© The Author 2006. Published by Oxford University Press.
ARTICLE |
Population-Based Assessment of the Surgical Management of Locally Advanced Colorectal Cancer
Affiliations of authors: Division of General Surgery (AG, NGC, AJS, CHLL), Institute for Clinical Evaluative Sciences (NGC, LR, CHLL), Toronto Sunnybrook Regional Cancer Centre (NGC, AJS, LR, CHLL), and Division of Surgical Oncology (NGC, AJS, CHLL), Sunnybrook Health Sciences Centre Department of Research Design and Biostatistics, Institute for Clinical Evaluative Sciences (AK), Department of Gastroenterology (LR), University of Toronto, Toronto, Canada
Correspondence to: Calvin H. L. Law, MD, MPH, FRCSC, Suite T2-001, 2075 Bayview Avenue, Toronto, Ontario, Canada M4N 3M5 (e-mail: calvin.law{at}sunnybrook.ca).
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ABSTRACT |
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Background: Evidence-based guidelines recommend multivisceral resection for patients with locally advanced adherent colorectal cancer because it reduces local recurrence and improves survival. However, this procedure can increase morbidity compared with standard resection and may not be practiced uniformly. We performed a population-based study to examine surgical practice and outcomes among patients with locally advanced adherent colorectal cancer in the United States. Methods: Patients who were 18 years or older and who had surgical resection for nonmetastatic, locally advanced adherent colorectal cancer from January 1, 1988, through December 31, 2002, were identified from the Surveillance, Epidemiology, and End Results (SEER) registry. Logistic regression was used to examine patient, tumor, and geographic factors associated with multivisceral resection. Cumulative early mortality (i.e., at 1 and 6 months after diagnosis) and 5-year survival were obtained from Kaplan–Meier estimates; adjusted risks of death were calculated using Cox proportional hazards models. All statistical tests were two-sided. Results: We identified 8380 patients who underwent surgical resection for locally advanced adherent colorectal cancer, of whom 33.3% were managed with multivisceral resection. Among colon cancer patients, younger age at diagnosis, female sex, SEER region, node negativity, and left-sided tumors were independently associated with having had a multivisceral resection. Among rectal cancer patients, younger age at diagnosis and female sex were positively and statistically significantly associated with multivisceral resection, whereas receipt of neoadjuvant radiation was inversely and statistically significantly associated with multivisceral resection. Compared with standard resection, multivisceral resection was associated with improved overall survival for patients with colon (hazard ratio [HR] = 0.89, 95% confidence interval [CI] = 0.83 to 0.96) and rectal (HR = 0.81, 95% CI = 0.70 to 0.94) cancer, with no associated increase in early mortality. Conclusions: The majority of patients with locally advanced colorectal cancer did not receive a multivisceral resection. The geographic variation in the application of this procedure in patients with colon cancer suggests that local organizational structures and processes of care may play an important role in patient treatment and, therefore, prognosis.
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INTRODUCTION |
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Colorectal cancer is the third most common incident cancer and the second leading cause of cancer deaths in the United States (1). In approximately 5%–15% of patients, the primary cancer directly invades adjacent organ structures and there is no evidence of distant metastases (2–11). Recent guidelines adopted by the National Cancer Institute (5) and the American Society of Colon and Rectal Surgeons (2,12) emphasize that appropriate surgical management of these locally advanced adherent colorectal cancers should include multivisceral resection, in which the cancer and adherent structures are removed en bloc. These guidelines are based on studies that have demonstrated that 40%–84% of adhesions between the cancer and the adjacent organs are malignant (4,5,11,13–24) and that intraoperative assessments of the nature of the adhesions are often inaccurate (4,5,11,16,17,23,24). Multivisceral resection among patients with locally advanced adherent colorectal cancer results in improved rates of margin-negative (R0) resections, local control, and overall survival (3,7,8,14,21,24–28), and results of some studies suggest that survival in patients with locally advanced adherent colorectal cancer is equal to that of patients with stage-matched colorectal cancer in which adjacent organs are not involved (7,14,21,24,26,28). Conversely, other reports document increased rates of local recurrence and inferior overall survival among patients who had colorectal resections in which the tumor was transected as a result of separation from adherent structures (3,10,18). Although multivisceral resection is associated with improved long-term survival, it is a complex surgical procedure that is associated with increased morbidity compared with standard colorectal cancer resection (7,10,11,14,17,23,24,27,29,30). Nonetheless, recent reports document that multivisceral resection is not associated with an increase in perioperative mortality rates compared with standard resection (7,10,11,17,22,24,27,29–37).
