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Composite Pelvic Exenteration: Is It Worthwhile?

From the Department of Surgery, Division of Surgical Oncology (MJL), St. Elizabeth’s Medical Center and Tufts University School of Medicine, Boston, MA; and Colorectal Service, Surgical Oncology Department (PL-P), Centro Médico Nacional Siglo XXI, Instituto Mexicano del Seguro Social, México.

Correspondence: Address correspondence and reprint requests to: Marvin J. Lopez, MD, St. Elizabeth’s Medical Center of Boston, 736 Cambridge Street, CMPI, Boston, MA 02135–2997; Fax: 617-789-3433; E-mail: marvin_lopez_md{at}cchcs.org

	ABSTRACT

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Background: In locally advanced pelvic cancer, tumor fixation to the bony pelvis is regarded as unresectable and often inoperable. Few data exist regarding the futility or utility of pelvic exenteration with en bloc resection of involved portions of the bony pelvis.

Methods: Thirty-four of 625 patients undergoing radical pelvic procedures had an en bloc resection of pelvic organs with portions of the bony pelvis. There were 19 female and 15 male patients, and the median age was 59 years. Primary neoplasms included 19 rectal, 6 cervicouterine, 4 anal, 3 vaginal, 1 sarcoma, and 1 penile. All but three patients underwent preoperative pelvic irradiation. Pelvic exenterations were posterior in 7 patients, anterior in 3, supralevator in 3, and total in 21 patients. Pelvic bony resections included portions of the sacrum-coccyx in 18 patients, ischium in 5, pubic symphysis in 4, and ischial pubic rami in 4, and hemipelvectomy was performed in 3.

Results: Surgical morbidity occurred in 67.6% (23) of 24 patients. Median follow-up was 37 months. Pelvic or perineal tumor recurrence was concurrent with distant metastases in 9 patients (26.4%); 6 (17.6%) had only distant relapse, and 2 (5.8%) died with local recurrence alone. Overall cancer-related mortality rate was 50%. Five-year overall and cancer-specific survival rates were 44% and 52%, respectively.

Conclusions: Substantial survival can be accomplished for patients whose tumors are fixed to limited portions of the bony pelvis. These procedures are still associated with substantial morbidity, but operative mortality is infrequent.

Key Words: Anal canal cancer • Gynecological cancer • Radiotherapy • Pelvic exenteration • Rectal cancer

	INTRODUCTION

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Ultraradical surgery for treatment of regionally advanced tumors of the pelvis was developed in the 1940s and was influenced by advances in radical cancer surgery. Total pelvic exenteration entails en bloc removal of the rectum and anus, urinary bladder, internal genitalia, associated pelvic lymph nodes, and portions of the perineum. First described as a palliative procedure for recurrent cancer of the uterine cervix, total pelvic exenteration is currently indicated primarily for the cure of locally advanced but biologically favorable pelvic neoplasms.¹ During 50 years of evolution, this operation has become standard procedure in surgical oncology.² In recent decades, pelvic exenteration has been refined and appropriately modified. Patient selection has improved, as have morbidity and mortality rates, resulting in long-term survival rates that compare favorably with those of other radical oncologic procedures.^2–5

Early developments of the procedure focused on techniques to minimize blood loss and improve fecal and urinary diversion.^6,7 Subsequently, attention was directed toward appropriate patient selection on the basis of tumor factors, especially the biologic behavior of certain colorectal cancers that, although attaining considerable size, did not metastasize.⁸ The decades of the 1980s and 1990s witnessed refinements in surgical technique, resulting in modifications of pelvic exenteration and development of reconstructive techniques to fill the empty pelvis. Both are credited with reducing operative morbidity; consequently, indications for the procedure have become more liberal.^9–11

