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© 2001 American Society for Clinical Oncology Impact of Surgical and Pathologic Variables in Rectal Cancer: A United States Community and Cooperative Group ReportByFrom the Division of Colon and Rectal Surgery, Cancer Center Statistics Unit, and Division of Medical Oncology, Mayo Clinic and Mayo Foundation, Rochester, MN; University of North Carolina School of Medicine, Chapel Hill, NC; Cancer and Leukemia Group B, St Mary’s/Duluth Clinic Health System and Duluth Community Clinical Oncology Program, Duluth, MN; and University of Southern California, Los Angeles, CA. Address reprint requests to Heidi Nelson, MD, Mayo Clinic, Division of Colon and Rectal Surgery, 200 First St SW, Rochester, MN 55905; email: nelson.heidi{at}mayo.edu
PURPOSE: Substantial and successful effort has been focused on decreasing the risk of local failure after rectal cancer surgery through the use of adjuvant therapies. Our study examined data from studies conducted by United States cooperative groups to investigate the impact of surgical and pathologic variables in rectal cancer outcomes. PATIENTS AND METHODS: Surgical and pathologic reports from 673 patients with stage II/III rectal cancer enrolled onto three adjuvant clinical trials were reviewed for tumor and surgical variables. Additional information on individual institutions and operating surgeon was collected. Variables were tested for association with 5-year local recurrence and survival after adjustment for adjuvant treatments and other important prognostic factors.
RESULTS: Five-year local recurrence and survival rates were 16% and 59%, respectively. Surgeons treating more than 10 study cases had lower local recurrence rates than those treating CONCLUSION: Moderate variability in outcomes among surgeons was detected in this high-risk population. Efforts to improve surgical results will require changes in reporting practices to allow for more accurate assessment of the quality of surgery.
RECTAL CANCER IS an important disease not only because of the number of United States citizens afflicted each year (36,400 estimated new cases in 20001) but also because of the increasing complexity of the treatments available and the outcomes expected. Patient quality of life has been enhanced by attention to sphincter-preserving procedures. In addition, the use of adjuvant chemotherapy and radiation therapy has not only increased survival rates, but equally importantly, it has reduced the likelihood of locoregional recurrences.2 Because of the substantial end-of-life disabilities and bleak hope for salvage often created by pelvic recurrences,3 considerable effort has been placed on the prevention of such local failures in the United States. This effort has focused on the selective application of adjuvant therapies based on tumor-dependent variables that predict risk.4 What has not been standardized as a risk factor is the contribution of the treating surgeon. The individual surgeon as a predictor of risk has not been investigated in the United States despite reports from several countries in Europe and Canada demonstrating that the surgeon is a critical variable in rectal cancer outcomes. Various studies have quoted local recurrence rates ranging from 4% to 55%.5-9 It would seem discouraging to consider that one half of the patients may have tumor recurrence and suffer only because of surgeon-related factors, particularly without any opportunity to overcome such shortcomings. It has been well demonstrated that effective solutions can stem from recognition of this problem. For example, the implementation of an educational program in Germany reduced local recurrence rates from 39% to less than 10%.8 In the present era, as we continue to maximize multimodality treatment of rectal cancer, it seems essential to investigate and address all possible sources of variability. Furthermore, because the standardization of radiation10 and chemotherapy11 has improved the quality of care, it is timely to consider the same process for surgery, the primary modality of cure for rectal cancer. Thus, we examined the degree of surgical variability within a United States community-based clinical trials cooperative group. Simultaneously, we examined pathologic variables because poor outcomes can be related not only to the individual surgeon, but also to the biologic aggressiveness of the tumor.
