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Annals of Surgical Oncology 9:380-387 (2002)
© 2002 Society of Surgical Oncology

ORIGINAL ARTICLES

A Population-Based Study of the Extent of Surgical Resection of Potentially Curable Colon Cancer

Alexandra M. Easson, MD, Michelle Cotterchio, PhD, Jacqueline A. Crosby, MD, Heather Sutherland, MSc, Darlene Dale, CCHR(A), Melyssa Aronson, MSc, Eric Holowaty, MD and Steven Gallinger, MD

From the Departments of Surgical Oncology (AME, JAC) and Epidemiology & Statistics (HS), Princess Margaret Hospital, Toronto, Ontario, Canada; Division of Preventive Oncology (MC), Surveillance Unit (EH), Ontario Cancer Registry (DD), Cancer Care Ontario, Toronto, Ontario, Canada; and the Familial GI Cancer Registry (MA) and Department of Surgery (SG), University of Toronto, Mount Sinai Hospital, Toronto, Ontario, Canada.

Correspondence: Address correspondence and reprint requests to: Alexandra Easson, MD, Room 3-130, Department of Surgical Oncology, Princess Margaret Hospital, 610 University Ave., Toronto, Ontario M5G 2M9, Canada; Fax: 416-946-6590; E-mail: easson.alexandra{at}uhn.on.ca


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: We attempted to determine factors contributing to the extent of initial curative resection for colon cancer in a population-based cohort. Total abdominal colectomy with ileorectal anastomosis (TAC-IR) may be considered for young patients or those with a colorectal cancer family history to prevent metachronous lesions and facilitate surveillance.

Methods: All Ontario patients newly diagnosed with colon cancer over 12 months beginning in July 1997 were staged at the time of surgery. The extent of resection was compared with variables, including familial risk obtained from the Ontario Familial Colon Cancer Registry.

Results: Complete staging was possible for 86% of patients. A total of 1223 patients had a potentially curative resection: 17%, 46%, and 36% were stage I, II, and III, respectively. Patients were more likely to receive a TAC-IR if they were <=50 years old (odds ratio [OR], 3.5; 95% confidence interval [CI], 1.8–6.6), if they had a synchronous lesion (OR, 28.37; 95% CI, 12.2–61.2), or if they were at a teaching hospital (OR, 2.8; 95% CI, 1.6–4.7), but not if they had a family history (OR, .7; 95% CI, .3– 1.5).

Conclusions: Young age, teaching hospital, and multiple cancers but not family history were important factors for performing a TAC-IR.

Key Words: Colorectal neoplasms • Surgery • Family history • Epidemiology • Neoplasm staging • Familial colorectal cancer


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The discovery of genetic abnormalities predisposing to colorectal cancer has begun to alter traditional surgical management. Prophylactic (procto)colectomy is advocated for patients with familial adenomatous polyposis (FAP) caused by germline adenomatous polyposiscoli mutations.1 Total abdominal colectomy with ileorectal or ileosigmoid anastomosis (TAC-IR) is the recommended initial surgical procedure for hereditary nonpolyposis colorectal cancer (HNPCC) patients known to carry germline mismatch-repair gene mutations.2–4 For most patients who present with colorectal cancer, however, decisions about definitive surgical management must be made without the benefit of genetic testing. Because of the lack of an easily recognized phenotype (excluding FAP), clinical characteristics are used to identify whether a patient’s colorectal cancer is sporadic or part of a known or as yet unknown hereditary cancer syndrome. These characteristics include a younger age at presentation, synchronous or metachronous cancers, and a family history of colorectal cancer.4,5

Approximately 25% of colorectal cancer patients have a personal or family history of the disease,1,6 and 7% of cases occur in patients younger than 50 years.7 Young age alone (younger than 50 years) is associated with a strong family history of colorectal cancer.8,9 The risk of colorectal cancer is increased with even a weak family history; in one large study, the relative risk for an individual with only one or with two or more affected relatives was 1.72 and 2.75, respectively, compared with individuals without a family history.6 This risk increases 5-fold for young patients.6,8,10 Known hereditary cancer syndromes such as HNPCC account for only 1% to 2% of patients with colorectal cancer.4

