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10.1245/s10434-006-9139-0
Annals of Surgical Oncology 14:583-590 (2007)
© 2007 Society of Surgical Oncology
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Original Article

Use of Tissue Expanders and Pre-operative External Beam Radiotherapy in the Treatment of Retroperitoneal Sarcoma

J. S. White1, D. Biberdorf1, L. M. DiFrancesco2, E. Kurien3 and W. Temple1

1 Department of Surgical Oncology, Tom Baker Cancer Centre, Calgary, Canada
2 Department of Pathology and Laboratory Medicine, University of Calgary, Calgary, Canada
3 Department of Radiation Oncology, Tom Baker Cancer Centre, Calgary, Canada


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Introduction: We report our experience of treating retroperitoneal sarcoma (RPS) using pre-operative external beam radiotherapy (EBRT) in combination with radical resectional surgery from 1990 to 2005.

Methods: Twenty-eight primary and 10 recurrent tumors were identified from a prospective database.

Results: The resection rate was 71% overall; 82% in primary (23/28) and 40% (4/10) in recurrent cases. EBRT was administered preoperatively in 25 patients, postoperatively in 1, and palliatively in 11. In 33 patients a saline-filled tissue expander was inserted into the abdomen before radiotherapy to displace small bowel from the radiation field. 4,500–5,000 cGy was administered in fractions of 180–200 cGy over a 5-week period; surgery followed 6–8 weeks later. Expander insertion was associated with minimal morbidity; 31/37 patients received a dose of 4,000 cGy or more (median 4,650 cGy). Median resected tumor diameter was 13 cm, and a median of three adjacent organs was resected per patient. Complete macroscopic resection was achieved in 25/27 patients (93%); R0 in 9 (33%) and R1 in 13 (48%) (microscopic margins unclear in 5). There was no postoperative mortality. Tumors were high-grade in 20 patients, low-grade in 14 and ungraded in 4. Actuarial 5- and 10-year survival for all patients was 74 and 60%. For operable primary tumors, the 5-year survival and disease-free rates were 90 and 80%. In four patients with operable recurrent tumors, median disease-free interval was 91 months (27–160). In the 11 inoperable cases, median survival after radiotherapy was 48 months (9–77).

Conclusions: We conclude that a combination of pre-operative tissue expander placement, high-dose EBRT and radical resectional surgery can achieve acceptable morbidity, extended survival and low long-term recurrence in patients with RPS.

Statistics: Median (interquartile range).

Key Words: Retroperitoneal sarcoma • Pre-operative radiotherapy • Recurrence • Survival


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Retroperitoneal sarcoma is a rare tumor, accounting for 15–25% of all soft tissue sarcoma, which itself makes up only 1% of all malignancies.1–3 In contrast to sarcoma of the limbs, surgical resection of retroperitoneal sarcoma is made more difficult by the proximity of vital abdominal structures, and resection margins are correspondingly closer.1 As a result, the rate of local recurrence after resection of retroperitoneal sarcoma is higher than for limb sarcoma, and it can exceed 40% at 5 years and 70% at 10–20 years after surgery.1,4–7 Disease tends to recur locally, both in the retroperitoneum and the peritoneal cavity but may also involve the liver and more distant sites.8 Five-year survival after surgery alone for retroperitoneal sarcoma has been reported to range from 20 to 52%.9,10 Factors which have been identified as prognostic include operability and completeness of resection, tumor size, tumor grade and histological subtype.11–20 Adjuvant chemotherapy for retroperitoneal sarcoma has not been shown to be beneficial for this group of tumors21 and some studies have suggested it may actually decrease survival,22–25 although it may be beneficial for some tumors with high mitotic rates.8

Adjuvant radiotherapy has been shown to have a powerful effect in the treatment of limb sarcoma, and can decrease local recurrence rates to as low as 10% when combined with surgery.26 It is thought that radiotherapy is effective in the treatment of sarcoma as it destroys cells within the flattened pseudocapsule developed as the tumor ‘pushes’ rather than infiltrates into normal surrounding tissue.8 Given that retroperitoneal sarcoma shows a similar spectrum of histological tumor types to limb sarcoma, it seems probable that adjuvant radiotherapy might have a similar beneficial effect in the treatment of retroperitoneal sarcoma when combined with radical resectional surgery.1,27 No consensus exists however on the ideal method of the delivering the desired dose of radiation to the retroperitoneum, and various authors have described the use of a combination of pre-operative, intra-operative and post-operative external beam radiotherapy, as well as the use of brachytherapy techniques.28–31 No randomized controlled trials on the subject have yet been reported, and the results of case series have been inconsistent, with some showing no benefit at all11 and others showing a significant reduction in local recurrence with a variety of radiation protocols.20,29,32,33 A number of authors have suggested that a high dose of radiation may be required to achieve satisfactory local control.34,35

