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10.1245/ASO.2006.03.029
Annals of Surgical Oncology 13:347-352 (2006)
© 2006 Society of Surgical Oncology
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Original Article

Can Rectal Cancers With Pathologic T0 After Neoadjuvant Chemoradiation (ypT0) Be Treated by Transanal Excision Alone?

Hagit Tulchinsky, MD1,2, Micha Rabau, MD1,2, Einat Shacham-Shemueli, MD3, Gideon Goldman, MD1,2, Ravit Geva, MD3, Moshe Inbar, MD3, Joseph M. Klausner, MD2 and Arie Figer, MD3

1 Proctology Unit, Tel Aviv Sourasky Medical Center, 6 Weizman St., Tel Aviv, Israel 64239
2 Department of Surgery "B," Tel Aviv Sourasky Medical Center, 6 Weizman St., Tel Aviv, Israel 64239
3 Department of Oncology, Tel Aviv Sourasky Medical Center, 6 Weizman St., Tel Aviv, Israel 64239

Correspondence: Address correspondence and reprint requests to: Hagit Tulchinsky, MD; E-mail: hagitt{at}tasmc.health.gov.il.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Background: Patients with rectal cancer who have complete rectal wall tumor regression after neoadjuvant chemoradiation probably have eradication of tumor cells in the mesorectum as well, thus raising the possibility of transanal excision.

Methods: All pathology reports of all patients with locally advanced low and mid rectal cancer who underwent preoperative chemoradiation followed by radical resection from May 2000 to June 2004 were reviewed to evaluate the correlation between complete tumor response (ypT0) and nodal response.

Results: One hundred one consecutive patients had neoadjuvant chemoradiation followed by definitive operation. Four were excluded, leaving 64 men and 33 women (median age, 62 years). Fifty-three patients (55%) had mid rectal cancer, and 44 (45%) had low rectal cancer. Fifty-eight patients (60%) underwent low anterior resection, and 36 (37%) underwent abdominoperineal resection. In 17 patients (18%), no residual tumor cells were present within the rectal wall. One patient (6%) with ypT0 disease had positive lymph nodes.

Conclusions: No residual tumor in the rectal wall correlates with the absence of viable cancer cells in the mesorectal tissue (94%). Approximately 10% of T1 tumors have involved lymph nodes, and local excision is an accepted option. Transanal excision could probably be considered in a highly selected group of patients with a mural pathologic complete response to neoadjuvant therapy. This approach should be prospectively investigated, and strict selection guidelines should be used.

Key Words: Rectal adenocarcinoma • Pathologic complete response • Surgery • Local excision


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Preoperative chemoradiation is used in locally advanced low and mid rectal cancer. It has been shown to decrease tumor size and significantly reduce local recurrence,1–3 as well as to facilitate sphincter-saving procedures.4–6 Tumor response to chemoradiation ranges from no response to clinical (cCR) and pathologic complete response (pCR). The reported rate of pCR ranges between 4% and 44%.7–18

The standard therapy after neoadjuvant treatment entails definitive surgery either by low anterior resection (LAR) or by abdominoperineal resection (APR) with total mesorectal excision (TME) for all acceptable-risk patients, regardless of the tumor response. Since it was recognized that neoadjuvant chemoradiation may achieve pCR, data have been reported in support of the contention that surgery may be avoided and chemoradiation can be the definitive treatment in selected cases.19,20 Additional reports have recommended transanal local excision in lesions with a cCR to determine the rectal wall pathologic response. Radical surgery was avoided if no tumor cells were found.21–23 One major concern with local excision, however, is not knowing the status of the mesorectal lymph nodes. Our assumption was that patients who had a rectal wall pathologic complete tumor response to preoperative chemoradiation (ypT0; y indicating pathologic staging after radiation) might have a similar response in the mesorectal lymph nodes and, therefore, that local excision could be offered to these patients, thereby avoiding radical surgery.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
From May 2000 to June 2004, patients with biopsy-proven locally advanced low (at or below 5 cm from the anal verge) and mid (6–11 cm from the anal verge) rectal adenocarcinoma were treated in our department with curative intent by preoperative chemoradiation followed by definitive resection via either APR or LAR with TME. These patients were retrospectively identified from a computerized database.

Pretreatment evaluation included physical examination, colonoscopy, rigid proctoscopy, chest radiograph, abdominopelvic computed tomography, and endorectal ultrasonography (ERUS). Tumor staging and distance from the anal verge were established by taking into account the combined results of all modalities used. Tumors were staged according to the tumor-node-metastasis staging system. Locally advanced tumors were defined as T3, T4, or tethered T2 tumors with any N.

