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Ann Surg. Nov 2001; 234(5): 633–640.
PMCID: PMC1422087

Preoperative Radiochemotherapy and Sphincter-Saving Resection for T3 Carcinomas of the Lower Third of the Rectum

Eric Rullier, MD,* Béatrice Goffre, MD,* Catherine Bonnel, MD, Frank Zerbib, MD, PhD, Michel Caudry, MD, and Jean Saric, MD*

Abstract

Objective

To evaluate the complications and oncologic and functional results of preoperative radiochemotherapy and sphincter-saving resection for T3 cancers of the lower third of the rectum.

Summary Background Data

Carcinomas of the lower third of the rectum (i.e., located at or below 6 cm from the anal verge) are usually treated by abdominoperineal resection, especially for T3 lesions. Few data are available evaluating concomitant chemotherapy with preoperative radiotherapy for increasing sphincter-saving resection in low rectal cancer.

Methods

Between 1995 and 1999, 43 patients underwent preoperative radiochemotherapy with conservative surgery for a low rectal tumor located a mean of 4.5 cm from the anal verge (range 2–6); 70% of the lesions were less than 2 cm from the anal sphincter. There were 40 T3 and 3 T4 tumors. Patients received preoperative radiotherapy with a mean dose of 50 Gy (range 40–54) and concomitant chemotherapy with 5-FU in continuous infusion (n = 36) or bolus (n = 7). Sphincter- saving resection was performed 6 weeks after treatment, in 25 patients by using intersphincteric resection. Coloanal anastomoses were associated with a colonic pouch in 86% of the patients, and all patients had a protecting stoma.

Results

There were no deaths related to preoperative radiochemotherapy and surgery. Acute toxicity was mainly due to diarrhea, with 54% of grade 1 to 2. Four anastomotic fistulas and two pelvic hematomas occurred; all patients but one had closure of the stoma. Distal and radial surgical margins were respectively 23 ± 8 mm (range 10–40) and 8 ± 4 mm (range 1–20) and were negative in 98% of the patients. Downstaging (pT0–2N0) was observed in 42% of the patients (18/43) and was associated with a greater radial margin (10 vs. 6 mm;P = .02). After a median follow-up of 30 months, the rate of local recurrence was 2% (1/43), and four patients had distal metastases. Overall and disease-free survival rates were both 85% at 3 years. Functional results were good (Kirwan continence I, II) in 79% of the available patients (n = 37). They were slightly altered by intersphincteric resection (57 vs. 75% of perfect continence; NS) but were significantly improved by a colonic pouch (74 vs. 16%;P = .01).

Conclusions

These results suggest that preoperative radiochemotherapy allowed sphincter-saving resection to be performed with good local control and good functional results in patients with T3 low rectal cancers that would have required abdominoperineal resection in most instances.

Carcinomas of the rectum infiltrating the muscular layer and the perirectal adipose tissue and located in the lower third of the rectum (i.e., T3 tumors within 6 cm of the anal verge [or anal margin]) are traditionally treated by abdominoperineal resection (APR). Indeed, local excision and sphincter-saving resection (SSR) are proposed only in patients with well-differentiated T1-T2 disease. For T3 disease, APR is justified by the difficulties of achieving radial and distal negative margins because of the narrow shape of the distal pelvis and the proximity of the tumor to the anal sphincter. To increase the rate of SSR procedures in rectal cancer, preoperative irradiation has been investigated. 1–8 However, no series specifically addressed the results of SSR procedures in T3 carcinomas of the lower third of the rectum. Moreover, few studies 3,7 have evaluated concomitant chemotherapy with preoperative radiotherapy to facilitate SSR.