Several theoretical advantages have been proposed for the use of external beam radiotherapy in the pre-operative setting:27 the tumor can be targeted better while still in situ; the same biological effect can be achieved using a smaller target volume and a lower total dose compared to post-operative radiotherapy; there is less tissue hypoxia in the pre-operative setting; irradiating the tumor pseudocapsule while still in situ may ‘sterilize’ the margin of the tumor and lead to less intraoperative shedding of viable tumor cells. In addition, in the pre-operative setting, there are no adhesions fixing the small bowel in the radiation field and the tumor mass may also displace small bowel away from the area to be treated, which should reduce the incidence of radiation-induced enteritis. On the other hand, it has been suggested that the high doses of radiation required to treat retroperitoneal sarcoma are associated with an unacceptable rate of radiation enteritis, which has been reported in up to 50% of patients treated with doses exceeding 5,000 cGy.36

In an effort to reduce the bowel-related morbidity of high dose radiation treatment for abdominal tumors, several centers have described the use of saline-filled ‘spacers’ or ‘tissue expanders’, which are inserted into the abdomen to displace the small bowel out of the radiation field. In the largest series reported to date, the technique has been shown to be effective in excluding the small bowel from at least 75% of the planned target volume in 89% of patients.37 The technique has been used in the irradiation of pediatric pelvic tumors, gynecological cancers and advanced colorectal tumors,37–40 and three case reports have described the use of the technique for the treatment of abdominal sarcoma.41,42

The aim of this paper was thus to describe the results of a novel technique utilizing abdominal tissue expanders in association with pre-operative external beam radiation for the treatment of retroperitoneal sarcoma at a single Canadian cancer center.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
In 1990, a novel protocol for the treatment of retroperitoneal sarcoma was established at the Sarcoma Clinic of the Tom Baker Cancer Centre, which serves the city of Calgary (population 1.2 million, 2005) and the southern part of the province of Alberta, Canada. This protocol involved the placement of saline-filled tissue expanders into the abdomen to displace small bowel prior to the administration of a course of external beam radiation treatment, followed by radical resectional surgery.

A prospective database was established to monitor the implementation of this new protocol, and to record information on all cases of retroperitoneal sarcoma treated at the Sarcoma Clinic. Information was collected by the treating physician on patient demographics, spacer placement, radiation treatment received, tumor characteristics, operative findings and complications and recurrence patterns. Information on patient follow-up, recurrence and survival was collected from the database and was cross-checked with information from outpatient clinics and the Alberta Cancer Registry. Ethical approval was obtained for chart review. Data was collected using Microsoft Excel (Microsoft, Seattle) and survival analysis was performed using Stata (StataCorp, Texas). Data analysis was performed in September 2005.

Thirty-eight consecutive patients with retroperitoneal sarcoma (22 females and 16 males) were seen in the Tom Baker Sarcoma Clinic from 1990 to 2005. Twenty-eight patients had primary disease (first presentation, no previous surgery), while 10 had disease which had recurred after previous surgery. There was a gradual increase in the number of cases seen at the clinic in succeeding 5-year periods: 10 in 1990–1994, 13 in 1995–1999 and 15 in 2000–2004. There was also a change noted in the ratio between primary and recurrent cases seen in the same 5-year periods, suggesting a changing referral pattern—4:6 in 1990–1006, 9:4 in 1995–1999 and 15:0 in 2000–2004.

Initial staging in all cases was performed by CT scanning of the chest, abdomen and pelvis, and CT-guided tumor biopsy. In cases after 2001, tumors were also staged using MRI. The left upper quadrant of the abdomen was the most common tumor location (13 cases), although a significant number of tumors were located in the pelvis (six cases), the right iliac fossa (five cases) and the left flank (four cases). There were smaller numbers of cases arising in the right upper quadrant, the right flank or the inferior vena cava (two cases each) and the left iliac fossa (one case). In three cases the tumor was so extensive that the initial site of origin could not be determined. Maximum tumor diameter ranged from 8 to 48 cm (median 20 cm).

Of the 28 primary cases, five were deemed inoperable due to the extent of disease or patient factors (82% operability rate, 23 patients). This was due to the presence of locally advanced disease involving major vascular structures or to the presence of distant metastasis at diagnosis. Of the 10 recurrent cases, 6 were deemed inoperable for similar reasons. Twenty-five of the 27 patients in which surgery was planned underwent pre-operative external beam radiotherapy, and one received radiation post-operatively. In the 11 patients in which surgery was not possible, palliative radiotherapy was given.