Traditional contraindications for pelvic exenteration include advanced age, major comorbidity or psychologic infirmity, extrapelvic metastasis, lymphatic or venous obstruction with lower-extremity edema, sacral plexus involvement, and tumor fixation to the bony pelvis.² However, owing to improvement in functional results and reduced mortality, some absolute contraindications have become less stringent. For instance, palliative pelvic exenteration in the presence of incurable disease has been advocated.¹¹ Encouraging results have been reported for sacral resection in the management of recurrent pelvic cancer.^12–17 However, data are lacking regarding the utility or futility of en bloc exenterative resections with portions of the bony pelvis. Brunschwig and Barber¹⁸ reported no cures among 28 patients undergoing composite pelvic exenteration. Yiu et al.¹⁹ reported a median survival of 49.2 months among surgically resected patients with rectal cancer and adjacent visceral involvement and a median survival of 13.2 months among those with pelvic wall involvement. The purpose of this report was to analyze the results of composite pelvic exenteration in a large, combined study of radical pelvic surgery.

	PATIENTS AND METHODS

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During the 22-year period from 1979 to 2001, 24 of 187 patients underwent radical pelvic surgery (performed by M. J. L.) involving pelvic bone resection en bloc with total or partial exenteration; the remaining 10 of 438 patients underwent composite pelvic exenteration at the Hospital de Oncología National Medical Center, in Mexico City, from 1994 to 2001. All patients underwent preoperative pelvic evaluation under anesthesia, including (when appropriate) cystoscopy and rigid or flexible sigmoidoscopy. All patients with rectal cancer had rectosigmoidoscopy or complete colonoscopy if possible. Preoperative chest x-rays and computed tomographic scans of the abdomen and pelvis were obtained in all cases. All patients were deemed to have tumors that were clinically fixed to limited portions of the pelvic bony structure.

Composite exenteration was the only form of treatment for three patients; two of them had rectal cancer and one had pelvic sarcoma. All remaining patients received definitive preoperative radiation therapy. In 11 patients, a prior surgical procedure had been performed elsewhere. Thirteen of the 19 patients with rectal cancer had prior resections, whereas 3 of 9 patients with gynecologic cancers had prior surgical treatment. In total, 17 patients underwent both surgery and radiation therapy before the composite exenterative procedure (Table 1). Follow-up was complete for all patients (mean and median follow-up of 56.1 months and 37 months, respectively).

Modified total pelvic exenteration was performed in 11 patients, preserving various portions of the genitourinary or gastrointestinal tract as indicated by the location and extent of the primary tumor. Urinary diversions in 26 patients who had anterior or total exenterations was performed with the ileal conduit method described by Bricker.⁶ All patients undergoing total pelvic exenteration had procedures done to fill the empty pelvis, including with omental pedicles alone (n = 14), omentum plus mesh reconstruction of the pelvic inlet (n = 4), and gracilis muscle myocutaneous flaps plus mesh (n = 3). All perineal incisions were closed primarily in two layers, and the pelvis was drained with closed-suction drains through the perineum in 23 patients. In eight patients the pelvis was packed with compresses moistened with Betadine (The Purdue Frederick Company, Norwalk, CT), which were removed on postoperative day 2 or 3, and in the remaining two patients a supralevator pelvic exenteration was performed (Table 2).

For composite pelvic exenterations, the area of limited tumor fixation to the bone is left intact until the perineal portion of the dissection is nearly completed. Thus, bony resection represents the last maneuver before the specimen is evacuated. In cases of anterior or lateral tumor fixation, perineal dissection is initiated in a direction opposite from the tumor fixation. For instance, in cases of tumor fixation to the symphysis of the pubis or to the pubic rami, dissection must begin posterolaterally, and the pelvis is then entered through a tumor-free space, dividing the inguinal ligament. The iliac vessels are mobilized laterally, and the pubic and ischial pubic rami and the symphysis of the pubis are divided with a Gigli or oscillating saw. Reconstruction is performed with the omental flap and Marlex mesh (Bard Cardiosurgery Division, Billerica, MA). In cases of ischium bone infiltration, perineal incision is continued on the midline of S1 or L5. Medial and lateral full-thickness flaps are formed from L5 to the ischial tuberosity. The gluteus maximus muscle is divided close to its origin in the sacrum, the sciatic nerve is mobilized laterally, and the insertions of the semitendinous, biceps femoris, and gemelli muscles are divided from the ischial tuberosity. The sacrotuberous ligament is divided and both rami of the ischium are transected with a Gigli or oscillating saw. The perineal defect is covered with the gluteus maximus muscles and the pelvis with the rectus abdominis or omental flap. After perineal soft tissue and musculature are divided, the levator ani is sacrificed circumferentially to the point of tumor fixation. The remaining levator and soft-tissue attachments are then divided and the specimen is delivered.

