Annals of Surgical Oncology 8:611-615 (2001)
© 2001 Society of Surgical Oncology
Adenocarcinoma of the Lower Third of the Rectum Surgically Treated With a <10-MM Distal Clearance: Preliminary Results in 35 N0 Patients
Salvatore Andreola, MD,
Ermanno Leo, MD,
Filiberto Belli, MD,
Giuliano Bonfanti, MD,
Grazia Sirizzotti, BSc,
Paolo Greco, MD,
Francesca Valvo, MD,
Gorana Tomasic, MD and
Gian Francesco Gallino, MD
From the Department of Pathology (SA, GS, GT), Division of Surgical Oncology B (EL, FB, GB, GFG), and Department of Radiotherapy (FV), Istituto Nazionale per lo Studio e la Cura dei Tumori, Milan, Italy; and the Department of Pathology (PG), Azienda Ospedaliera Ospedali Garibaldi, S.Luigi, S.Curro’, Ascoli-Tomaselli, Catania, Italy.
Correspondence: Address correspondence and reprint requests to: Dr. Salvatore Andreola, Anatomia Patologica, Istituto Nazionale Tumori, Via Venezian 1, 20133 Milano, Italy; Fax: 39-2-2390756; E-mail: gios{at}istitutotumori.mi.it
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ABSTRACT
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Background: Recent reports suggest that a distal clearance (DC) of 10 mm at the lower surgical margin may be considered adequate in the surgical treatment of rectal cancer, but there are no data on the possible adequacy of a <10-mm DC in N0 patients in whom a good prognosis can otherwise be expected, that is, those with negative surgical margins and negative lymph nodes.
Methods: Between November 1991 and December 1998, 154 consecutive patients with adenocarcinoma of the lower third of the rectum had a total rectal resection with total mesorectal excision and coloendoanal anastomosis. Among 76 N0 patients, there were 35 with <10-mm DC and 41 with 
10-mm DC. Each group was divided into two subgroups depending on whether the surgical margins were involved or not, and the rate of local recurrence in the various categories was compared. All B2 Astler-Coller stage patients in the series received postsurgical chemoradiotherapy.
Results: The local recurrence rate in the 35 patients with DC <10 mm was 11.4% and that of the 41 patients with DC 10 mm was 7.3%. When only patients with negative surgical margins were considered, the local recurrence rate was 3.4% for those with <10-mm DC and 5.1% for those with 10-mm DC.
Conclusions: Our results suggest that a radical surgery with <10-mm DC followed by chemoradiotherapy may be adequate in N0 patients, provided that a careful pathologic examination of the surgical specimen excludes the presence of lymph node metastases and that the distal rectal and mesorectal resection margins fall in healthy tissue.
Key Words: Rectal adenocarcinoma • Distal clearance • Local recurrence • Sphincter-saving surgery
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INTRODUCTION
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Sphincter-saving rectal surgery requires the determination of the optimal length of the distal resection margin. Traditionally, the shortest curative distal clearance (DC) has been said to be 2 cm from the outer edge of the tumor,1–8 but recent reports have suggested that a DC of 1 cm may be sufficient.9,10 The issue is crucial for N0 patients, in whom a limited tumor spread and a good prognosis are expected, and for whom the decision of performing a sphincter-saving resection is largely dependent on the expected DC length. Here we report our preliminary results on 35 N0 patients treated by total rectal resection with total mesorectal excision and coloendoanal anastomosis for adenocarcinoma of the lower one-third of the rectum in whom the DC was <10 mm.
