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10.1245/s10434-007-9385-9
Annals of Surgical Oncology 14:1870-1877 (2007)
© 2007 Society of Surgical Oncology
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Original Article

Pelvic Exenteration Affords Safe and Durable Treatment for Locally Advanced Rectal Carcinoma

Christopher J. Gannon, MD1, Jonathan S. Zager, MD1, George J. Chang, MD1, Barry W. Feig, MD1, Christopher G. Wood, MD2, John M. Skibber, MD1 and Miguel A. Rodriguez-Bigas, MD1

1 Department of Surgical Oncology, Unit 444, The University of Texas M. D. Anderson Cancer Center, 1515 Holcombe Boulevard, Houston, Texas 77030, USA
2 Department of Urology, Unit 1373, The University of Texas M. D. Anderson Cancer Center, 1515 Holcombe Boulevard, Houston, Texas 77030, USA

Correspondence: Address correspondence and reprint requests to: Miguel A. Rodriguez-Bigas, MD; E-mail: mrodbig{at}mdanderson.org


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
Background: Treatment of locally advanced rectal carcinoma (LARC) often involves exenterative surgery, which can be associated with high perioperative morbidity and mortality. To assist in patient selection for radical surgery, we sought to determine clinicopathologic factors influencing recurrence and disease-free survival (DFS) of LARC.

Methods: Consecutive patients with LARC undergoing exenterative surgery were retrospectively identified in our institutional database. Factors evaluated included age, sex, primary versus recurrent tumors, neoadjuvant or adjuvant chemoradiotherapy, resection margin status, recurrence, time to recurrence, and survival. The primary outcome was DFS. Secondary outcomes were overall survival and perioperative morbidity.

Results: A total of 72 patients were identified; median age was 52 years, and median follow-up time was 30 months. The overall complication rate was 43%; rates were similar among the patients with primary (47%) or recurrent (37%) LARC. Primary or recurrent tumor status was the only factor significantly predictive of outcome after exenteration. Local recurrence rates were lower in the primary group (primary 22%, recurrent 52%, P = .05). A significant difference in 5-year DFS was found between primary and recurrent tumor (52% vs. 13%; P < .01). The median time to recurrence was longer in the patients with primary LARC (17 months vs. 8 months; P < .01).

Conclusions: The complication rates for pelvic exenteration remain high, but the morbidity can typically be managed without a clinically important increase in hospitalization. In primary LARC, an aggressive surgical approach provides most patients 5-year DFS. Select patients with recurrent LARC will also benefit from pelvic exenteration.

Key Words: Pelvic exenteration • Rectal carcinoma • Complication rate • Pelvic recurrence


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
The incidence of rectal cancer remains high in the United States with more than 40,000 new cases expected in 2006.1 Rectal adenocarcinoma is considered locally advanced rectal carcinoma (LARC) when the tumor breaches the confines of the rectal wall and invades via direct extension into the mesorectum or adjacent organs or is noted to be fixed on clinical examination.2–4 These features are identified by a clinical evaluation that includes endoscopic ultrasonography (EUS), computed tomographic (CT) scan, and magnetic resonance imaging (MRI), as well as a physical examination. These tumors are categorized as either T3 or T4 by the staging system of the American Joint Committee on Cancer.5 The definition of LARC does not take in to account nodal disease or distant metastases. In the United States, evaluation of the Surveillance, Epidemiology, and End Results cancer database reveals that up to 18% of rectal cancer cases can be considered LARC.6

Potentially curative resections of LARC may involve resection of contiguous pelvic organs, including exenterative procedures. Historically, the morbidity and mortality rates for pelvic exenteration have been reported to be more than 50% and 10%, respectively.7,8 Because of the considerable operative risks, the benefit of these radical extirpative operations has been questioned. Some centers may not offer pelvic exenteration as an option for LARC because of the risks and perceived lack of benefit. Although unresected LARC will inevitably become symptomatic and will impair the patient’s quality of life, surgery such as colostomy may provide some relief. However, patients have an increased risk of chronic severe pain and diminished quality of life if they present with pelvic pain.9 No established survival benefit has been associated with incomplete resection in LARC;10 several studies have found that the median survival time for patients with LARC treated with nonsurgical therapy is <2 years.11,12