In 33 cases, one to two saline-filled tissue expanders were inserted via laparotomy to displace the small bowel away from the planned radiation target volume (23 cases: 1 expander; 10 cases: 2 expanders). An initial dissection was performed to free any tethered bowel and mobilize it away from the tumor mass. The bowel was then held away from the tumor using sponges. Tissue expanders were interposed between the tumor and the bowel and were held in place using a portion of Dexon mesh which was sutured to adjacent peritoneal and fascial structures to maintain expander position. Each tissue expander was 700 ml in volume, measuring 14.6 x 6.7 cm (Technology for Life®, product no. 3612-06R). In a further three cases, the tumor appeared to be displacing the small bowel from the target volume already, and tissue expander insertion was not required. In the remaining case, a tissue expander was placed in similar fashion at the time of definitive tumor resection and radiation was given postoperatively. Patients appeared to tolerate tissue expander insertion well, and the only significant morbidity was minor wound infection in 2 of 34 cases (5.8%).

Two weeks after tissue expander insertion, external beam radiation therapy was commenced in 36 patients. The planning target volume (PTV) was calculated in each case as gross tumor volume plus a 1.5 cm margin. Three-dimensional conformal radiation planning was then used to achieve a 95% isodose line covering the PTV while keeping the dose to adjacent organs within acceptable limits. Treatment plans typically employed three or four fields, with field sizes usually at least 20–25 cm wide and at least 20 cm long. The standard planned pre-operative treatment dose was 4,500–5,000 cGy given in 180–200 cGy daily fractions for 5 days per week for 5 weeks, and the full planned dose was delivered in 20 of 25 patients. Patients undergoing palliative therapy received a similar treatment regimen, and a dose of 4,000 cGy was delivered in 8 of 11 patients. Thirty-one of 37 patients received a dose of 4,000 cGy or more (median 4,650 cGy; interquartile range 4,500–5,000 cGy). The treatment appeared to be well tolerated, although several patients complained of nausea, constipation and a feeling of abdominal fullness. One patient developed radiation-induced cystitis, and another was briefly admitted to hospital for conservative management of a self-limiting episode of ileus.

Six to eight weeks after the completion of radiotherapy, definitive resectional surgery was performed in 27 patients (23 primary and 4 recurrent cases). In addition to the tumor, a median of three additional organs were resected en bloc (range 0–5; organs included: pancreas, spleen, kidney, adrenal, colon, bladder, external iliac artery, liver, diaphragm, ovary, aorta, inferior vena cava, coccyx, section of pelvis and rib). A complete macroscopic resection was achieved in 22 of 23 primary cases (96%) and in three of four recurrent cases. There was no perioperative mortality. Pathologic analysis determined that microscopic margins were negative (R0) in nine cases (33%), positive in 13 cases (48%) and unclear in five cases (19%).

Routinely prepared histological slides from all cases were reviewed by a pathologist with expertise in soft tissue sarcoma. Tumors were graded using the French Federation of Cancer Centers Sarcoma Group System.43 Nineteen of the 38 tumors were classified as liposarcoma. Half of the primary tumors (14 of 28) were liposarcomas, but a range of other tumor types were also present: synovial sarcoma (3), leiomyosarcoma (2), hemangiopericytoma (2), malignant fibrous histiocytoma (MFH) (1), fibrosarcoma (1), chordoma (1), mesenchymal chondrosarcoma (1), and not otherwise specified (NOS)/other (3). Half of the ten recurrent tumors were also liposarcomas (5), followed by two leiomyosarcomas, one MFH, one fibrosarcoma, and one NOS tumor.

Twenty of the 34 tumors (59%) in which a grade was assigned were high-grade (grade 2 or 3). In the primary tumor group, 64% of the cases were high grade (4/28 = grade 2 and 14/28 = grade 3). Seven cases (25%) were low grade, while the remaining three (11%) could not be graded. Of the recurrent group, the majority (7/10) were grade 1 tumors, followed by two grade 3 tumors, and one non-graded tumor. Patient and tumor characteristics are summarized in Table 1Go.


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  		TABLE 1. Patient and tumor characteristics
 

   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
The estimated actuarial 5-year survival for all patients with retroperitoneal sarcoma was 74%, and the 10-year survival was 60% (Fig. 1Go). The actuarial 5-year survival was 90% for operable primary disease, 80% for recurrent inoperable disease, 75% for recurrent operable disease and 0% for primary inoperable disease (3-year survival in this group: 20%). At a median follow-up of 57 months (interquartile range 34–94 months), 20 of 23 patients with operable primary disease remain alive (87%). All 11 patients receiving palliative radiotherapy have deceased, as have three of four patients with operable recurrent disease; one patient has been lost to follow-up.