For tumors fixed to the sacrum and coccyx, it is critical to establish early in the course of the operation the proximal sacral extent of tumor involvement. Therefore, presacral space must be opened early and a tumor-free plane must be established to at least the S2 to S3 level. If proximal sacral involvement is evident, the tumor is considered unresectable.^21–23 A Kirschner wire is drilled through the midline of the sacrum at a point no less than 2 cm from the advancing edge of the tumor and driven through the intergluteal skin. This marks the site of posterior transection of the sacrum. After dissection of the entire pelvis, urinary diversion and a colostomy are completed, the abdomen and perineum are closed, and the patient is repositioned prone for the sacral part of the procedure. When total exenteration is being performed, the perineal incision is continued in a posterior direction to a point 2 to 3 cm cephalad from the Kirschner wire. When a posterior exenteration alone is required en bloc with sacral resection, the preferred incision is posterior sacral, with limbs curving around gluteal creases.¹⁴ After subcutaneous flaps are raised, the gluteus maximus and medius muscles are dissected from the sacrum. Sacrotuberous and sacrospinous ligaments are incised at their respective attachments to the ischial tuberosity and ischial spine. Sciatic nerves are located and protected and the pelvis is entered medial to sciatic nerves through the endopelvic fascia, and the sacrum is transected immediately above the marking pin, usually through S2 or S3.

	RESULTS

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Information regarding lymph node status was available for 25 patients: 17 with rectal cancer, 6 with cervical cancer, and 2 with anal canal. For the remaining nine patients, all of whom had been operated on previously elsewhere, outside pathology reports did not refer to lymph node status. Among the nine patients with rectal cancer whose lymph node status was known, seven had lymph node metastasis. There were no lymph node metastases in three of six patients with cancer of the cervix or in patients with sarcoma and recurrent anal, vaginal, or penile cancers, all of whom, with the exception of the patient with soft-tissue sarcoma, had prior definitive pelvic irradiation. Periosteal or cortical bone involvement was proven histologically in 32 of 34 patients; 9 of the specimens contained bone marrow tumor infiltration. The two exceptions were the patient with soft-tissue sarcoma of the pelvis, in whom the extent of the neoplasm precluded preservation of the hemipelvis, and one with recurrent rectal cancer. R0 surgical resection was performed in 30 patients, and the remaining 4 had microscopically involved resection margins (R1); none had macroscopically involved resection margins (R2).

Operating time ranged from 7 to 20 hours (average, 11.4 hours), and blood loss was 750 to 4250 mL (average, 1500 mL). Nine patients had no blood transfused. The 30-day hospital mortality rate was 0%. Complications of multiple abdominal and perineal fistulas occurred in one patient, who died 65 days after total pelvic exenteration. Complications developed in 23 patients (67.6%). Thirteen of 23 complications had an infectious origin, and these included 9 wound infections, 3 pelvic abscesses, and 1 case of pneumonia (Table 3). Reoperation to control sepsis, to reconstruct flap necrosis or sacral wound dehiscence, or to perform ureteroileal reanastomosis, was needed in nine patients.

Eight of 19 patients with rectal cancer had recurrent disease. Pelvic or perineal recurrence developed simultaneously with distant metastasis in five patients; in three patients, distant relapse occurred without local recurrence, and none had isolated local recurrence. All of these patients died of progressive metastatic disease.

Five of six patients with cervical cancer had recurrent disease. Three had combined recurrences (local and distant), one had isolated distant metastatic disease, and the remaining patient had an isolated pelvic recurrence. Two of these five patients are alive with metastatic disease 5 years postoperatively. Of four patients with anal canal cancer, two had a recurrence, one had an isolated distant recurrence, and one had an isolated pelvic and perineal recurrence. One of three patients with vaginal cancer had a combined recurrence, but the other two were alive at the 60-month and 204-month follow-up. The patient with soft-tissue sarcoma was tumor-free at 130 months, and the patient with penile squamous cell carcinoma had a distant metastasis. Overall treatment failure rate was 50% (17 of 34).