Chemotherapeutic regimens for all patients were 5-fluorouracil based. The dose of 5-fluorouracil was 180 mg/m2/day administered by a continuous infusion for 5 days per week for 5 weeks. Radiotherapy was administered 5 days per week for 5.5 weeks. The pelvic dose was 45 Gy with an addition of 180 cGy for 3 days as a boost to the tumor region (total, 50.4 Gy). Clinical response was assessed by physical examination and rigid rectoscopy 5 to 7 weeks after neoadjuvant therapy. ERUS was performed whenever possible to restage patients. Patients who had a rectal wall scar and no detectable tumor on rectal examination, rectoscopy, or ERUS were defined as having a cCR.

All patients underwent definitive surgery 6 to 8 weeks after completion of chemoradiation, regardless of the clinical response. Most operations were performed by surgeons with specialty training in colorectal surgery. All the medical records and pathologic reports were reviewed to identify patients with ypT0 and to evaluate the correlation between ypT0 and the mesorectal nodal response. A pCR was defined as the absence of viable tumor cells in the specimen. In cases for which only acellular pools of mucin were noted, the response was considered complete.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 CONCLUSIONS
 REFERENCES
 
One hundred one consecutive patients with locally advanced low and mid rectal cancer underwent preoperative chemoradiation followed by radical surgery with TME. Four patients were excluded from analysis because of liver metastases diagnosed before or during the operation, leaving a study population of 97 patients. There were 64 men (66%) and 33 women, with a median age of 62 years (range, 23–86 years). Patient and tumor characteristics and operative procedures are listed in Table 1Go. ERUS was performed in 87 patients (90%) before treatment. The tumor blocked the passage of the probe in three patients. All the study patients underwent operation with curative intent. Two had an R2 resection by a low Hartman’s procedure, and all others had an R0 resection. Thirty-three patients (34%) were assessed to have a cCR.


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  		TABLE 1. Patient characteristics
 
Table 2Go shows the distribution of the pathologic tumor staging for the entire study cohort. Tumor downstaging occurred in 44 patients (45%). Seventeen patients (18%) had no evidence of viable tumor cells in the rectal wall. The pCR rate among all patients, however, was 16% (16 of 97). One patient with ypT0 had mesenteric lymph node involvement: therefore, the positivity rate was 6% (1 of 17).


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  		TABLE 2. Pathologic staging
 
Three additional patients had microscopic foci of cancer cells in the rectal wall with no lymph node involvement. Lymph nodes harboring tumor were found in 28 (37%) of 75 patients with ypT2 and ypT3 tumors, ypT2N1 in 19% (5 of 26 ypT2), and ypT3N1 in 49% (23 of 47 ypT3) of patients. The median number of lymph nodes harvested and examined by the pathologist was 5 (range, 1–17) for the pCR group and 7 (range, 1–25) for the rest of the patients.

The mean follow-up was 25 months (median, 22.6 months; range, 6–56 months). Overall, seven patients (7%) developed local recurrence, eight (8%) developed metastatic disease, and two had a combination of local and distant recurrence. In the pCR group, no local recurrence occurred, and two patients were found to have lung metastases 10 and 12 months after surgery. There was no statistically significant difference in overall survival between the patients with a pCR to neoadjuvant therapy and those with residual disease.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
CONCLUSIONS
 REFERENCES
 
The standard surgical treatment of locally advanced low and mid rectal adenocarcinoma is LAR or APR with TME, according to tumor location. Surgical resection alone has high rates of locoregional failure.24 Serious consideration has been given to adjuvant therapy regimens over the past two decades. Postoperative chemoradiotherapy has been shown to improve local control and long-term survival as compared with surgery alone or surgery with radiation.25,26 Preoperative chemoradiation has potential advantages over postoperative therapy: it reduces the risk of small-bowel toxicity, it is delivered to an undisturbed tissue and vascular bed, and it has long-term functional advantages because it avoids neorectum radiation damage.27 Evidence has emerged from large clinical trials demonstrating tumor downstaging that increases the probability of tumor resectability and allows sphincter-saving surgery for patients who otherwise would have required permanent colostomy.1,3–6,28 A decrease in local recurrence rates and improved survival have been reported.29–32 Furthermore, neoadjuvant therapy may result in complete eradication of all viable tumor cells from the rectal wall and mesorectum, a condition known as pCR. The pCR rate of 16% in this study compares favorably to those from previous studies.7–18 As the use of preoperative therapy has broadened, more rectal cancers have resulted in cCR and pCR.

A pCR is considered by some authors as a favorable prognostic factor for improved local recurrence and disease-free survival.2,33–36 It may represent a subgroup of rectal cancers with better biological behavior. Theodoropoulos et al.34 reviewed 88 patients with uT3 and T4 low and mid rectal cancers. Those with a pCR were characterized by significantly better disease-free survival (P = .04), and the overall 5-year survival of patients with a pCR was 100%, compared with 82.5% of patients without a pCR (P=.08). Garcia-Aguilar et al.35 found a disease-free survival of 95.2% for 21 patients with a pCR versus 55.4% for 140 patients without a pCR (P = .03). Kaminsky-Forrett et al.36 evaluated the prognostic value of tumor downstaging and showed that the 3-and 5-year cancer-specific survival rates were 100% for ypT0N0 and ypT2N0, 89% and 68% for ypT3N0, and 64% and 0% for ypT2/3N1, respectively.