Despite this evidence and the guidelines supporting the role of multivisceral resection in patients with locally advanced adherent colorectal cancer, some authors (3,11) have noted that this procedure is not always practiced. The use of limited resection rather than multivisceral resection in these patients may be influenced by factors related to the surgeon and/or the patient. Insufficient patient workup and subsequent failure to recognize the locally advanced nature of the colorectal cancer before surgery or a surgeon's reluctance or inexperience in performing multivisceral resection may account for suboptimal management of some patients with curable disease. Alternatively, patients' perspectives on multivisceral resection, or comorbidities that might render patients less likely to tolerate operative morbidity, may result in a decision to avoid multivisceral resection. The literature contains no population-based studies that have examined the surgical management of patients with locally advanced adherent colorectal cancer to determine the patterns of surgical practice. This study evaluates practices related to the use of multivisceral resection for patients diagnosed with locally advanced adherent colorectal cancer, factors that are associated with the type of surgical resection these patients receive, and outcomes related to the type of surgery performed.
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METHODS |
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Data Sources
Data for this study were obtained on August 5, 2005, from the Surveillance, Epidemiology, and End Results (SEER) program registries that covered the following 11 regions: San Francisco, Hawaii, Detroit, Utah, Seattle, New Mexico, Connecticut, Iowa, Atlanta, Los Angeles, and San Jose–Monterey (38). These registries include incident cancers and follow-up information reported through December 31, 2002. The case ascertainment rate in the SEER program is greater than 97% (39). All the regional registries that comprise the SEER program hold the highest certification of data quality given by the North American Association of Central Cancer Registries (40). To ensure the completeness and accuracy of the reported data, the SEER program conducts regular quality-control studies and training sessions to address deficient areas (41). The current standard for the accuracy of SEER data is an error rate of less than 5% (42).
Study Population
All patients who were 18 years or older and diagnosed from January 1, 1988, through December 31, 2002, with colorectal adenocarcinoma were identified for potential inclusion in this study. The diagnosis of colorectal cancer was established, defined by the following International Classification of Diseases for Oncology (ICD-O-2) codes (43): C18.0 (cecum), C18.2–C18.9 (ascending colon through sigmoid colon), C19.9 (rectosigmoid), and C20.9 (rectum). Patients were excluded if they had metastatic disease or had not undergone surgical resection of their tumor. The study cohort included patients with colorectal cancers that had invaded through the serosa [defined as T4 under the tumor-node-metastasis staging system (44)] and into adjacent organs, as defined by SEER Extent of Disease codes 60, 65, 66, 70, 75, and 80 (Table 1), which are abstracted by SEER coders from clinical, radiologic, surgical, and pathology reports (45). Data from the surgical reports were considered especially important for coding the extent of disease for tumors that were not completely resected. In addition, for patients who received neoadjuvant therapy, extent of disease information includes information obtained from surgical and pathology reports compiled after the patients have received neoadjuvant therapy because clinical stage (before neoadjuvant radiation) and pathologic stage are not reported separately in SEER registries.
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The selection criteria for the study cohort was chosen such that all members of the cohort had colorectal cancer staged as T4 (44) with invasion of adjacent organs (locally advanced adherent colorectal cancer) and therefore required a multivisceral resection for cure. For comparison, we also identified a cohort of patients with colorectal cancers that had invaded through the serosa but that were not adherent to adjacent organs (SEER Extent of Disease codes 50 and 55). This study was approved by the Research Ethics Boards at the University of Toronto and Sunnybrook Health Sciences Centre.
Variables
We collected data on the following variables: patient demographic characteristics (i.e., age at diagnosis, sex, and race), SEER registry region, date of diagnosis, tumor characteristics (i.e., grade, nodal status, and tumor location), radiation therapy (none, neoadjuvant, or adjuvant), type of surgery (multivisceral resection versus standard resection), and overall survival, which is directly recorded in the SEER registry and is based on the patient's date of diagnosis and date of death. Cut points for age were chosen to reflect clinically relevant considerations with respect to the surgical candidacy of patients with colorectal cancer. Rectosigmoid cancers were grouped with rectal cancers because of their similar anatomic relationships and surgical treatment. For colonic cancers, tumor location was subclassified into left-sided cancers (distal to the splenic flexure) or right-sided cancers (proximal to the splenic flexure). The primary outcome was the type of surgery performed; secondary outcomes were short-term mortality and long-term overall survival. The SEER registry is considered reliable in identifying major surgical procedures for colorectal cancer (46). Because the date of surgery was not recorded in the registry, we defined short-term mortality associated with surgery as mortality at 1 and 6 months after the date of diagnosis. This definition was chosen to account for perioperative mortality after immediate surgery or after surgery following neoadjuvant radiation.