Fourteen patients were alive and free of disease at follow-ups ranging from 3 to 16 years. The remaining three patients died of non-cancer-related causes: one died of long-term surgical complications, one of myocardial infarction 2 years postoperatively, and one of a cerebral vascular accident 3 years after exenteration. Therefore, the 5-year survival rate was 44% and the 5-year cancer-specific survival rate was 52%, as is depicted in Fig. 1.

View larger version (18K): [in this window] [in a new window]   FIG. 1. Kaplan-Meier survival of 34 patients treated with composite pelvic exenteration.

	DISCUSSION

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION REFERENCES

 
Within the pelvic region, few neoplasms can be resected when they are locally advanced and fixed to bony portions; this fixation is extensive and frequently associated with distant metastases. Notable exceptions include patients with pelvic soft-tissue sarcomas for which hemipelvectomy is justified and selected patients with recurrent rectal adenocarcinomas invading the sacrum.^12–17 In nonvisceral sarcomas, adjacent visceral involvement is infrequent; therefore, exenterative surgery is seldom required. Conversely, in recurrent rectal cancer, posterior or total exenteration is usually needed to secure tumor-free surgical resection margins. The most frequent scenario is that a patient who is treated with low anterior resection or abdominoperineal resection later has tumor recurrence between the lower urinary tract and the sacrum (in men) or the vagina and the sacrum (in women).

Resection of pelvic organs with bony parts is a natural extension of pelvic exenteration, with reported 5-year survival rates of 30% to 40% among patients with locally advanced pelvic neoplasms.^{2–5,12–17} Early attempts at composite exenterations yielded poor results, with only four of 28 patients surviving 5 years or more. However, all eventually died of recurrent cancer.¹⁸ The current experience suggests that periosteal or cortical bone invasion per se is not a prognostically unfavorable factor. On the other hand, discontiguous or multiple pelvic bone metastasis, even if resectable, must be viewed as distant metastatic disease and as a contraindication to resection.²³ We have consistently opposed the use of pelvic exenteration as a palliative procedure because of its high associated morbidity and severe impact on the quality of life for the patient and the family.^2–5,21 This is particularly true when life expectancy is only a few months.

Indications, contraindications, and patient selection factors that apply to pelvic exenteration without bone resection are the same as those in which bone may need to be resected. As with other involved tissues where a 2-cm margin is sufficient, it is not necessary to remove full thickness of bone at point of fixation, but a segmental resection will ensure a tumor-free surgical resection margin. Marginal resection of bone without causing complete fracture may be sufficient to obtain a tumor-free margin. Therefore, substantial portions of pelvic bone can be resected without destabilizing the pelvic framework. In the present series, resections of pubic, ischiopubic, or ischial bone were segmental resections. No instances of osteomyelitis or osteoradionecrosis occurred.

This procedure, as with other ultraradical pelvic operations, is fraught with significant morbidity. In this series, morbidity did not seem to arise from the bony part of the resection, except in two cases in which dehiscence of posterior skin and subcutaneous tissue occurred after sacral resection. Tissue separation was probably due to insufficient soft-tissue mobilization to protect the cut end of the sacrum. Morbidity of pelvic exenteration has been well studied.^2–5,23 Pearlman²³ reviewed this subject and reported complication rates ranging from 18% to 50% for pelvic exenteration. When bone resections, particularly sacral resections, are included, the morbidity is likely to increase. Wanebo and associates¹⁴ reported 45 complications in 24 patients undergoing abdominosacral resection and extended exenterations. The scope of morbidity was similar to that in the present series and parallels that in our previous publications on this subject.^2–5,9 Blood loss can be substantial in these operations, with an average of 5000 to 6000 mL.^12,23,24 Average blood loss of 1500 mL in our series is attributed to the use of electrocautery throughout pelvic and perineal resection. Isolation and individual ligation of pelvic visceral vessels help control bleeding. Sacral transection can lead to brisk bleeding; therefore, this part of the procedure is performed immediately before removing the specimen. Liberal use of bone wax and hemostatic material also aids in minimizing blood loss.