The Amsterdam criteria to define HNPCC combine family history with young patient age (Table 1).11 HNPCC patients with mismatch-repair gene mutations have an up to 75% lifetime risk of colorectal cancer.2,12 Known gene mutations have been found in 40% to 70% of families who satisfied the Amsterdam criteria, in 18% to 26% of those with strong family histories not fulfilling Amsterdam criteria, and in 17% if patients had a young age of onset alone.13–17 This suggests that genetic mutations have not yet been identified for the majority of patients with a family history of colorectal cancer and young age at onset. Expanded clinical criteria have been developed to broaden genetic testing for patients with familial colorectal cancer, including Mount Sinai Hospital criteria,18 modified Amsterdam criteria,19 and others.20,21


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  		TABLE 1. Criteria used by the Ontario Familial Colon Cancer Registry to classify familial risk of colorectal cancer patients
 
Standard treatment for potentially curable colon cancer is segmental resection of the tumor and its mesentery with or without adjuvant chemotherapy. Postoperative colonoscopic surveillance detects local recurrence and metachronous lesions. For the majority of patients with no colorectal cancer family history, the cumulative risk of developing a metachronous lesion is 6.3% after 18 years of follow-up.22 Young patients, however, have a cumulative risk of 30% after 40 years of follow-up, 23,24 and the risk in HNPCC is 40% after 10 years.17 TAC-IR at initial operation reduced the incidence of metachronous lesions by approximately 50% in a group of HNPCC families.3 The risk for an individual with familial colorectal cancer not due to known germline mutations is unknown, but it may fall somewhere between the aforementioned percentages. TAC-IR as the initial curative procedure may therefore be considered for all patients who are young or for those with a strong family history.5,23,25,26 TAC-IR prevents metachronous lesions and facilitates surveillance of the residual rectum now easily performed with a sigmoidoscope.

There are few population-based studies of the surgical management of colon cancer. This study used a population-based database to determine what factors were associated with the extent of initial curative surgical resection for colon cancer performed by surgeons in a large North American geographic region. In particular, we sought to determine whether the extent of colon surgery was associated with any factors, such as young age at presentation or a family history of colorectal cancer, predisposing to a high risk of metachronous colon cancer.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
The Ontario Cancer Registry (OCR), which receives information on all cancer cases in the province of Ontario, Canada (population 11 million), was used to identify all cases of colorectal cancer for a 1-year period beginning July 1, 1997. The OCR was also used to create the Ontario Familial Colon Cancer Registry (OFCCR), one of six international sites participating in the Co-Operative Familial Registry for Colorectal Cancer Studies, established by the National Cancer Institute. The OFCCR is a population-based registry that approached all patients newly diagnosed with colorectal cancer in Ontario from the ages of 20 to 74 years from July 1, 1997, to June 30, 2000. Patients with FAP were excluded, because they are maintained in a separate registry.27 Patients identified by OCR pathology reports were mailed consent forms and a detailed family and personal history questionnaire after we obtained permission for contact from their physicians. Patients were then classified into low, intermediate, and high familial risk for colorectal cancer. Additional details of the OFCCR have been fully described elsewhere28; for the purposes of this study, the intermediate-risk criteria used by the registry were modified to include 6 of the 12 criteria that directly related to personal and family history (Table 1). Local ethics review boards approved this study under the research plan of the OFCCR.