Data for our retrospective study included patients previously accrued in three study protocols (79-47-51, 86-47-51, and 90-47-51/INT 0114) conducted by the North Central Cancer Treatment Group (NCCTG). The NCCTG is a community-based oncology cooperative group that includes 18 main member institutions and approximately 200 treating institutions located primarily in the United States Midwest. The medical records of 673 patients already included in three previously published prospective randomized trials12-14 were analyzed. All patients had undergone surgical treatment with curative intent for stage II and III rectal adenocarcinomas and had received postoperative radiation therapy, with a total radiation dose between 45 Gy and 54 Gy. Location of the inferior tumor edge at or below the sacral promontory or within 12 cm from the anal verge was requisite to define rectal cancer. Technical details about radiation treatments have been reported elsewhere.12-14 The above-mentioned trials were designed to test the efficacy of various adjuvant chemotherapy regimens. In particular, NCCTG study 79-47-51 evaluated the effect of fluorouracil and semustine and was open between 1979 and 1986.12 NCCTG study 86-47-51 was a controlled evaluation of adjuvant protracted infusion of fluorouracil as a radiation enhancer and fluorouracil plus semustine. This study was active from 1987 to 1990.13 Protocol 90-47-51 analyzed the effect of leucovorin versus levamisole in addition to fluorouracil and enrolled patients between 1990 and 1992.14 Both protocols 86-47-51 and 90-47-51 were multicooperative group studies completed by the Gastrointestinal Intergroup. Only those patients entered by NCCTG members are included in this analysis. All NCCTG patients enrolled onto these three studies are included in this analysis. For each patient, the operating surgeon with his/her NCCTG membership status and the treating institution were identified. Various biologic and surgical variables, that is, tumor characteristics and surgical techniques, respectively, were retrieved from the original operative and pathologic reports and reviewed by the first author. Biologic variables included T and N classification, extent of the radial spread of the tumor into the perirectal fat (in millimeters), and the incidence of tumor adherence to adjacent organs or structures. Nodal status was recorded with respect to the total number of lymph nodes retrieved and the number and percentage of nodes positive for disease (positive nodes). Technical variables included the type of procedure performed (anterior resection v abdominoperineal resection), length of the resected specimen and the distal resection margins (in centimeters), incidence of intraoperative inadvertent perforation of the rectum, and radial-free margins (in millimeters). For local adherence of the primary tumor, the type of surgical management was noted (en bloc resection of the rectum and the adjacent structure v dissection of the area of adherence). The primary and secondary end points for our study were local tumor recurrence and overall survival, respectively. Follow-up with periodic endoscopy was conducted quarterly for the first 18 months and annually or semiannually thereafter, as detailed previously.12-14
Statistical Analysis
The overall 5-year local recurrence and survival rates were 16% and 59%, respectively. Study patients were treated by 339 surgeons in 152 different institutions. Ninety-six institutions treated only one patient each, and thirty-one institutions treated between two and four patients each. Eighteen institutions provided between five and 20 patients, and only seven institutions provided more than 20. No association was observed between institutional contribution to the trials and cancer outcome (Table 1). However, patients treated by surgeons with more cases entered onto the studies had a lower local recurrence rate than those treated by surgeons with fewer (P = .025). For example, the local recurrence rate in patients treated by surgeons with more than 10 cases entered onto the studies was 11%, and the rate in patients treated by surgeons with 10 or fewer cases entered onto the studies was 17%. (Table 1, Fig 1). Among the high-volume surgeons (> 10 patients), there were no significant differences for local recurrence or survival rates. This effect remained significant at P < .01 after adjustment for patient T and N classification. NCCTG members treated 123 patients (18%), compared with 548 treated by nonmembers (81%). Membership status was unknown for two patients. NCCTG membership did not correlate with cancer outcome. The respective local recurrence rates for members and nonmembers were 15% and 16%, respectively, (P = .66) and the overall survival rates were 61% and 59%, respectively (P = .49).
Analysis for T and N status, after adjusting for the adjuvant treatment received, indicated both T and N stage as independent predictors for overall survival (P < .001 for both T and N). However, in this select high-risk population, only N stage was associated with the local recurrence rate. In patients with T2 disease, nodal classification was not associated with any variation in cancer outcome. Nodal classification correlated with both outcome measures in patients with T3 disease (Table 5). Among patients with node-negative disease (negative nodes), only T3, N0 satisfied the criteria to enter the trials, and this group had a 10% local recurrence rate and 71% overall survival rate.
The type of procedure performed, distal resection margins, and inadvertent intraoperative perforation of the rectum were all nonsignificant technical variables, despite 15% of the anterior resections having distal margins of less than 1 cm (Table 2). Inadvertent rectal perforation was reported in only 33 patients (5%), and although it showed a trend, it did not show a difference in cancer outcomes sufficient to reach statistical significance. The length of resected bowel did not correlate with local recurrence rates. The effect of local tumor growth was assessed through the analyses of local adherence and radial extent of the tumor (Tables 3 and 4). Tumor adherence to adjacent structures was encountered in 79 patients (12%) and was associated with a significant increase in local recurrence and decrease in overall survival rate (P < .001). However, treatment of such cases with en bloc resection did not significantly affect cancer outcome when compared with that of patients who had dissection of the area of adherence. Both tumor spread and tumor-free radial margins were reported suboptimally. Tumor spread into the perirectal fat was assessed in 138 patients (21%) and radial free margins were measured in 215 patients (32%). The analysis of the available data indicated that the former was unrelated to cancer outcome. In contrast, radial free margins were significantly correlated with local recurrence (Fig 2) but not with overall survival. In particular, a free radial margin of less than 1 mm was associated with a 25% local recurrence rate, whereas more than 1 cm of free radial margin resulted in a 3% local recurrence rate (P = .01).