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METHODS AND PATIENTS
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Between November 1991 and December 1998, 154 consecutive patients with adenocarcinoma of the lower one-third of the rectum had a total rectal resection with total mesorectal excision and coloendoanal anastomosis at the Istituto Nazionale per lo Studio e la Cura dei Tumori, Milan. All tumors were located between 4 and 5 cm from the anal verge. Patients were operated by the same surgical team (EL, FB, GFG), and all pathologic examinations were performed by the same pathologist (SA). Specimens were received unfixed, opened longitudinally, straightened without stretching, and pinned to a corkboard. The distance from the tumor to the distal resection margin was measured after fixation in 10% buffered formalin for 24 hours. The extent of distal intramural tumor spread (DITS) in the submucosa and/or muscularis propria was measured on the histologic slide, and the final DC was calculated by subtracting the extent of the DITS (if any) from the distance from the resection margin to the tumor as measured during the gross examination. The distal rectal resection margin and the circumferential resection margin of the mesorectum were examined in all cases, the latter by sampling a 1-mm thick slice of adipose tissue from the whole surface of this margin, In fact, we usually consider the circumferential resection margin positive when we find the tumor <1 mm from the margin.11 Cases in which either margin was involved by tumor were coded as margin-positive. Lymph nodes were search by manual dissection, as previously described.12,13
The pathologic stage for the entire series, defined according to the Astler-Coller system, was as follows: 30 (20%) stage B1; 47 (30%) stage B2 (for the total of 77 N0 patients); 13 (9%) stage C1; and 64 (41%) stage C2. The mean number of examined lymph nodes was 36 in stage B1 cases, 46 in stage B2, 37 in stage C1, and 42 in stage C2.
The 77 N0 patients were divided into two groups depending on DC length: 42 in which the DC was 10 mm (one of them was excluded because no clear information on his follow-up was obtained during the last control) and 35 in which the DC was <10 mm. The latter constitute the subject of this study. Following conventional current practice, all of these patients were offered an abdominoperineal resection, but they all refused it. All stage B2 patients received postoperative chemoradiotherapy. The median follow-up was 51 months, with a range of 20–100 months.
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RESULTS
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Analysis of the 35 cases with 
10-mm DC revealed that 10 of the tumors were stage B1 and 25 were stage B2. The mean DC length was 4.4 mm, with a median of 5.0 mm. (By comparison, the mean DC in the cases with 10-mm DC was 18.4 mm, and the median was 15.0 mm).
In three cases (all stage B1), the tumor was very close to the distal margin, but the exact DC could not be measured owing to laceration of the rectal wall developed during surgery; these cases were classified as "negative distal resection margin, DC not measurable" but < 10 mm (nm). Distal intramural spread was present in two B1 patients (3.2 and 3.4 mm, respectively), and four B2 patients (13.5, 3, 2.6, and 3 mm, respectively). Positive surgical margins were documented in 6 of 35 patients with <10-mm DC (5 in the rectal margin and 1 in the mesorectal margin). This is in contrast with 2 of 41 patients with 10-mm DC, both of which were in the mesorectal margin.
The overall local recurrence rate for N0 patients with <10-mm DC was 11.4% (4 of 35 patients), whereas that of the 41 patients with 10 mm was 7.3%. When only cases with negative surgical margins were considered, the recurrence rate was 3.4% in the cases with <10-mm DC (1 of 29) and 5.1% in cases with 10-mm DC.
When all N0 cases were evaluated, depending on the status of the surgical margins, it was found that the local recurrence rate was 60% in those with positive margins and 3.3% in those with negative margins. Of the four local recurrences in the group with <10-mm DC, two occurred in B1 patients (one died of unrelated disease; one is alive with no evidence of disease 9 months after a radical surgical resection of the recurrence) and two in B2 patients (one died of disease, one is alive with no evidence of disease 13 months after a radical surgical resection of the recurrence). Three patients (all stage B2) developed lung metastases; in two of them, tumor emboli had been found in the intramural blood vessels in the surgical specimens. No local recurrences were found in any of the six cases with distal intramural spread. The main pathologic features and follow-up of all the series are summarized in Tables 1, 2, 3, and 4.