Figure 1
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  		FIG. 1. Actuarial survival of all patients with retroperitoneal sarcoma (n = 38).

 
The estimated actuarial 5-year recurrence-free rate in patients with operable primary retroperitoneal sarcoma was 80% (Fig. 2Go). The 10-year recurrence-free rate in this group was estimated at 45%. Of 23 patients with operable primary disease, 6 (26%) suffered recurrence of disease in the follow-up period. The median time to recurrence in these six patients was 41 months (interquartile range 35–68 months). All of these recurrences occurred locally; only one was suitable for further resection. The median survival after recurrence in these six patients was 17 months (interquartile range 8–39 months).


Figure 2
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  		FIG. 2. Actuarial disease-free survival of patients with operable primary retroperitoneal sarcoma (n = 23).

 
Of the four patients with operable recurrent disease, all recurred again, two locally and two with distant metastasis. The median interval before recurrence was 91 months (interquartile range 27–160 months), and the median survival after recurrence was 20 months (interquartile range 14–28 months). Further resection was performed in the two cases of local recurrence.

These figures compare favorably with larger studies on recurrence after surgery for retroperitoneal sarcoma which describe a median disease-free interval of 22 months and a 5-year survival of 37%.44

In the 11 patients with inoperable disease who received palliative radiotherapy only, the median survival was 48 months (interquartile range 9–77 months).

In patients with high-grade tumors, median survival was 41 months (16–72) compared to 71 months (53–115) in those with low-grade tumors. The same pattern was observed in primary and recurrent cases: median survival 55 months versus 41 months in primary cases by grade, and 82 months versus 39 months in recurrent cases by grade. The estimated 5-year survival in all in patients with low-grade tumors was 88%, while it was 57% in all patients with high-grade tumors. Grade was also observed to have an influence on recurrence: the median disease-free interval after surgery in patients with low-grade tumors was 54 months (26–71) versus 37 months (35–76) in patients with high-grade tumors.

Although there was some inconsistency in the reporting of surgical margins, median disease-free intervals appeared to be longer in patients with a negative microscopic margin compared to those with a positive margin (51 months (35–68) versus 37 months (29–76)).

In those 19 patients with liposarcoma (14 primary, 5 recurrent, 16 operable), 17 underwent tissue expander placement with a median delivered dose of radiation of 4,800 cGy. Nine patients had high-grade tumors (eight primary, one recurrent). The 5-year survival was 80% for all patients with liposarcoma and 86% for patients with primary operable disease. The 5-year recurrence-free rate in 11 patients with primary operable liposarcoma was 75%.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
This paper demonstrates that the combination of pre-operative tissue expander placement, external beam radiotherapy and radical resectional surgery can achieve acceptable morbidity, low long-term recurrence rate and extended survival in patients with retroperitoneal sarcoma.

The 5-year overall survival rate of 70% we report for all cases of retroperitoneal sarcoma regardless of previous surgery or operability is the highest yet described in the literature and compares with figures of 45–66% reported in similar series.10,11,14,15,29,31,45,46 The 10-year survival rate of 60% we observed exceeds figures of 27–46% previously reported.2,10,11,46

The 80% 5-year recurrence-free rate described here for patients with operable primary disease is the lowest reported in the literature to date, and compares favorably with other recent studies describing local control in 63–74% of cases.10,11,18,29,31,46 The estimated 45% 10-year recurrence-free rate we observed also compares well with other series2,6 and suggests that many patients achieve durable long-term local control with this protocol. All recurrences observed occurred locally at the operative site or in adjacent peritoneum, the majority within 4 years of the original surgery, which is in accordance with previous published reports.8

The tumor size and range of pathology observed concurs with most other series of retroperitoneal sarcoma, with a histological diagnosis of liposarcoma in 50% of all cases and 16 of 27 operable cases.3,16 Figures for survival and recurrence appeared similar in liposarcoma and other tumor types. We also observed that tumor grade has an important effect on survival and recurrence rates, as noted by many previous studies.11–20 The 82% operability rate we demonstrated for primary tumors also agrees well with other papers.3,45,46 Complete macroscopic resection was achieved in 96% of primary cases and 75% of recurrent cases, a pattern described in other published series.2,23 Complete macroscopic resection is a powerful prognostic factor which has been associated with long-term disease-free survival,13,15,17–20 and this may partly explain the favorable results observed in our series.