The aim of this study was to evaluate the complications and oncologic and functional results of preoperative radiochemotherapy and SSR for T3 cancers of the lower third of the rectum. The originality of the present prospective study was to propose a standardized conservative treatment for patients with T3 low rectal carcinomas including preoperative radiochemotherapy and intersphincteric resection. At the beginning of the study, conservative surgery was proposed mainly for patients with lesions more than 3 cm from the anal verge. Because of the high rate of complications and inadequate functional results of anorectal reconstruction after APR, 9 we rapidly considered all patients with T3 low rectal carcinomas for conservative surgery, even if the internal anal sphincter was involved. Only tumors with fixation to pelvic side wall or genital organs (T4 tumors) and lesions with infiltration of the external anal sphincter or levator ani were excluded, except in some patients with metastases. The goals of this prospective multimodal approach were to achieve negative radial margins by using intensive neoadjuvant treatment combining high-dose radiotherapy and concomitant chemotherapy; to obtain negative distal margins by using intersphincteric resection for very low tumors; and to obtain a local recurrence rate of less than 5% if surgical margins were negative.

PATIENTS AND METHODS

Patients

From 1995 to 1999, 118 patients with T3-T4 rectal carcinomas treated by preoperative radiation with concomitant chemotherapy were recorded in our computerized database. Sixty patients had a tumor in the lower third of the rectum (2–6 cm from the anal verge): 43 underwent SSR and 17 APR. Abdominoperineal resection was performed mainly for T4 disease (n = 6) or T3 at 2 to 3 cm from the anal verge (n = 9); two patients who underwent surgery at the beginning of our experience underwent APR for T3 lesions more than 3 cm from the anal verge. The rate of SSR was 72% (43/60): it was 78% (40/51) for all T3 tumors and 94% (32/34) for T3 rectal cancers located more than 3 cm from the anal verge. The 43 patients who underwent SSR form the basis of this study.

Characteristics of patients are shown in Table 1. All patients were evaluated before radiation by the surgeon using digital examination with and without voluntary anal contraction. The mean lower edge of the tumor was 4.5 ± 1.4 cm (range 2–6) from the anal verge, or approximately 2.5 cm (range 0–4) from the dentate line. Seventy percent (30/43) of the patients had a tumor less than 2 cm from the anal ring, and some lesions infiltrated the internal anal sphincter. Evaluation included endorectal ultrasound, abdominal and pelvic computed tomography scanning, chest radiography, carcinoembryonic antigen measurement, colonoscopy, and biopsy. All the patients had a proven adenocarcinoma of the rectum. According to the TNM classification, there were 40 T3 lesions and 3 T4 (genital fixation); four patients had potentially resectable liver metastases (M1). T1 and T2 lesions were excluded from the study because, in our experience, the former are treated by local excision and the latter by rectal resection, both usually without neoadjuvant treatment.

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Table 1. PATIENT CHARACTERISTICS (n = 43)

Neoadjuvant and Adjuvant Treatments

Most patients (n = 37) were treated at Saint-André Hospital with a preoperative radiation dose of 44 Gy administered in fractions of 2 Gy during a 4.5-week period using four fields, megavoltage (18 MV), and the technique of virtual simulation. The superior border was at the L5–S1 junction, and the whole anal canal and the anal margin were included inferiorly. Lateral borders extended 1 cm beyond the bony pelvis, including the internal but not the external iliac vessels. The posterior border was at least 1 cm behind the anterior bony sacral margin. Then, a boost of 10 Gy was given using four reduced fields including tumor with a 2-cm margin. In the whole series, the mean tumor dose was 50 Gy (range 40–54).

All the patients received preoperative chemotherapy concomitant with radiotherapy using 5-fluorouracil (5-FU) in either a continuous infusion (400 mg/m2 per day for 21 days; n = 36) or a bolus (350 mg/m2 for 5 days during the first and the last week of irradiation; n = 7) with folinic acid.

In this series, 16 patients also received intraoperative radiotherapy of 15 Gy in a prospective trial. Thirty-seven patients received postoperative adjuvant chemotherapy with 5-FU and folinic acid for 6 months.

Surgical Procedure

Surgery was performed 6 weeks after preoperative treatment. A midline laparotomy was performed. The inferior mesenteric artery was divided at its origin, 1 cm from the aorta. The splenic flexure was mobilized and the descending colon was transected to remove the irradiated sigmoid. The rectum was dissected to the pelvic floor, removing the totality of the mesorectum and preserving the hypogastric plexus nerves.