All newly diagnosed colon cancer cases diagnosed in a 12-month period (July 1, 1997, to June 30, 1998) were staged by an author (A.M.E.) according to the American Joint Committee on Cancer tumor-node-metastasis staging system29 to identify all nonmetastatic and potentially curable colon cancer primary tumors treated by surgical resection. Staging information was obtained from two separate sources. Tumor depth and nodal status were obtained from the pathology report available from the OCR. To determine metastatic status, the OCR requested the operative report and discharge summary of the surgical resection admission directly from the hospital where the surgery had taken place. Imaging studies were often included. These reports were requested only for the first year of the OFCCR because of financial considerations. All patients deemed M0, or having no metastatic disease, were included in this study if (1) a perioperative ultrasound or computed tomographic scan of the abdomen was reported as normal; (2) in the operative report, the surgeon reported the absence of liver (by palpation) or other metastases at laparotomy and reported that a complete resection had been performed; or (3) it was indicated in the discharge summary or operative report that a perioperative metastatic work-up was normal. Blind restaging of a random sample of 40 patients by the same and a second investigator (J.A.C.) for intra- and interobserver reliability resulted in a Cohen’s {kappa} of .96 for both, indicating excellent agreement. Patients with a previous resection for colon cancer were analyzed separately. The OCR also provided data on tumor location, history of metachronous or synchronous cancer, and treating hospital (teaching or nonteaching). Teaching hospitals were defined as those with surgical residency programs.

The outcome variable was TAC-IR versus a lesser resection. For the purpose of this study, we combined segmental resection and hemicolectomy as a single variable. Statistical analysis was performed with univariate ({chi} 2) statistics and multivariable logistical regression, and significance was set at the P <= .05 level.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
There were 3394 eligible patients who had a new diagnosis of colorectal cancer in Ontario from July 1, 1997, to June 30, 1998. Rectal cancer was diagnosed in 1062 (31%) patients, and these patients were excluded from this study. A further 322 (9%) patients were excluded because (1) medical records were unavailable (n = 104), (2) the diagnosis was apparently incorrect (other or recurrent cancer, or in situ disease only; n = 84), (3) polypectomy was the sole treatment (n = 60), (4) it was not possible to classify a rectosigmoid tumor as a rectal or colon cancer (n = 57), or (5) the diagnosis was carcinomatosis of unknown origin (n = 17).

Of the 2010 eligible colon cancer patients, 1727 (86%) were staged as described in Fig. 1. Characteristics of the 1223 patients who had a potentially curative colon resection and were included in this analysis are listed in Table 2. The mean age was 66 ± 5.6 years (median, 66 years). The distribution of cancer at presentation by sex and stage was similar to that of other population-based studies.7,30 Of the 124 patients <50 years old at diagnosis, the tumor distribution was equal between right-sided (proximal to the splenic flexure; n = 64) and left-sided (n = 60) lesions. Patients with right-sided lesions tended to be younger (P = .07). Young patients were more likely to have a positive family history (P = .049).



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  		FIG. 1. Stage distribution of eligible colon cancer patients in Ontario for a 12-month period beginning July 1, 1997. Patients with potentially curable colon cancer (n = 1223) were analyzed in this study. TNM, tumor-node-metastasis system.

 

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  		TABLE 2. Patient profile: potentially curable colon cancer patients (N = 1223)
 
Assessment of familial risk was possible for 662 (54%) of 1223 of the colon cancer patients (Table 3). The number of patients fulfilling high-risk criteria (2.8%) was similar to the rate of HNPCC found in other population-based groups.31– 33 Of note, a family history, whether positive or negative, was recorded by surgeons anywhere in the operative report or discharge summary in only 6.6% of cases (data not shown). Of greater importance, the majority of patients with a high or intermediate familial risk had only a segmental resection as their initial curative surgical procedure.


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  		TABLE 3. Characteristics of colon cancer patients who responded to the OFCCR family history questionnaire (N = 662)
 
Results of the univariate and multivariate analyses are listed in Table 4. Patients <50 years old were 3.5 (95% confidence interval [CI], 1.8– 6.6) times more likely to have a TAC-IR than a segmental resection. The presence of synchronous colorectal polyps, cancer, or both made TAC-IR 29.3 (95% CI, 13.4–64.2) times more likely, as did a metachronous or synchronous noncolorectal cancer (odds ratio, 2.5; 95% CI, 1.1–6.1). Patients treated at teaching hospitals were 2.8 (95% CI, 1.6–4.7) times more likely to have a TAC-IR. These patients were not different from those who had their surgery at nonteaching hospitals with respect to age, stage, or tumor location, but these institutions did have a higher, but not statistically significant, frequency of patients with an intermediate or high-risk family history (data not shown). A total of 326 surgeons performed colon resections: 221 (65%) in nonteaching and 105 (32%) in teaching hospitals. In the nonteaching centers, 35 surgeons performed 39 total colectomies (1.1 per surgeon), and in the teaching hospitals, 28 surgeons performed 43 total colectomies (1.56 per surgeon). An intermediate or high-risk family history of colorectal cancer, however, did not result in a statistically significantly higher likelihood of receiving a TAC-IR instead of a segmental resection (odds ratio, .7; 95% CI, .3–1.5).