Statistical Analysis
Descriptive statistics were calculated for all variables. Categorical variables were compared using chi-square tests. Continuous variables were tested for normality and compared using Student's t test if normality was satisfied and Wilcoxon's rank sum test if it was not. We used logistic regression analysis to estimate crude relationships between the variables and the primary outcome. A multiple logistic regression model was then used to control for the potential confounding effect of patient factors, tumor factors, and treatment-related variables (i.e., type of radiation treatment). The Hosmer–Lemeshow goodness-of-fit statistic (47) was assessed to ensure the validity of the model. Odds ratios (ORs) and 95% confidence intervals (CIs) were generated for all variables. Unadjusted short-term mortality (at 1 month and 6 months after diagnosis) and overall survival were modeled using Kaplan–Meier curves; log-rank tests were used to analyze the differences between the survival curves. Cox proportional hazards models were used to adjust the survival analysis for potential confounders. Proportional hazards assumptions were confirmed graphically by plotting the log of the negative log of the survival function versus the log of time. We tested for interactions between multivisceral resection and lymph node status or receipt of radiation therapy. Hazard ratios (HRs) and 95% confidence intervals were generated, with hazard ratios less than 1.0 indicating survival benefit (or reduced mortality). Kaplan–Meier analyses and Cox proportional hazards models were used to compare the survival of the patients with locally advanced adherent colorectal cancer with that of the comparison cohort of patients with T4 colorectal cancer that was not locally adherent. All statistical tests were two-sided. Statistical significance was defined as P less than .05. Statistical analyses were performed with the use of SAS software (version 9.1; SAS Institute, Cary, NC).
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RESULTS |
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We identified 229 538 patients who were at least 18 years old and diagnosed with colorectal adenocarcinoma from January 1, 1988, through December 31, 2002, in the 11 SEER regions. Of these patients, 9651 (4.2%) had locally advanced adherent colorectal cancer, of whom 8380 underwent a surgical resection. A further 12 199 patients with T4 nonlocally advanced colorectal cancer (i.e., without invasion of adjacent organs) were identified for the comparison cohort.
Descriptive statistics for the study population are shown in Table 2. The mean age at diagnosis for the entire cohort was 69.4 years; the patients with colon cancer were statistically significantly older than those with rectal cancer (70.3 years versus 66.0 years; P<.001). There were more females than males in our study population, and most were white. The primary tumor was colonic in 79.2% of the patients and rectal in 20.8% of the patients. Positive lymph nodes were found in 51.5% of the patients.
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Multivisceral Resection
In our study population, 33.3% of the patients (range across the 11 SEER regions = 26.0%–38.7%) received multivisceral resection, and there was no statistically significant difference between the proportion of colon cancer patients (32.9%) and rectal cancer patients (34.7%) who received multivisceral resection (P = .16). Table 3 shows factors associated with having multivisceral resection for patients with colon and rectal cancers. In unadjusted analyses, the following factors were positively associated with having multivisceral resection among colon cancer patients: age at diagnosis less than 80 years, female sex, lower tumor grade, negative lymph node status, SEER region, left-sided cancers, and receipt of adjuvant radiation. Among rectal cancer patients, female sex and SEER region were positively associated with having a multivisceral resection, whereas receipt of neoadjuvant radiation was negatively associated with this outcome. Race was not statistically significantly associated with having multivisceral resection for either colon or rectal cancer.