In all the patients, conservative surgery was decided on before neoadjuvant treatment. Although preoperative radiochemotherapy was used, the surgical objective was to obtain a distal margin of at least 2 cm. In some patients with favorable pelvis who had a tumor 5 to 6 cm from the anal verge, when technically feasible, a low anterior resection was performed. A clamp was applied below the tumor and a stapled coloanal anastomosis was performed. In the other patients, especially those with a tumor less than 2 cm from the anal ring, intersphincteric resection was performed. 10 Transanal intersphincteric resection was started just below the dentate line for lesions 3.5 to 5 cm from the anal verge, and the upper half of the internal anal sphincter was removed. It was started 5 mm from the anal verge for lesions at or below 3 cm, and the whole of the internal sphincter was removed (Fig. 1). The level of transection of the internal sphincter was decided on before radiotherapy in all patients.

figure 8FF1
Figure. 1. Goals for conservative surgery for low rectal cancer using preoperative radiochemotherapy. (A) Low T3 rectal tumor before treatment presenting as a vegetative lesion infiltrating the extramuscular area. (B) Tumor after preoperative radiochemotherapy: ...

Details of surgical procedures are presented in Table 2. Intersphincteric resection was performed in 25 patients. Coloanal anastomoses were transanal manual in 32 patients and stapled in 11 patients. The mean distance of the anastomosis from the anal verge was 1.9 cm (range 0.5–4). A colonic J pouch was performed in 86% of the patients and a diverting loop ileostomy in all patients. Pelvic resection was considered as macroscopically complete in all patients. Two patients underwent posterior colpectomy and another one underwent partial prostatectomy for T4 lesions. Patients with synchronous liver metastases underwent hepatectomy (n = 2) and definitive palliative chemotherapy (n = 2).

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Table 2. SURGICAL TREATMENT (n = 43)

Assessment

After the end of treatment, patients were enrolled in a follow-up program that included clinical, laboratory (carcinoembryonic antigen), and radiologic (abdominal and pelvic computed tomography scanning, chest radiography) investigations every 6 months. Colonoscopy was performed 1 year after surgery, then every 3 years. No patient was lost to follow-up, and the median follow-up was 30 months (range 7–69).

Local recurrence was defined as any recurrence diagnosed or suspected in the pelvis (tumor bed, pelvic nodes, anastomosis, drain site, or perineum) occurring alone or with other sites of recurrence. The Kaplan-Meier method was used to estimate the overall and disease-free survival rates. Time to last follow-up evaluation, treatment failure, or death was measured from the date of initiation of radiation therapy.

Functional results after coloanal anastomoses were assessed by an independent observer (B.G.) using a standardized questionnaire. Continence was evaluated using the score of Kirwan et al. 11 Patients with occasional mucus leakage occurring with or without flatus incontinence, but without any stool leakage, were considered to be stage 2.

RESULTS

Complications

There were no deaths related to preoperative radiochemotherapy or surgery. All patients finished the planned course of radiotherapy. The acute toxicity of preoperative radiochemotherapy was evaluated in a homogeneous group of patients who were treated at Saint-Andre Hospital and received 5-FU in continuous infusion. The incidence of acute toxicity is shown in Table 3. There was no hematologic toxicity. The most common acute toxicity was diarrhea, occurring in 54% of the patients, all but one grade 1 or 2. No patient required hospital admission because of acute toxicity.

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Table 3. ACUTE TOXICITY OF PREOPERATIVE RADIOCHEMOTHERAPY (n = 33)

The median postoperative hospital stay was 16 days (range 8–57). Postoperative complications are presented in Table 4. Four patients had anastomotic fistula; two of them needed transvaginal repair for rectovaginal fistula. Pelvic hemorrhage occurred in two patients, requiring in one patient definitive colostomy for colonic necrosis resulting from massive colonic pouch hematoma. All patients but one had closure of the stoma.

