had received BT. All six patients who experienced late toxicity had received BT.

The pattern of recurrence is shown in Table 3. With a median follow-up of 19 months (range, 1–56 months), local recurrence had developed in 19.6% (9 of 46), and systemic recurrence developed in 2.2% (1 of 46). A total of 34 of 46 patients are alive with no evidence of disease, with 1 patient having had a second resection of a local recurrence.


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  		TABLE 3. Pattern of recurrence and final disease status in 46 patients resected with curative intent
 
Survival Analysis
Overall Survival
The OS for all 55 patients at 24 months was 72.8% (Table 4). The OS at 2 years was 77.9% for primary RPS and 64.4% for locally recurrent presentation (not significant by z-test). The OS at 2 years was 94.7% for low-grade RPS and 60.0% for high-grade RPS (P < .05 by z-test). Log-rank analysis of the survival curves showed a statistically significant difference in OS between low- and high-grade tumors (P < .05).


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  		TABLE 4. Overall and disease-free survival at 2 years (%)
 
OS was assessed in the cohort of 46 patients who underwent complete gross resection with curative intent (Fig. 2A, Table 4). The OS at 2 years for completely resected disease was 88.0%. OS at 2 years for patients with resected disease presenting with primary disease was 96.7% (n = 30) compared with 74.1% for those with locally recurrent presentation (n = 16; not significant by z-test; Table 4). However, there was a statistically significant difference in the OS curves for primary versus locally recurrent presentation by log-rank analysis (P < .05; Fig. 2B). OS at 2 years for low-grade RPS in resected patients was 94.7% compared with 82.5% for high-grade RPS (not significant by z-test; Table 4); there was no statistically significant difference between the OS curves for low- and high-grade RPS after curative resection (Fig. 2C).



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  		FIG. 2. Overall survival in patients resected with curative intent. (A) Overall survival in all patients (n = 46) was calculated by the method of Kaplan and Meier. The median follow-up time was 19 months. (B) Overall survival according to presentation. There was a statistically significant difference between primary and locally recurrent presentation (P < .05; log-rank analysis). (C) Overall survival according to histological grade.

 
Disease-Free Survival
DFS was calculated for the 46 patients who underwent complete surgical resection of their tumor with curative intent (Table 4, Fig. 3A–C). DFS at 2 years was 79.5% (n = 46). DFS at 2 years was 93% in patients with primary presentation, versus 58% for locally recurrent presentation (n = 30 and 16, respectively; P < .05 by z-test). In addition, there was a statistically significant difference in DFS curves between primary and recurrent presentation by log-rank testing (P < .05; Fig. 3B). DFS at 2 years was 94.5% for low-grade tumors and 67.7% for high-grade tumors (not significant by z-test), and there was no statistical difference between the DFS curves demonstrated on log-rank analysis (Fig. 3C). The effect of BT on OS and DFS could not be assessed statistically because the limited number of patients in each group and short follow-up time in those not receiving BT caused skewing and instability of rates in this initial analysis.



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  		FIG. 3. Disease-free survival in patients resected with curative intent. (A) Disease-free survival in all patients (n = 46), calculated with the Kaplan-Meier method. The median follow-up was 19 months. (B) Disease-free survival according to presentation. There was a statistically significant difference between primary and locally recurrent presentation (P < .05; log-rank analysis). (C) Disease-free survival according to histological grade.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
CONCLUSIONS
 REFERENCES
 
Postoperative XRT has been associated with improved disease outcomes in some retrospective, nonrandomized studies of RPS. One report showed improved actuarial 10-year local relapse-free survival from 35% to 55% in unirradiated versus radiated patients after complete resection.15 Tepper et al.16 reported improved local control for patients who received >60 Gy compared with <50 Gy. Fein et al.17 reported local control rates of 72% vs. 38% for patients who received more versus less than 55 Gy; these rates were measured at 2 years after treatment. Previous data from our own institution8 showed a similar differential in local control rates at 2 and 5 years for patients who received greater or less than 35 Gy after complete excision, although the rates had reached equivalency by 10 years.