The purpose of this study was to evaluate survival and recurrence outcomes after exenterative surgery for rectal carcinoma at a tertiary-care center to determine the clinicopathologic factors that affect these outcomes.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
Patient Identification and Management
Consecutive patients with LARC undergoing multivisceral resection from January 1996 to December 2003 were identified in the University of Texas M. D. Anderson Cancer Center’s institutional database, and their records were retrospectively reviewed. This study was approved by our institutional review board.

Seventy-two patients with primary or recurrent LARC treated with exenterative surgery were identified. Tumor staging was obtained by cross-sectional imaging (CT or MRI, EUS, or both). All patients had disease confined to the pelvis at the time of resection. Exenterative surgery was defined as total pelvic exenteration (TPE), supralevator exenteration (SLE), or posterior pelvic exenteration (PPE). TPE included the en bloc removal of the rectum, anus, urinary bladder, prostate in men, and uterus and ovaries (if present) in women. SLE included the removal of rectum, uterus, vagina, ovaries, and or/bladder and prostate with the reestablishment of intestinal continuity. PPE included removal of the ovaries (if present), uterus, posterior vaginal wall, and rectum. The surgical approach was based on the patients’ findings at presentation and at surgical exploration. Surgical resectability was determined by the individual surgeon and based on the guidelines listed in Table 1Go. Pelvic exenteration was delayed at least 6 weeks after chemoradiation and up to 10 weeks.


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  		TABLE 1. Contraindications to pelvic exenteration for curative intent
 
Radiation treatment was delivered by a three-field belly-board technique to either a total dose of 45 Gy in 25 fractions or with an additional boost of 7.5 Gy in five fractions to the primary tumor site.

Data Collection
The medical records were evaluated for clinical factors including age, sex, primary versus recurrent tumors, use of neoadjuvant or adjuvant therapy, complications, presence of recurrence, time to recurrence, and total follow-up time. Operative factors examined included the extent of resection, the type of reconstruction, and the use of intraoperative radiotherapy (IORT). Pathologic factors evaluated were histologic characteristics, margin status, and pathologic tumor, node, metastasis system stage. Perioperative mortality was defined as death within 30 days of the pelvic exenteration. Major morbidity was defined as those complications requiring reoperation or prolonging the length of hospital stay >20 days.

Statistical Analysis
Mean differences between the treatment groups were compared by the {chi}2 test for univariate analysis. Recurrence and survival outcomes were evaluated by the Kaplan-Meier test and the log rank test for comparisons of categorical predictor variables. All analyses were performed by StatSoft software, version 6.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 CONCLUSION
 REFERENCES
 
Patient Population
The 72 patients identified had a mean age of 52 years (range, 20–79 years). Sex distribution was nearly equal (51% male). The median follow-up for all patients was 40 months (range, 5–119 months). Forty-five (63%) of 72 patients were treated for primary disease. Preoperative staging of the 45 primary lesions with imaging by EUS, CT, or MRI revealed 13 T3 and 32 T4 tumors. Of the 13 T3 lesions, 4 were fixed to adjacent structures on preoperative examination. The remaining nine T3 lesions had close or questionable invasion of adjacent structures anteriorly or laterally on preoperative imaging, and all nine of those patients went on to have PPE.

Preoperative chemoradiation was administered to 61 (85%) of 72 patients. The median preoperative radiation dose was 45 Gy (range, 36–67.2 Gy). Concurrent chemotherapy was 5-fluorouracil, either as infused 5-fluorouracil or capecitabine. Thirty patients received either continuous 5-fluorouracil or bolus dosing; the other 31 patients received capecitabine as part of the chemoradiation regimen. Only one patient received more than 56 Gy, and this patient had received this dose at an outside facility before evaluation and treatment at the M. D. Anderson Cancer Center.