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Table 4. POSTOPERATIVE COMPLICATIONS

Late toxicity occurred only in patients who received intraoperative radiotherapy: three patients had sensory neuropathy requiring daily narcotics and one patient needed surgery to treat partial sacral necrosis. No patient had small bowel obstruction, ureteral stenosis, or urinary incontinence.

Downstaging and Surgical Margins

After preoperative radiochemotherapy, all the tumors appeared as an ulcerative scar without any vegetative component. The mean tumor size in fresh specimens was 3.6 cm (range 1–12). The tumor was well differentiated in 5 patients, moderately differentiated in 27, and poorly differentiated in 3; 4 tumors had a colloid component, and 4 were sterilized. The mean distal margin, assessed in fresh specimens without traction, was 23 ± 8 mm (range 10–40). The mean radial margin, assessed microscopically on fixed and India ink-stained specimens, was 8 ± 4 mm (range 1–20). Both distal and radial margins were negative (>1 mm) in 98% of the patients (42/43); they were positive (≤1 mm) in one patient. This patient had a pT3N1 7-cm residual lesion located 6 cm from the anal verge.

After preoperative radiochemotherapy for T3 low rectal carcinomas, downstaging (defined as pT0–2N0 lesions) occurred in 42% of the patients (18/43). Complete and partial pathologic response rates were respectively 9% (4 pT0N0) and 33% (4 pT1N0, 10 pT2N0). Three additional patients (7%) had tumor downstaging without nodal downstaging (2 pT2N1, 1 pT2N2), giving an overall tumor downstaging rate of 49%. Patients with downstaging had a greater radial margin than those without downstaging: 10 versus 6 mm (P = .02; Mann-Whitney test).

Local Control and Survival

After a median follow-up of 30 months, the rate of local recurrence was 2% (1/43). One patient who had a T3N1 lesion 5 cm from the anal verge and who was treated by 40 Gy with a 5-FU bolus (without downstaging) had anterior pelvic recurrence 22 months after low anterior resection. Local control was achieved by pelvic exenteration. Pulmonary metastases occurred 24 months later and were treated by chemotherapy; the patient was alive 5 years after primary treatment. None of the patients who received high-dose preoperative radiation with 5-FU in a continuous infusion and underwent intersphincteric resection had local failure.

Distal recurrence occurred in four patients: two had liver metastases treated by hepatectomy and two had pulmonary metastases treated by chemotherapy. One patient with liver cirrhosis underwent hepatectomy for hepatocarcinoma 18 months after treatment of rectal cancer. The 3-year overall and disease-free survival rates were both 85% (Fig. 2).

figure 8FF2
Figure 2. Overall survival after preoperative radiochemotherapy and sphincter-saving resection for T3 low rectal carcinomas (n = 43).

Among the patients treated by APR during the same period, two patients with T4 lesions and respectively R1 (microscopic) and R2 (macroscopic pelvic residual disease) had local recurrence. Overall, during the study period, the rate of local recurrence after preoperative radiochemotherapy and rectal resection (with or without SSR) for carcinomas of the lower third of the rectum was 5% (3/60).

Functional Results

Functional results of coloanal anastomoses after preoperative radiochemotherapy were assessed in 37 patients who had ileostomy closure with more than 1 year of follow-up (Table 5). The median stool frequency per 24 hours was 2.5 (range 0.5–5). Seventeen patients (46%) had fragmentation of stools and six (16%) experienced urgency. Three patients with a pouch needed enemas for difficulty in evacuating. Seventy-nine percent of the patients had good continence (65% perfect continence, 14% with flatus or mucus leakage), 16% had moderate incontinence (stool leakage once or twice a week), and 5% had major incontinence with stool leakage daily. Although functional results in terms of continence tended to be less satisfactory in the patients with intersphincteric resection (57% vs. 75% perfect continence), the difference was not significant (P = .31, Fisher exact test). However, functional results were significantly better in patients with a pouch coloanal anastomosis than after a straight anastomosis (74% vs. 16% perfect continence;P = .01).