These reports demonstrate that low-dose postoperative XRT does not prevent local recurrence of RPS but that higher doses can delay the time to local recurrence.8,11 Factors that have limited the usefulness of XRT include inadequate radiation doses and inadequate treatment volumes. The delivery of a full radical dose of postoperative XRT is hampered by the presence of small bowel loops in the tumor bed and accurate identification of the target volume after surgery. Postoperative radiation is clearly associated with a significant risk of severe acute and late bowel toxicity.18

In this study, we used preoperative XRT. Preoperative XRT provides the advantage of having cross-sectional imaging available to plan the radiation fields directly onto the tumor, and the tumor mass acts as a tissue expander, displacing sensitive structures out of the radiation field. A very large volume was treated to 45 Gy with minimal acute toxicity. The majority of patients resected for cure received preoperative XRT (n = 41), and RTOG acute radiation toxicity scores were all <=2. Only 2 of 41 patients experienced postoperative wound-healing complications, in contrast to the significant risk of wound-healing complications recently shown to be associated with preoperative radiotherapy for extremity sarcoma.19

Postoperative BT was used in an effort to achieve a further 25-Gy dose escalation. Previous reports in the literature have shown impressive control rates with intraoperative radiotherapy for dose escalation. In a randomized trial that tested the effect of intraoperative radiotherapy in addition to postoperative XRT, Sindelar et al.11 showed a reduction in the 8-year local relapse rate from 80% to 40%; the intraoperative boost increased the total dose of radiation to 60 Gy. During our initial patient accrual, patients were given postoperative BT in a nonselective manner. High rates of acute postoperative toxicity were noted, in particular relating to duodenitis and gastric outlet obstruction. This was self-limited in most patients, but two experienced serious and irreversible injury. This toxicity may well have been due to a combined effect of both the XRT and BT, but the individual effect of each technique is difficult to distinguish. It seemed that upper-abdominal placement of BT afterloading catheters was associated with the highest morbidity because of sensitivity of the duodenum to radiation injury. Therefore, in our later patient accrual, patients were more selectively given BT with avoidance of proximity to the duodenum. Since then, no further cases of clinically significant duodenitis have developed.

Although our follow-up is still relatively immature, the OS for patients who underwent resection is 88% at 2 years, which is encouraging. The subset analysis of primary presentation and low-grade tumors yields even more impressive 2-year OS rates of 94.7% and 96.7%, respectively. Our DFS rate at 2 years in the curatively resected patients with primary RPS (n = 30) was 92.6% (95% confidence interval, 83.2%–100%). This compares favorably to the 2-year DFS of 81% reported by Lewis et al.3 from Memorial Sloan-Kettering Cancer Center for 231 patients with primary RPS who underwent complete gross resection alone.

Recurrent presentation and high histological grade have previously been shown to be associated with an adverse outcome in several series.15,20– 23 Our data show that presentation with locally recurrent disease is associated with a decrease in both OS and DFS in surgically resected patients, compared with primary presentation. Although primary versus recurrent status may represent a marker for biology of disease, the difference in outcome supports an aggressive therapeutic approach at the time of primary presentation and argues for evaluation of these patients at a cancer center with experience in the multidisciplinary management of RPS.

In this study, a statistically significant difference in OS was shown between high- and low-grade tumors for the group of 55 patients entered onto our protocol of combined management. However, in the group of patients undergoing curative resection (n = 46), there was no demonstrable difference in outcome on the basis of high- versus low-grade histology, partially because of the more limited numbers in each group. In addition, the nine patients entered on the trial who were unable to complete the protocol all died within 6 months, and all had high-grade tumors. Their exclusion from the analysis of resected patients diminishes the difference between high- and low-grade tumors.

Evaluation of the pattern of treatment failure showed that the majority of patients who developed recurrence had local recurrence. Of the 46 patients resected for cure, only 1 patient (2.2%) developed systemic metastases. A total of 56.5% (26 of 46) of the curatively resected patients had histologically high-grade tumors. Because previous series have demonstrated that high-grade tumors have a greater propensity to develop distant metastases, 24 we speculate that preoperative XRT may have had a mitigating effect on the development of distant metastases in patients treated with combined therapy in this trial. Further follow-up is required to accurately determine the long-term outcome in this group of patients.


   CONCLUSIONS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
REFERENCES
 
Preoperative XRT for resectable RPS was associated with minimal acute toxicity. However, our preliminary results with BT to the upper abdomen have shown significant acute postoperative and late toxicity. Selective application of BT and technical modifications have successfully reduced this toxicity to an acceptable level. We currently avoid application of BT to structures in the upper abdomen.

Both locally recurrent presentation and high histological grade were associated with adverse outcome. The high local failure rate for patients presenting with recurrent disease emphasizes the importance of aggressive local therapy at the time of initial presentation.

We achieved promising results with a combined treatment protocol of radiation dose escalation using preoperative XRT and postoperative BT. Given the 97% 2-year DFS we have achieved in patients with primary presentation, we are continuing patient accrual to this protocol. Longer follow-up is necessary to conclusively establish the safety and efficacy of selective BT. In addition, we advocate a multi-institutional randomized controlled trial of preoperative XRT versus surgery alone to definitively determine the optimal management of RPS.


   Footnotes
 
Presented at the 54th Annual Cancer Symposium of the Society of Surgical Oncology, Washington, DC, March 15–18, 2001.

Received for publication March 17, 2001. Accepted for publication January 18, 2002.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 

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