Most patients with primary disease (55%) underwent PPE, and most patients treated for recurrent disease (70%) underwent TPE. This difference of operative strategies between patients with primary LARC and those with recurrent LARC reached statistical significance (P = .01).

Reconstruction of the pelvic and/or perineal defect required the use of a myocutaneous flap in 29 patients (40%). Where possible, an omental pedicle flap was used (53%, n = 38; Table 2Go).


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  		TABLE 2. Clinicopathologic characteristics among 72 patients with locally advanced rectal carcinoma who underwent exenterative surgery
 
IORT was administered to 22 patients (31%), 14 of whom had primary tumors and 8 of whom had recurrent disease. The IORT dose administered was either 10 Gy or 15 Gy, depending on the previous radiation dose. All were treated with IORT because of concern for close and/or involved radial margins.

Pathologically negative margins (R0 resection) were achieved in 65 (90%) of 72 patients. The remaining seven patients (10%) had a microscopically positive margin (R1 resection). Of the 65 patients with an R0 resection, 44 patients had primary disease and 21 patients had recurrent disease. Four of the seven patients with an R1 resection had recurrent disease.

Complications
The overall rate of complications was 43% (Table 3Go). Neoadjuvant chemoradiotherapy (CRT) had no observable effect on postoperative complication rates (42% after CRT, 47% without CRT, P = NS). There was also no statistically significant difference in the occurrence of a complication between patients who had undergone resection for primary tumors and those who had undergone resection for recurrent disease (47% vs. 37%, respectively; P = NS). The extent of resection had no statistically significant effect on the complication rates (TPE, 47%; PPE, 42%; SLE, 36%; P = 1.0). The type of pelvic defect reconstruction also had no significant effect on complication rates (omental, 30%; myocutaneous, 46%; no reconstruction, 75%; P = NS). Similarly, the use of IORT did not affect the complication rates (41% with IORT, 44% without IORT, P = NS). No additional factors (age, sex, pathologic margin) had any significant effect on the complication rate (data not shown).


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  		TABLE 3. Complications of pelvic exenteration among 72 patients with locally advanced rectal carcinoma
 
The most common complication was small bowel obstruction (SBO) (Table 3Go), but only 3 of the 11 patients required laparotomy. All reoperations for SBO occurred >30 days after the exenterative surgery. Half of the SBOs occurred in the group of patients who had received no reconstructive flap, representing 42% of the patients in the no-flap group (5 of 12). All except one of the intra-abdominal and pelvic abscesses were drained percutaneously.

Major complications, defined as those requiring additional operation or a prolonged hospital stay of >20 days, occurred in 18% of the total group and are listed in Table 3Go. Six patients had major complications resulting in a prolonged hospital stay without reoperation; these were two cases each of enterocutaneous fistulae, respiratory failure with pneumonia, and urinary conduit leaks. Major complications in the perioperative period were associated with a prolonged median length of stay of 27 days compared with a median stay of 9 days for those patients without complications in the perioperative period (P < .001). No perioperative deaths occurred in this series of patients.

Survival
The 5-year overall survival rate was 48% for all patients. The 5-year overall survival was 65% among those with primary cancers compared with 22% among those with recurrent disease (P = .0007, Fig. 1Go). The 5-year disease-free survival (DFS) rate for all patients was 38%; it was 52% among those treated for primary cancers compared with 13% among those treated for recurrent cancers (P < .01, Fig. 2Go). The only factor found to be predictive of poor outcome was recurrent presentation (Fig. 1Go). In evaluating the subgroup presenting with recurrent LARC, no specific clinicopathologic factor was able to determine worse outcome (data not shown).


Figure 1
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  		FIG. 1. Kaplan-Meier curves showing overall survival in patients with primary locally advanced rectal adenocarcinoma (LARC) versus patients with recurrent LARC after treatment with pelvic exenteration (P = .0007).