There is a paucity of data regarding anterior or total exenteration with en bloc resection of ischiopubic or iliac bone.¹⁸ The use of hemipelvectomy, although well-established for treatment of advanced soft-tissue or bone sarcomas, has not been reported in combination with pelvic exenteration for locally advanced pelvic cancers. Lopes and associates¹³ recently reported a case in which a patient underwent internal hemipelvectomy for local pelvic recurrence after right colectomy, with a successful outcome. In the present study, a posttraumatic paraplegic patient with recurrent rectal cancer was treated elsewhere with extensive percutaneous drainage for multiple gluteal and ischiorectal rectal abscesses. Cytological examination of smear specimens from all draining sinuses revealed adenocarcinoma cells. Owing to the extensive intrapelvic and extrapelvic soft-tissue tumor invasion, hemipelvectomy with preservation of sacroiliac joint was performed.

In their report on the largest series of composite resections for posterior pelvic malignancy, Wanebo and associates¹² analyzed their experience with 76 patients. This series included 18 patients with musculoskeletal primary neoplasms and 58 with locally advanced recurrent pelvic (primarily anorectal) cancers. Overall mortality was 7.9%, whereas long-term estimated survival was 24% for rectal cancer and 22% for epidermoid carcinomas.¹² Pearlman and associates²⁴ reported 19 patients undergoing pelvic exenteration for locally advanced or recurrent anorectal cancer. Of this group, seven patients underwent sacropelvic exenteration. The local recurrence rate was 28%, and 53% of patients were living free of disease 12 to 53 months postoperatively.²⁴ Sugarbaker reported six patients treated with en bloc sacral resection for rectal adenocarcinoma. Four of six patients were alive during follow-up longer than 3 years.¹⁷

Patterns of recurrence have been studied for pelvic exenteration but are not clear for composite resections.^25,26 For rectal cancer and gynecologic malignancy treated by exenteration, the locoregional failure rate ranged from 30% to 50% for the former and 20% to 50% for the latter. Our local recurrence rate of 32% after composite pelvic exenteration is comparable to the 28% recurrence rate reported by Pearlman and associates.²⁴ Currently, information about the role of the decreasing local recurrence rate with the use of intraoperative radiotherapy is conflicting, but some groups advocate its use for patients with R1 resections.^27,28 Others have found no benefit.²⁹ On the basis of these patterns of recurrence, our group believes that the composite pelvic exenteration should not be considered a palliative operation, and therefore patients with bone marrow tumor infiltration, lymph node metastasis, or involved margins (R1 or R2) should be excluded from this extensive surgery.

The surgical literature supports the notion that training and technical expertise, along with a modicum of judgment, are the ingredients for a successful outcome of these procedures.^30,31 Although long-term freedom from disease is the primary purpose, functional results are imperative to extend quality of life. Bricker,⁶ a pioneer of radical pelvic surgery, emphasized nearly 50 years ago that "if we cannot leave a patient with a functional outcome compatible with a reasonable existence, we are not morally justified in performing this morbid procedure."

In conclusion, results of this combined series suggest that tumor fixation to limited portions of the bony pelvis is not a contraindication to resection. Substantial survival can be achieved for patients whose tumors are generally regarded as unresectable. However, these procedures are still associated with substantial morbidity, but operative mortality is infrequent.

	FOOTNOTES

 
Tumor fixation to the bony pelvis is not an absolute contraindication to resection. Overall cancer-related survival rate was 52% among 34 patients following en bloc resection of pelvic organs with portions of the bony pelvis.

Received for publication March 8, 2003. Accepted for publication September 22, 2003.

	REFERENCES

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Lopez, M. J. Articles by Luna-Pérez, P. Search for Related Content PubMed PubMed Citation Articles by Lopez, M. J. Articles by Luna-Pérez, P. Related Collections Surgery Radiation Therapy