These lines of evidence raise several questions concerning the correct management of tumors that undergo a cCR to neoadjuvant therapy. Standard therapy entails proctectomy after neoadjuvant therapy by LAR or APR with TME to all acceptable-risk patients, regardless of the tumor response. Nevertheless, there are arguments that support less radical surgery.

First, APR and LAR with coloanal anastomosis, with or without a colonic J pouch and with or without diverting ileostomy or colostomy, are associated with significant morbidity, altered continence, and a less-than- perfect quality of life. Second, there are data to suggest that surgery may be avoided and that chemoradiation can be the definitive treatment in selected cases.19,20 Habr-Gama et al.20 suggested that a subset of patients with a cCR to preoperative radiation with or without chemotherapy might be spared surgery, with a 5-year overall and disease-free survival of 100% and 92%, respectively (the mean follow-up was 57.3 months). The argument against nonoperative treatment in these patients is that a cCR was found by some authors not to be an accurate predictor of a pCR.37,38 Hiotis et al.37 assessed the predictive value of a cCR in 488 patients. The cCR rate, as determined by digital rectal examination and proctoscopy or ERUS, was 19%, and of these patients, only 25% had a pCR. Third, full-thickness local excision has been offered to patients with distal rectal cancers that have been downstaged to less than T2 or those who have a cCR after neoadjuvant chemoradiation. 21,22,28,39,40 Kim et al.21 treated 22 complete clinical responders by full-thickness local excision, of which 17 (65%) were complete pathologic responders. After a mean follow-up of 24 months, none of the patients with a pCR had had recurrence. Mohiuddin et al.39 reported 15 patients who had T3 or >3-cm tumors that were downstaged with high-dose preoperative radiation and met the standard criteria for full-thickness local excision (tumor less than T2 and <3 cm). The reported 5-year survival rate was 88%, and the local recurrence rate was 0%. Schell et al.22 reported on 11 patients with significant downstaging of their tumors who underwent transanal excision and were followed up for a median of 48 months. There were no local recurrences, and one patient (9%) developed pulmonary metastases. Other groups have reported similar results and also showed that local control and survival rates were comparable to those achieved with radical surgery.23,41 Bonnen et al.23 performed local excision in 26 patients, half because of patient refusal of APR. Fourteen patients (54%) had a pCR, and 35% had microscopic residual disease. Two local recurrences occurred at a mean follow-up of 46 months. The 5-year actuarial overall survival rates were 86% for the local excision group and 85% for the cCR group who underwent radical operation.

One major concern with local excision is the status of the mesorectal lymph nodes or mesorectal tumor deposits among patients with tumors downstaged to ypT0, which, in theory, may ultimately lead to locoregional recurrence. In this study, the rate of positive lymph nodes among ypT0 tumors was 6%. The numbers in the literature vary between 2% and 13%.38,42,43 Read et al.42 studied a group of 644 patients who underwent either neoadjuvant radiotherapy alone or chemoradiation and found a pCR in 41 of them (6%). Lymph nodes harboring metastatic tumor were found in only 1 (2%) of 42 ypT0 patients. Onaitis et al.38 reported 29 patients with a cCR who underwent resection: 19 specimens revealed a ypT0 response, and lymph node metastases were present in 2 (10%). Better predictors for mesorectal involvement, such as histopathologic and biochemical features of the tumor, and more reliable imaging methods should be examined to allow improved selection of patients for local excision and lower rates of local recurrence. A recent article by Bedrosian et al.44 demonstrated the compartmentalized breakdown of residual mesorectal disease in patients with T3 or T4 tumors who were downstaged to T2 or lower. Overall, 17% had residual extramural disease, of which 9% were patients with ypT0 tumors. Exclusion of poorly differentiated tumors had the greatest effect in this group: this reduced the incidence from 9% to 5%. The authors concluded that local excision should be recommended with caution, because better markers are still needed to identify the subgroup of patients with pCR who will benefit from limited surgical therapy.

As for early rectal cancer of the mid and distal rectum, local excision has been an accepted option, although up to 13% of T1 tumors have associated involved lymph nodes.45–47 In light of our findings and others in the literature, transanal excision could probably be considered in a highly selected group of patients.


   CONCLUSIONS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
REFERENCES
 
Our data indicate that nodal metastases are infrequent in patients with a mural tumor that shrinks to pT0 after neoadjuvant chemoradiotherapy. This selected group of patients could probably be considered for transanal excision. Strict selection guidelines, as well as large prospective clinical trials that compare the results of local excision and standard surgery, are needed before this treatment strategy is adopted.


   ACKNOWLEDGMENTS
 
The authors thank Esther Eshkol for editorial assistance.

Received for publication March 4, 2005. Accepted for publication September 8, 2005.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 

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