Between zero and 56 nodes were retrieved and analyzed. For 23 patients (3.4%), the pathologic report did not mention lymph node examination or did not specify the number of lymph nodes retrieved. In addition, eight patients (1.2%) had no lymph nodes found at pathologic examination (Fig 3). Although 18% of patients had four or fewer nodes examined and 68% had fewer than 12, the number of lymph nodes retrieved did not correlate with local recurrence or overall survival.
On univariate analysis, the number and percentage of positive lymph nodes correlated with local recurrence and overall survival. However, on multivariate analysis, although both were independent factors predictive of overall survival, only the percentage of positive nodes, not the number, was independently predictive of local recurrence (Tables 6 and 7).
There are two striking but affirming results from our study: (1) the overall rate of local recurrence was low considering this high-risk population, and (2) the degree of surgeon variability was relatively modest. Several contemporary series of patients with curable rectal cancer treated with surgery alone report local recurrence rates of less than 10% in nonselected populations17-22 even though rates in excess of 25% to 50% have often been reported.6,23-25 Because the NCCTG study population consisted only of high-risk patients (stage II to III disease) who received treatment in diverse community-based and cooperative group centers, the overall local recurrence rate of 16% was lower than anticipated, even considering that the patients had radiation therapy. The ability of radiation therapy to control locoregional disease is well established, and yet even with pelvic radiation, patients with high-risk disease often have locoregional recurrence rates of 20% to 30%.26,27 The application of adjuvant therapy undoubtedly decreased recurrence rates. It also likely decreased the degree of variation. Not unexpectedly, the only other report to demonstrate a narrow range of recurrence also included radiation treatment as a component of treatment.7 Even with radiation therapy, there is still clinically relevant variation, suggesting ample room for improvement. How can such improvement be accomplished? In Sweden, Canada, and several European centers, highly variable local recurrence rates have been attributed to lack of specialization. Only with focused and centralized efforts have rates and variation been reduced.8,9,18,28 In fact, results from our study, an inverse relationship between surgeon study participation and low local recurrence rates, suggest that such a strategy may have merit.29,30 Our data are limited, however, because overall patient volume of operating surgeons and information regarding degree of specialization were not examined. Also, the patient number is not sufficiently large to recommend the daunting task of implementing a program of practice restriction. This was never the intent of the study. Rather, the intent was to identify technical details within the operative and pathologic records that could suggest areas of improvement that could be implemented within cooperative groups. Results from the data contained within the operative and pathology notes were noteworthy for two findings: (1) the frequency of apparently suboptimal practices was higher than expected, and (2) classic technical factors did not correlate with cancer outcomes. Despite the low overall local recurrence rates, several variables demonstrated unanticipated results, including the frequency of a small number of lymph nodes retrieved, a short length of bowel resected, and narrow distal margins, and the high rate of tumor transection in the presence of adherence. For staging purposes, lymph nodes are removed at operation and examined histologically for the presence of metastases. Previous studies have documented the relative accuracy of staging according to the number of lymph nodes evaluated histologically, with a minimum of 12 or 13 negative nodes yielding the greatest degree of accuracy for identifying true node-negative disease.31,32 The College of American Pathologists Consensus Statement of 1999 has recommended that, if fewer than 12 nodes are found, additional visual enhancement techniques should be considered.33 Although investigations of high-risk rectal cancer typically only require the presence of node-positive or locally advanced (T3 or T4) disease, for the three NCCTG trials, 3.4% of patients had no report on lymph node status, 1.2% had no nodes examined, 18% had fewer than four nodes examined, and 65% had fewer than 12 nodes examined. The need to treat these patients cannot be challenged. However, the difficulty of assigning risk of recurrence must be compromised in the absence of full staging. Whether modifications in surgical techniques could improve these results without the assistance of pathology is doubtful. Evidence that surgical treatment itself did not meet typical oncologic ideals was indicated by the rate of tumor transection (51% of adherent tumors) and the rate of distal margins less than 1 cm (15%), especially because en bloc resection34 and margins of 1 to 2 cm35,36 are considered the standard. Therefore, the relationship between surgical techniques and oncologic outcomes was studied. Because classic surgical teachings emphasize en bloc resection, it was unexpected that results did not confirm a significant disadvantage for patients who had tumor transection (P = .88), especially considering