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In adjusted analyses, both age at diagnosis less than 80 years (OR for age 65–79 years versus
80 years = 1.29, 95% CI = 1.12 to 1.50, P<.001; OR for <65 years versus 80 years = 1.39, 95% CI = 1.19 to 1.64, P<.001) and female sex (OR = 1.45, 95% CI = 1.29 to 1.63, P<.001) were independently and positively associated with having a multivisceral resection for colon cancers. These factors were also statistically significantly associated with multivisceral resection for rectal cancers (OR for age <65 years versus 80 years = 2.05, 95% CI = 1.41 to 2.98, P<.001; OR for female sex = 4.07, 95% CI = 3.13 to 5.29, P<.001). In addition, SEER region was statistically significantly associated with having a multivisceral resection for colon cancer (OR for the region with the highest odds versus that with the lowest odds = 2.18, 95% CI = 1.40 to 3.41, P<.001). For rectal cancers, differences were noted between the regions with highest and lowest odds of multivisceral resections (OR = 4.7, 95% CI = 1.4 to 15.7), but the overall degree of regional variation did not reach statistical significance (P = .17). Other variables that were positively associated with multivisceral resection for colon cancer included node-negative status (OR = 1.34, 95% CI = 1.19 to 1.51, P<.001), left-sided cancers (OR = 2.07, 95% CI = 1.83 to 2.33, P<.001), and receipt of neoadjuvant radiation (OR = 3.12, 95% CI = 1.01 to 9.62, P = .047). Neoadjuvant radiation was inversely associated with multivisceral resection for rectal cancers (OR = 0.57, 95% CI = 0.38 to 0.85, P = .006). Survival
Age at diagnosis less than 80 years, female sex, and negative nodal status were associated with better overall survival in patients with locally advanced adherent colon and rectal tumors in adjusted analyses (Table 4). SEER region was also statistically significantly associated with overall survival for both colon (HR for region with highest hazard versus lowest hazard = 1.61, 95% CI = 1.25 to 2.08) and rectal cancers (HR for region with highest hazard versus lowest hazard = 2.01, 95% CI = 1.23 to 3.28). Among colon cancer patients, tumor grade was statistically significantly associated with overall survival: patients with grade I or II colon cancers had better overall survival than patients with grade IV colon cancers. Among rectal cancer patients, receipt of adjuvant or neoadjuvant radiation was statistically significantly associated with better overall survival. In unadjusted analyses, patients who received multivisceral resection had better survival than patients who received standard resection (P<.001; Fig. 1). Overall 5-year survival was 35.1% (95% CI = 33.1% to 37.0%) in the multivisceral resection group and 27.7% (95% CI = 26.4% to 28.9%) in the standard resection group. Having had a multivisceral resection was independently associated with improved overall survival among both colon cancer patients (HR = 0.89, 95% CI = 0.83 to 0.96) and rectal cancer patients (HR = 0.81, 95% CI = 0.70 to 0.94).
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There were no statistically significant interactions between multivisceral resections and either nodal status (P = .69) or type of radiation therapy received (P = .52 for neoadjuvant radiation, P = .16 for adjuvant radiation, P = .18 for other types of radiation), indicating that multivisceral resection was associated with a survival benefit regardless of the patient's nodal status or the type of radiotherapy received. Patients with locally advanced adherent colorectal cancer who received multivisceral resection had statistically significantly worse overall survival than stage-matched patients without locally adherent disease in both crude (Fig. 1) and multivariable (HR = 1.48, 95% CI = 1.39 to 1.58) analyses. Finally, in patients with locally advanced adherent colorectal cancer, multivisceral resection was not associated with an increase in adjusted mortality either at 1 month after diagnosis (HR for colon cancer patients = 0.82, 95% CI = 0.66 to 1.02; HR for rectal cancer patients = 0.95, 95% CI = 0.50 to1.83) or at 6 months after diagnosis (HR for colon cancer patients = 0.77, 95% CI = 0.67 to 0.89; HR for rectal cancer patients = 0.72, 95% CI = 0.49 to 1.07).
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DISCUSSION |
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Current evidence indicates that, compared with standard resection, multivisceral resection for nonmetastatic locally advanced adherent colorectal cancer is associated with improved local recurrence rates and improved overall survival (3,7,8,10,14,21–28). Furthermore, current guidelines for colorectal cancer surgery advocate this approach (2,5,12). However, we found that only one-third of the patients in our study population who underwent surgical resection for locally advanced adherent colorectal cancer received a multivisceral resection. These patients had a clinically significant overall survival benefit with no increase in short-term mortality compared with similar patients who did not receive multivisceral resection.