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Table 5. FUNCTIONAL RESULTS

DISCUSSION

Our results showed that conservative surgical treatment was possible for patients with T3 carcinomas of the lower third of the rectum, with a low local recurrence rate and good functional results. Preoperative radiochemotherapy and intersphincteric resection enabled us to obtain negative radial and distal margins in 98% of patients. This high rate of negative margins correlates well with our 2% local recurrence rate and supports our initial hypotheses.

Several specialized groups have investigated SSR for low rectal cancer, with local recurrence rates ranging from 4% to 17%;1,2,5,6,12–16 however, most series included some T2 lesions and mainly tumors located 5 cm or more from the anal verge. In the current series, all the tumors were T3, confirmed by transrectal ultrasound, and 70% were less than 2 cm from the anal ring (<5 cm from the anal verge). Traditionally, most of these patients would have required APR. In our experience, using a multimodal approach, the rate of SSR for T3 tumors was 94% for lesions more than 3 cm from the anal verge and 78% for lesions 2 to 6 cm from the anal verge.

For most surgeons, the limits of SSR involve the technical possibility of obtaining a negative distal margin through the abdominal approach. For instance, Rouanet et al 2 performed APR if frozen sections of the resected specimen were positive, and Gouillat et al 8 did so if the distal margin was less than 1 cm. By using the abdominal approach, conservative surgery may be limited by bulky tumors (i.e., T3 lesions) and by a narrow android pelvis. Preoperative radiotherapy may be used in part to sterilize the distal intramural spread of the tumor to decrease the surgical distal margin. However, rectal transection can go through the tumor because it is often nonpalpable and difficult to assess after irradiation. Transanal intersphincteric resection is a technique that allows us to obtain sufficient distal margin in all patients, including those with lesions involving the internal anal sphincter. In our series, the mean distal margin was 2.3 cm; margins were negative in 98% of patients. Only one patient treated by low anterior resection (i.e., without intersphincteric resection) had positive distal margins. Intersphincteric resection requires the surgeon to decide on the exact level of transection of the internal anal sphincter from the anal verge before irradiation, after meticulous clinical, endoscopic, and radiologic assessment of the tumor. This is to avoid underestimating the irradiated tumor. Finally, if the technique of intersphincteric resection is used, the lower edge of the tumor should not be the limiting factor for SSR.

Involvement of the radial margin is the most important predictive factor for local recurrence after rectal cancer excision. 16–18 Achieving negative radial margins for carcinomas of the lower third of the rectum remains a challenge because, at this level, the mesorectum (i.e., the perirectal adipose tissue) is either thin or lacking. This should be the main contraindication for SSR in T3 low rectal tumors. Preoperative radiochemotherapy decreases the tumor volume, induces downstaging, and facilitates surgical resection (see Fig. 1). In addition, it transforms the vegetative component of the tumor into an ulcerative scar, and this may decrease intraoperative tumor seeding. We observed significant tumor regression, with a 42% rate of both tumor and nodal downstaging (pT0–2N0) and a 49% rate of tumor downstaging (pT0–2). This high rate of tumor regression, compared with the 18% to 26% reported after preoperative radiotherapy alone, 19,20 is similar to the 53% to 64% observed after preoperative radiotherapy potentiated by chemotherapy. 7,21,22 Using 5-FU in a continuous infusion, as in the series of Rich et al 21 and Janjan et al, 7 may improve tumor response compared with bolus 5-FU, as also suggested by a recent study. 23 In our series, the greater radial margin observed in patients with downstaging suggests that preoperative radiochemotherapy facilitated the achievement of negative radial margins. Indeed, the rate of positive radial margins after surgery alone for rectal cancer ranges from 12% to 27%, 17,24 whereas it was 2% in our series using preoperative radiochemotherapy. Combining the transabdominal approach with intersphincteric resection, making anatomic dissection easier, is probably another factor that contributed to achieving negative radial margins.