that the presence of tumor adherence and narrow tumor-free margins was associated with high rates of local recurrence. Certainly, the data on en bloc resection suggest a clinical trend. Perhaps the findings are not statistically meaningful because of the small sample size. The standard tenets of surgery in this regard should not be challenged on the basis of these results; rather, larger studies should be performed. Another unanticipated finding was the 15% frequency of distal bowel margins of less than 1 cm. This may be explained by selection bias, that is, the greater tendency for patients to be enrolled onto an adjuvant trial when margins are narrow, either because it was a more challenging tumor or it was technically more difficult to accomplish wide margins. Regardless, the extent of distal margins did not correlate with outcome, perhaps because of the small sample size or, alternatively, the techniques of pathologic examination were not standardized.37,38 It became apparent to us that several technical variables were poorly documented in the records, including data specific for inadvertent bowel perforation, extent of radial spread, and radial tumor-free margins. Although these factors have been reported to influence rates of recurrence,9,39,40 they were documented infrequently—a problem of omission. Surgeons and pathologists need to work together to improve reporting of these crucial factors, particularly for documentation of radial free margins as recommended in the College of the American Pathologists Consensus Statement 1999.33 The provocative findings specific to the ratio of the number of positive nodes relative to the number of nodes examined need to be considered. Our data, as expected, confirmed the inverse correlation between the number of positive lymph nodes and survival.20-22 What was not expected was the strong and significant direct correlation between the percentage of positive lymph nodes and local recurrence. Because inadequate resection of local nodal tissue (ie, mesorectal tissue) around the rectum influences local recurrence rates,20 we tested the possibility that the percentage of positive nodes predicted local failure. In fact, unlike survival data in which the percentage and number of positive nodes were both independently predictive, only the percentage of positive nodes was predictive for local recurrence on multivariate analysis. The concept that nodal disease contributes to locoregional failure is further substantiated by the data on recurrence and survival rates according to T and N classification. Whereas N was highly predictive of local recurrence and overall survival, T was only predictive of survival. As an example, data from our study and others confirm low local recurrence rates (10%) but only modest survival rates (71%) for T3, N0 lesions.41,42 The information on nodal disease and its correlation with survival and local failure have not only predictive value but surgical implications as well. These data support the concept that the better the nodal clearance (ie, the lower the percentage of positive nodes), the lower the risk of local relapse, suggesting a therapeutic role for lymphadenectomy. It is postulated that a high percentage of positive nodes indicates narrow nodal margins and a greater risk of residual disease and locoregional relapse. Previous efforts at radical lymphadenectomy have not proven effective for several reasons.43 Perhaps the use of sentinel node mapping with the selective application of extended lymphadenectomy will refine our understanding of the role of surgery in controlling locoregional nodal failures. In conclusion, moderate surgeon variability was detected, and suboptimal surgical practices and reporting were identified in a high-risk population of patients receiving multimodality therapy. Although outcomes no doubt could be improved with appropriate attention to reducing surgical variability, the information in current operative and pathologic reports is not sufficient to evaluate the quality of surgery. A novel finding of our study is the relationship of the percentage of positive nodes with survival and local recurrence. This not only is relevant for prognostic purposes but also suggests that further investigation into the role of surgery in nodal clearance is warranted.
Supported in part by grant no. CA-25224 from the National Cancer Institute.
Presented at the Thirty-Fifth Annual Meeting of the American Society of Clinical Oncology, Atlanta, GA, May 15-18, 1999, and available online (http://www.conference-cast.com/asco/lecture_frame.htm) and on CD-ROM.
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Copyright © 2001 by the American Society of Clinical Oncology, Online ISSN: 1527-7755. Print ISSN: 0732-183X
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ABSTRACT
INTRODUCTION
10 (11% v 17%, P = .02). Free radial margins also correlated with local recurrence (P = .01). Type of surgery, distal margins, and tumor radial spread were not significant. Tumor adherence to adjacent structures predicted local recurrence (35% v 14%, P < .001) and survival (30% v 63%, P < .001), regardless of en bloc resection. Although T and N classification predicted survival (P < .001), only N classification correlated with local recurrence. The number and percentage of positive nodes correlated with survival, but only the percentage independently predicted local recurrence. Several pathologic and surgical variables were reported suboptimally. 