Several patient-related factors were associated with whether a patient had a multivisceral resection. Not surprisingly, patients who were younger at diagnosis were more likely than older patients to undergo multivisceral resection, perhaps reflecting a reluctance by surgeons to perform radical surgery on older patients, who may be at increased risk of perioperative morbidity and mortality (48–57). Nonetheless, advanced age at the time of surgery need not be the sole contraindication to major surgery, in particular because recent studies have demonstrated that appropriately selected elderly colorectal cancer patients who undergo major colorectal cancer surgery can have excellent surgical outcomes (7,29,52,58–67). There was a striking sex bias toward multivisceral resection being performed more in female than male patients. Among rectal cancer patients, female patients were approximately four times as likely as male patients to undergo a multivisceral resection. This finding is consistent with those of previous studies (3,10,11,23) and likely reflects the potential morbidity associated with complex genitourinary resection and reconstruction that is required when there is malignant invasion of male urologic structures such as the prostate (6,7,32,33,68). Because the surgery may involve total pelvic exenteration (multivisceral resection of all pelvic organs) with creation of dual ostomies, patients and physicians may be reluctant to accept the morbidity and lifestyle adjustments that may result. However, Wright et al. (68) showed that patients who have had a previous pelvic exenteration are able to adjust to the lifestyle changes associated with dual ostomies and are willing to tolerate the procedure and its resultant morbidity in an effort to achieve cure. Moreover, results of several studies (69–73) suggest that, among cancer patients, having an ostomy may not result in a substantial decline in the health-related quality of life.
We found that colon cancer patients who had negative lymph nodes were more likely to receive multivisceral resection than colon cancer patients with node-positive disease. Nonetheless, data from this study and other research (28) confirm that multivisceral resection confers a survival benefit to patients, regardless of their nodal status. In addition, patients with right-sided cancers (proximal to the splenic flexure) were less likely to receive multivisceral resection than patients with left-sided disease. Margin-negative resection of right-sided locally advanced adherent cancer can be challenging due to tumor invasion of structures such as the stomach, liver, biliary system, and the proximal pancreas. Nevertheless, results of several studies (74–80) confirm that patients with invasion into the head of the pancreas or duodenum can achieve improved overall survival with en bloc pancreaticoduodenectomy compared with patients treated nonsurgically. Patients who received neoadjuvant radiation for rectal primary tumors were less likely to receive multivisceral resection than patients who did not receive radiation. The explanation for this finding is unclear from the data. One hypothesis may be that, in the setting of neoadjuvant radiation, malignant adhesions between the tumor and adjacent organs are mistaken for radiation-induced inflammatory adhesions. However, a study by Gohl et al. (81) found that rates of malignant adhesions were similar in patients who received neoadjuvant radiation and those who did not (34% versus 36%), suggesting that neoadjuvant radiation does not obviate the need for multivisceral resection.
Our results extend those of Hunter et al. (3), who reported on 43 colorectal cancer patients treated at a single academic center from 1975 to 1979. In that study, the 35% of patients with locally adherent colorectal cancer who did not undergo multivisceral resection had higher rates of local recurrence and mortality than the 65% of patients who were treated with multivisceral resection. The rate of multivisceral resection found in our population-based study of locally advanced adherent colorectal cancer was much lower (i.e., 33.3%), suggesting that multivisceral resection rates may be higher at specialty centers such as that in the study by Hunter et al. (3). In the present study, multivisceral resection was associated with a survival benefit compared with standard resection in both unadjusted and adjusted analyses. These benefits are clinically significant but are more modest than expected based on reports in the literature (3,7,8,14,21,24–28) regarding survival rates of patients treated with multivisceral resection for colorectal cancer. We found that patients who received multivisceral resection had worse survival than stage-matched patients who did not have locally adherent disease, in contrast to findings in previous smaller studies (7,14,21,24,26,28) that found that the two groups of patients had similar overall survival. Our finding suggests that, despite receiving the appropriate type of operation, the quality of surgery in some of the patients treated with multivisceral resection may have been suboptimal with respect to factors such as presence of tumor at the resection margins. Among patients receiving multivisceral resection, those with positive margins have worse survival than those with negative margins (3,11,23,29,30); thus, positive margins in some study patients who received multivisceral resections would be expected to reduce the observed survival benefit of multivisceral resection. Furthermore, other aspects of care, such as receipt of adjuvant therapy or intensity of follow-up, may also play a role in patient outcome.