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DISCUSSION
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The first problem in evaluating the DC length concerns the method employed to measure the distance from the distal resection margin to the tumor, because there is no agreement as to whether DC should be measured on the fresh specimen or after formalin fixation. Probably this dispute will never be solved, because there is no clear demonstration that one method is more reliable than the other. Under the circumstances, the best one can do is to standardize the procedure by having the patients operated on by a dedicated surgical team and the specimens examined by the same pathologist. Alas, this is usually possible only within a single institution. As a consequence, data from different studies are difficult to compare. In our study, we have chosen to measure the DC after fixing the specimens in formalin for 24 hours and handling them in exactly the same fashion. Technical issues aside, there are recent reports that consider acceptable a 1-cm DC for most rectal adenocarcinomas and maintain the feasibility of the sphincter-saving techniques in this group.9,10
In accordance with this view, our preliminary results seem to support that a <10 mm-DC in radical surgery associated with chemoradiotherapy may be adequate in patients without lymph node metastases provided that the distal resection margin of the rectum and the mesorectal resection margin fall in healthy tissue.
In our series, the local recurrence rate in patients with negative resection margins was 3.4% in <10-mm DC and 5.1% in 10-mm DC, suggesting that the DC length does not play a mayor role in the development of local recurrence. Conversely, the local recurrence rate for cases with positive versus negative margins was 60% and 3.3%, respectively, indicating that the presence of neoplastic foci at the distal resection margin of the rectum or on the mesorectal resection margin are ominous events predictive of a high risk of tumor recurrence which is difficult to control by a postoperative chemoradiotherapy approach. In margin-negative cases, postoperative chemoradiotherapy may be useful in sterilizing foci of tumor in N0 B2 patients, making the sphincter-saving technique feasible even with <10-mm DC, provided the pathologic staging has been sufficiently accurate. We think that the crucial factor in choosing the sphincter-saving technique (thus avoiding the resection of the anal sphincter in <10-mm DC cases) is the selection of patients who can be confidently regarded as being free of lymph node metastases. During the routine pathologic examination of the surgical specimen, it is very easy to miss small positive lymph nodes, thus leading to inclusion of patients with metastatic disease in the N0 group and thereby causing misinterpretation of the clinical results. This is so because the presence of metastatic lymph nodes is an indicator of a wide intrapelvic spread of tumor which can lead to local tumor recurrence regardless of the extent of the DC. Similarly, it is very important that the circumferential resection margin of the mesorectum be accurately examined, because tumor foci can be present in this area in a small percentage of N0 patients, who will have, as a result, a higher risk of tumor recurrence. Guided by these preliminary data, in our clinical practice we consider acceptable the risk of a sphincter-saving technique without subsequent resection of the anal sphincter in patients with <10-mm DC, but only if a high number of lymph nodes has been examined and if there is microscopically no tumor in the resection margin of the rectum and/or mesorectum. This is due to the assumption that these patients have a limited spread of the tumor and that they can benefit from postoperative chemoradiotherapy treatment.
The importance of the histologic examination of the resection margin is a major problem in oncologic surgery and has been repeatedly highlighted in various tumor types. In malignant colorectal polyps treated by endoscopic resection, histologic examination of the whole stalk of the polyp is mandatory to rule out the presence of tumor on the resection margin. In case of negative resection margin on the base of the stalk, the chances of tumor recurrence or of residual tumor in the intestinal wall is extremely low.14
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CONCLUSION
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In conclusion, our preliminary results suggest that patients with N0 adenocarcinoma of the lower third of the rectum can be adequately treated by the sphincter-saving resection and postoperative chemoradiotherapy without further resection of the anal sphincter, even if the DC is <10 mm, as long as the distal rectal and circumferential mesorectal resection margins fall in healthy tissue. Conversely, our data suggest that chemoradiotherapy has few chances of being successful in patients with positive surgical margins, even if the foci of involvement are only microscopic.
Received for publication December 12, 2000.
Accepted for publication January 22, 2001.
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ABSTRACT
INTRODUCTION