 

Figure 2
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  		FIG. 2. Kaplan-Meier curves showing disease-free survival (DFS) in patients with primary locally advanced rectal carcinoma (LARC) versus patients with recurrent LARC after treatment with pelvic exenteration (P < .01).

 
The recurrence patterns for primary and recurrent LARC are shown in Table 4Go. Pelvic exenteration provided local control for 67% of the entire cohort of patients. Five of the 72 patients (7%) had local recurrence alone, 19 (26%) had local recurrence and distant disease, and 14 (19%) had distant disease alone. The overall recurrence rate in patients treated for primary disease (44%) when compared with those treated for recurrent disease (67%) did not reach the level of statistical significance (P = .10).


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  		TABLE 4. Patterns of disease recurrence among 72 patients with LARC after exenterative surgery
 
The most common pattern of recurrence in patients treated for primary disease was distant metastases alone (50% of recurrences). In patients treated for recurrent disease, the most common recurrence pattern was concurrent local recurrence and distant metastases (72% of recurrences). No difference in 5-year DFS was noted with the use of neoadjuvant CRT (44 % 5-year DFS, n = 61; 48% 5-year DFS for patients without neoadjuvant CRT, n = 11; P = .70). Among patients with primary LARC, the 5-year DFS was 55% after neodajuvant CRT. Among patients with locally recurrent LARC, the 5-year DFS was 23% after neoadjuvant CRT (P = .003, vs. primary LARC). Eleven patients (seven with primary LARC and four with recurrent LARC) did not receive neoadjuvant CRT, and five of these patients experienced a recurrence (four with local component of recurrence). The use of neoadjuvant CRT seemed to improve local only recurrence (4.9% CRT vs. 18.2% no CRT, P = .20), but the difference did not achieve statistical significance.

Extent of resection was not a major factor in recurrence rates. The overall recurrence rate for patients who underwent TPE was 53%, for SLE was 36%, and for PPE was 62% (P = 1.0). Similarly, there was no statistically significant difference in the distribution of patients with any component of local recurrence (local recurrence alone, or local plus distant recurrence) between the different resection types (TPE 41%, SLE 7%, PPE 37%; P = .1).

Of the 22 patients who received IORT, four were alive without disease at the time of our data collection, and 18 had experienced recurrences. These recurrences after IORT had a local component in 10 cases (45%). IORT had no effect on DFS (P = .15).

Of the seven patients who had R1 resections, six were dead of disease at the time of our data collection. Four patients experienced early recurrence of disease and died of it in less than 12 months. The other two patients died at 37 and 48 months after their resection. All six of these patients had a component of local recurrence, but they died of sequelae of distant disease. The only surviving patient from the R1 resection group has had no recurrence at 40 months of follow-up.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
CONCLUSION
 REFERENCES
 
LARC remains a therapeutic challenge. Preoperative CRT has been successful in downstaging the rectal tumor’s T stage,3,13 but has not been demonstrated to provide uniform results in regional nodal tissues.14,15 As such, radical surgery is required to provide potentially curative therapy as well as local control of the tumor burden in the pelvis. The goal of radical surgery is to provide an en bloc resection of all involved organs and provide a margin-negative resection that can often only be achieved with pelvic exenteration.

In this series, we have demonstrated that pelvic exenteration for LARC results in good disease control (22% local recurrence component in primary LARC) and low operative mortality. Although the overall complication rate remains high (43%), it compares favorably with the results from other studies that describe patients undergoing a variety of pelvic operations.4,16,17 Most of these complications were not serious and were able to be managed without operative intervention, such as percutaneous drainage of pelvic fluid collections. Our zero mortality rate remains lower than that reported in most other series.7,18–20

Outcome
Two-thirds of the patients in our series had no evidence of local recurrence at their last follow-up visit. Recurrence confined to the pelvis was only found in only five patients (7%) after pelvic exenteration. An additional 26% of the patients had combined local and distant recurrence. Hafner et al.21 reported a locoregional recurrence as the first recurrence in 25% of 68 patients undergoing pelvic exenteration. Kakuda et al.19 reported a pelvic recurrence rate of 32% in 22 cases of pelvic exenteration for recurrent rectal carcinoma. Eighty-five percent of the patients in our series underwent neoadjuvant CRT. Even though there was no statistically significant difference in local-only recurrence rates with CRT in our study, the sample size of the patients who had not received CRT was too small to make a statistical impact (n = 11; 2 local-only recurrences).