Most series studying the treatment of resectable low rectal cancer with the goal of sphincter preservation used preoperative radiotherapy alone with high-dose irradiation (>45 Gy) (Table 6). Surgery was performed 6 to 8 weeks after treatment to improve downstaging. 25 Therefore, during a period of 3 to 4 months between diagnosis of the disease and rectal resection, no treatment was given to prevent distal metastases, although adjuvant chemotherapy showed improving survival rates. 26,27 Adding chemotherapy to preoperative radiotherapy may improve both local control and distal disease. Indeed, the results of our series and results from other single institutions showed a local control rate of more than 90% and a survival rate of 60% to 80% using such multimodality regimens for T3 or T4 disease. 3,21,22,28–31

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Table 6. PREOPERATIVE RADIOTHERAPY FOR SPHINCTER-SAVING RESECTION IN LOW RECTAL CANCER

The rate of complications induced by preoperative radiochemotherapy is low. In our series, grade 3 toxicity occurred only for diarrhea in 2% of the patients, and no hematologic toxicity was recorded. These results are similar to the 1% rate of grade 3 diarrhea and the 6% rate of grade 3 hematologic toxicities reported by Rich et al, 21 who used 45 Gy and a concurrent continuous infusion of 5-FU for 5 weeks. Moreover, a continuous infusion of 5-FU appears to be well tolerated compared with bolus 5-FU or drug association. 3,22,28,29 Postoperative complications, especially anastomotic fistula (9%), did not require early postoperative reoperation, and all these patients had stoma closure. In our experience, the rate of anastomotic fistula was not higher after preoperative radiotherapy than after surgery alone. 32 Recently, Pucciarelli et al 33 showed that early postoperative complications of rectal cancer resection were not increased by preoperative chemotherapy; we also observed this in our series (unpublished data).

Although some authors have questioned the advantages of SSR for low rectal cancers in term of quality of life, 34 a permanent colostomy must be considered a serious handicap compared with coloanal anastomosis. Indeed, the results of coloanal anastomosis improved significantly during the past decade with the addition of a colonic pouch, because this decreases stool frequency, urgency, and incontinence. 35 Moreover, carrying out an anastomosis with unirradiated bowel by removing all the sigmoid colon may avoid the disappointing results reported in some trials using neoadjuvant treatment. 36 In our series, the splenic flexure was mobilized in all patients, all the sigmoid was systematically removed, and a pouch was performed in most patients. We believe that these standardized surgical issues have facilitated the achievement of good functional results. Technical aspects of preoperative radiation therapy, including the multiple-fields technique, short fractions, virtual simulation, and respect of the lower part of the anal sphincter in some patients with favorable disease, may also have contributed to the preservation of anal sphincter function. 37 In the current series, although intersphincteric resection was performed in 25 patients, 79% of the evaluable patients had good continence. In coloanal anastomoses, the lack of a significant difference in continence between patients with intersphincteric resection and those without was also reported by Gamagami et al, 38 who performed removal of the internal anal sphincter for conservative treatment of low rectal carcinoma. Perfect continence has been reported in 50% to 70% of patients after partial or total excision of the internal anal sphincter with or without a colonic pouch. 10,13,38–40

In conclusion, using a multimodal approach, conservative treatment was possible in patients with T3 carcinomas of the lower third of the rectum that would have required APR in most instances. Preoperative radiochemotherapy was associated with a low rate of complications and induced significant downstaging, which increased radial margins. Combining such a regimen with intersphincteric resection led to the achievement of distal and radial negative margins, allowing a low local recurrence rate. Functional results were not significantly altered by intersphincteric resection and were improved by adding a pouch to the coloanal anastomosis. These results suggest that T3 carcinomas of the lower third of the rectum are suitable for a conservative approach with neoadjuvant combined treatments and adapted surgical techniques, although the role of preoperative radiochemotherapy must be confirmed by a randomized controlled trial.

Acknowledgments

The authors thank Dr. G. Belleannée, Pr. A. de Mascarel, and Ms. Martre from the Department of Pathology, Haut-Lévèque Hospital, Bordeaux, France, for their contribution in prospective assessment of rectal specimens.

Footnotes

Correspondence: Eric Rullier, MD, Service de Chirurgie Digestive, Hôpital Saint-André, F-33075 Bordeaux, France.

E-mail: eric.rullier@chu-bordeaux.fr

Accepted for publication February 8, 2001.

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