Although this study was not designed as a trial of the use of tissue expanders, we believe that the use of these devices to displace small bowel from the radiation field is a safe and effective way of facilitating delivery of full-dose radiation prior to radical surgery for retroperitoneal sarcoma. Since adopting this protocol, we have observed a reduction in the expected incidence of acute side effects associated with radiation therapy, and a decreased requirement for medications to counter these effects, suggesting that tissue expander placement combined with careful radiation planning reduces the volume of small bowel treated. We agree with other authors who contend that delivery of an adequate dose of adjuvant radiotherapy is essential if local control of retroperitoneal sarcoma is to be achieved, and that the benefit of giving lower doses of adjuvant radiation may be limited.29,30,33,36,47 We hypothesize that the use of abdominal tissue expanders increases the effective dose of radiation able to be delivered to the tumor, maximizing its biological effectiveness and enhancing the results of resectional surgery. A similar effect could perhaps be achieved by the use of newer radiation delivery techniques such as intensity-modulated radiation therapy (IMRT) to reduce the dose administered to small bowel. However, IMRT alone may increase the amount of soft tissue irradiated to a lower dose, which may in turn increase the risk of future radiation-induced second malignancy compared to 3D conformal radiation in combination with a tissue expander.

This study also suggests that adjuvant radiotherapy can have a significant effect on recurrent retroperitoneal sarcoma, and when combined with surgery, can delay further recurrence by several years. It also appears to have a valuable role in palliation: 50% of patients with inoperable disease were observed to survive more than 2 years after a course of palliative radiation. We did observe that late recurrence and death can occur more than 5 years after surgery in a significant proportion of patients, with some patients experiencing recurrence over 10 years after initial treatment.

The results of this study compare favorably with a recent prospective trial on adjuvant radiotherapy (pre-operative, intra-operative, brachytherapy) in the treatment of 72 patients with operable intermediate-and high-grade retroperitoneal soft tissue sarcoma. The study combined a phase I trial and a pilot study from two centres employing different treatment protocols utilizing a combination of pre-operative chemotherapy, intra-operative electron beam radiotherapy, pre-operative EBRT and brachytherapy. Although information on the adverse effects of pre-operative radiotherapy was not provided, the authors reported that 64 of 72 patients completed the planned pre-operative radiotherapy, and 32 of 37 patients treated at one centre received a planned dose of 45 Gy. The authors reported a 5-year overall survival of 61% and a 5-year recurrence-free rate of 60% in 54 patients undergoing an R0/R1 resection. The 5-year overall survival in all 72 patients regardless of resection status was 50%. These results may reflect the exclusion of patients with low-grade malignancy from one center in the trial.

Ideally, we would like to see the results of our study confirmed by a large, prospective, multi-center, randomized controlled trial. Unfortunately, other authors have pointed out the difficulties of recruiting patients with retroperitoneal sarcoma to such a trial: much variation in treatment has already been established between different centers, accrual to any trial would be slow due to the rarity of the condition and extended follow-up would be required.48 We agree with a recent editorial that the investigation of adjuvant treatment for retroperitoneal sarcoma is at a "crossroads" of sorts, and that it is unlikely that a large trial will ever address the issue of adjuvant therapy of this "orphan disease."49 Two trials (RTOG-S0124 and ACOSOG-Z9031) on the condition recently closed prematurely due to poor accrual,50 possibly due to established physician and institutional bias for or against adjuvant radiotherapy which prevented patient enrolment. We would suggest that if a large trial cannot be conducted, some useful information may be gleaned by establishing a national prospective database to record information on the treatment of retroperitoneal sarcoma. Institutions such as our own could then continue to provide treatment according to locally established protocols but would submit their results for comparison with other protocols used in other institutions. Analysis of this database might then provide definitive evidence on the benefit of adjuvant treatment for this condition. It is hoped that such a strategy might provide a firm evidence base to establish the role of adjuvant radiotherapy in the treatment of retroperitoneal sarcoma.

In conclusion, this study demonstrates that the combination of pre-operative tissue expander placement, external beam radiotherapy and radical resectional surgery is feasible and safe in the treatment of retroperitoneal sarcoma and that acceptable morbidity, extended survival and low long-term recurrence can be achieved in patients with this condition.


   FOOTNOTES
 
Previously Presented in Oral Form to the Canadian Surgery Forum, September 10, 2005, Montreal, Canada.

Present address: J. S. White, Royal Alexandra Hospital, 4th Floor CSC, 10240 Kingsway, Edmonton, AB T5H 3V9, Canada. Address correspondence and reprint requests to: J. S. White; E-mail: edmontonsurgeon{at}mac.com

Received for publication June 23, 2006. Accepted for publication June 26, 2006.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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