In this study, we found statistically significant regional variation in the rate of multivisceral resection for locally advanced adherent colorectal cancer, despite adjustment for confounding variables. For colonic tumors, there was a 2.18-fold difference in the odds of multivisceral resection across the 11 SEER regions. For rectal tumors, although the overall degree of regional variation was not statistically significant, there was nearly a fivefold difference between the region with the highest odds of a multivisceral resection and the region with the lowest odds. Numerous reports in the literature document geographic variation in the rates at which various surgical procedures are performed (82–90). However, many of these studies involved clinical scenarios for which there is legitimate equipoise in the choice of treatment [e.g., prostatectomy for benign prostatic disease or hemorrhoidectomy (86–89)]. By contrast, our study population comprised patients who had cancers that required a multivisceral resection to ensure that resection would be curative. Therefore, the geographic variation in the rates of multivisceral resection that we observed suggests that local factors associated with the patient, the tumor, or the health care provider and that are not recorded in the SEER registry may influence the decision to perform multivisceral resection in the management of this patient population.
There are several limitations to our study. First, we were unable to draw conclusions regarding the associations between some factors (i.e., patient comorbidities, patient preference, the nature or extent of preoperative workup, surgeon and hospital case volumes, or hospital characteristics) and the receipt of multivisceral resection because the SEER registry does not contain information on those variables. However, the effect of patient preference and fitness to undergo a multivisceral resection was minimized because our study cohort was restricted to patients who underwent major colorectal surgery, and thus all patients presumably agreed to and were deemed fit to undergo major surgery. Second, because the SEER registry also does not report information on the exact date of surgery, we used short-term mortality (i.e., mortality at 1 and 6 months from the date of diagnosis) to estimate perioperative mortality. Because all patients in the registry had surgery within 4 months of diagnosis, the 1- and 6-month time windows captured the perioperative period for all patients in our study population. Third, we were able to examine the type of operation performed but could not evaluate how quality indicators such as margin status influenced the use of multivisceral resection because this information is also not recorded in the registry. A negative resection margin (i.e., an R0 resection) is the goal of any curative-intent surgery, and the decision to perform multivisceral resection is the first step to achieve this goal for patients with locally advanced colorectal cancer. The absence of information in the registry on margin status, comorbidities, and use of chemotherapy also imposed inherent limitations on our secondary analysis of overall survival because these are potentially important factors that could influence survival. Therefore, we can draw conclusions about the appropriateness of the type of operation performed but cannot make determinations on the quality of that operation. Finally, it is possible that we inadvertently excluded patients in whom no recognition of possible adjacent organ involvement was noted on imaging or in the operative note and in whom a standard resection was performed. These patients would have been coded as having T4 disease without adjacent organ invasion. Had these patients been included in our study, the true rate of multivisceral resection would have been even lower than what we report here. However, the magnitude of this ascertainment bias is likely to be small.
This study is, to our knowledge, the first to examine, at a population level, the rate of surgical management and outcomes for a cohort of patients who underwent surgery for locally advanced adherent colorectal cancer. We found that only one-third of patients who had surgical resection for this disease underwent multivisceral resection, and there was considerable variation in the rate at which the procedure was performed by SEER region, patient factors, and tumor factors. Nonetheless, patients who received multivisceral resection had improved overall survival without increased short-term mortality. Given that appropriate surgery is a critical step in the treatment of these patients, further study is warranted to elucidate factors related to the structures and processes of care that contribute to deficiencies in surgical care and to determine future interventions to improve the quality of care delivered to this population of patients.
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NOTES |
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Dr C. H. L. Law is a Career Scientist of the Ontario Ministry of Health and Long-Term Care (MOHLTC) and is supported through a Health Research Personnel Development—Career Scientist Award. Drs A. Govindarajan, N. G. Coburn, and C. H. L. Law contributed to all parts of the study (design, data collection, analysis and interpretation, writing of the manuscript, and the decision to submit the manuscript for publication). Dr A. Kiss contributed to the analysis and interpretation of the data. Dr L. Rabeneck contributed to the interpretation of the data, the writing of the manuscript, and the decision to submit the manuscript for publication. Dr A. J. Smith contributed to the design of the study, interpretation of the data, writing of the manuscript, and the decision to submit the manuscript for publication. The MOHLTC provides research salary support to Dr C. H. L. Law and was not involved in any part of this study, including its design, data collection, analysis, interpretation of data, writing of the manuscript, or the decision to submit for publication.
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Manuscript received February 1, 2006; revised July 25, 2006; accepted August 4, 2006.
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