The 5-year overall survival and DFS rates for primary LARC far surpass those for recurrent rectal adenocarcinoma requiring pelvic exenteration. The 5-and 10-year overall survival rates for this group were 65% and 38%, respectively (Fig. 2Go). Given the potential long-term benefit, pelvic exenteration for primary LARC should be pursued when indicated.

In patients with recurrent LARC, our 5-year DFS rate of 13% and 5-year overall survival rate of 22% compare favorably with those in other reports, in which overall survival ranges from 14% to 31%.7,16,21,22 In our series, the 2-year DFS rate is 35%, with an overall 2-year survival rate of 60% in patients treated for recurrent disease. No clinicopathologic factors were greatly predictive of worse outcome in this recurrent LARC group. With so few long-term survivors after a potentially debilitating resection, the use of pelvic exenteration in recurrent LARC demands careful patient selection.

Complications
SBO was the most frequent complication in our series, but it was managed without surgery in nearly 75% of these patients. Those cases of SBO that required operative intervention all occurred >30 days after exenteration. Two cases of obstruction were related to mesenteric nodal recurrence. The third case of obstruction that required surgery was due to adhesions. No radiation enteritis was encountered in these cases. Certainly advances in wound care, diagnostic imaging, and interventional radiology have benefited those patients with complications such as enteric fistulae and intrapelvic abscesses that in the past would have mandated surgical exploration.23–26

More than 80% of patients were deemed to have substantial pelvic defects requiring the use of autologous tissue flaps. A small group of patients (n = 12) did not receive any type of flap. There was no statistical difference in the complication rate between this group and that of patients who received flaps. One-third of these patients without flaps did present later with SBO, representing 50% of all SBO in this series. This suggests that use of autologous tissue flaps may play a role in preventing future SBO.

Perioperative Mortality
The perioperative mortality rate of 0% was unexpected. Given the extent of the operation and the median age of the patients with this diagnosis, we suspect that careful patient selection along with the supportive services available at a tertiary academic center played a role in our outcome. Mortality rates of >10% have been reported in the literature.7,8 Other contemporary series report mortality rates in the 5% range in relatively large numbers of pelvic exenteration patients—that is, more than 20.19,27,28 In contrast to the 30-year experience at the Roswell Park Cancer Institute, which reported a 6% perioperative mortality rate in 75 pelvic exenteration patients,17 our report reflects a more contemporary experience over 8 years. Thus, factors such as advances in anesthesia, cardiology, and critical care likely have had an effect on our study results.

These data lead us to believe that proper surgical planning and technique play important roles in determining the outcomes after pelvic exenteration. We believe that the surgeon should determine the patient’s resection status before institution of any therapy and then use a multidisciplinary approach to derive a treatment plan. This method requires not only multimodal therapy from the radiation oncologists and medical oncologists, but also multispecialty evaluation from urologists and plastic reconstructive surgeons. It is through this planning and multimodal therapy that the patient has the best opportunity to gain the benefits of a potentially curative approach while minimizing the morbidities of the extirpation.


   CONCLUSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
REFERENCES
 
Our results suggest that pelvic exenteration for LARC is safe and may provide durable local control. Although the morbidity rate remains high, the severity of these complications is by no means a prohibitive factor when considering pelvic exenteration as a therapeutic option. We were unable to elucidate any particular clinicopathologic factors that were predictive of poor outcome, other than recurrent disease. We conclude that patients with LARC warrant further study to ascertain which patients would experience maximal benefit with minimal morbidity from this radical surgery.

Received for publication November 15, 2006. Accepted for publication January 20, 2007.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 

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