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  		TABLE 4. Association between patient factors and extent of colon resection (TAC-IR vs. lesser resection)
 
Fifty-seven patients presented with metachronous colorectal cancer, having had a previous cancer colon resection at least 1 year before and in a different segment of the colon or rectum (Fig. 1). The mean age of these subjects was 66.36 ± 1 years, and the median age was 69 years (range, 42–74 years). The average interval between the cancer diagnoses was 9.2 ± 1.1 years, with a median of 7 years (range, 1–31 years). Of note, 25 (44%) of 57 had a high- or intermediate-risk family history. However, only 22 (38.6%) of 57 had a completion colectomy at the time of their second operation.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
This is the first population-based study to examine the extent of initial resection for potentially curable colon cancer. Most patients, as expected, received a segmental resection; however, surgeons in Ontario were more likely to perform TAC-IR, rather than a lesser resection, as the initial curative resection for young patients and for patients with multiple cancers. A strong family history of colorectal cancer did not seem to be a factor in this decision. These findings are especially powerful because of the population-based study design.

The accurate staging of metastatic status is a major challenge when attempting perioperative tumor-node-metastasis staging with use of cancer registries. Although tumor stage and nodal status are readily attainable from the pathology report, there is no single source of data to determine metastatic status at the time of diagnosis. In addition, there is little consensus among clinicians with respect to standard perioperative work-up of colorectal cancer patients. Nevertheless, we were able to stage 86% of the patients by using the combined information from the pathology report, operative report, and hospital discharge summary.

Differences in surgical morbidity and long-term functional outcome between TAC-IR and segmental resection have not been studied in this patient population. Series of TAC-IR for FAP patients report a morbidity of 10% to 23% and a mortality34,35 of 0% to 1.1%. These rates are similar for non-FAP patients undergoing segmental resection.36 FAP patients report a mean of 3 to 3.6 bowel movements in 24 hours after TAC-IR, with some patients requiring antidiarrheal medication37,38; this rate may or may not be similar in the general population. The risk of developing cancer in the rectal segment in HNPCC patients is estimated to be 3% every 3 years after TAC-IR.39 TAC-IR allows for easy rectal surveillance with a sigmoidoscope. The long-term functional consequences after TAC-IR must be balanced against the ease of postoperative surveillance and the prevention of metachronous polyps and cancer when considering this operation.

Obtaining high response rates to family history questionnaires has been difficult for genetic studies of colorectal cancer because of the extensive study requirements, issues of confidentiality, and high cancer mortality rate.40 The overall first-year response rate to the OFCCR family history questionnaire for all colorectal cancer patients was 61%; the response rate was 54% for the colon cancer patients. This rate was similar to, although slightly lower than, responses to the Ontario Familial Breast Cancer Registry, which collected family history data for breast cancer over a similar time period.41 The only other population-based colorectal cancer study in the past decade conducted in Ontario obtained a response rate42 of 74%. This study had less extensive requirements and did not involve family members. Two recent US population-based case-control studies43,44 of colorectal cancer reported response rates of 65%. A comparison of first-year responders and nonresponders of the OFCCR showed no significant differences in patient age, sex, or tumor stage, although there was slightly higher participation among patients living in rural areas.28 For the purpose of this analysis, it seems unlikely that the patient’s decision to respond to the questionnaire would be associated with the extent of surgery performed.

Knowledge of colorectal cancer genetics, with particular attention to the diagnosis of hereditary cancer syndromes, allows for targeted surveillance and management strategies for patients at high genetic risk, as well as the opportunity to intervene on behalf of not only one patient, but also an entire family. Any preoperative assessment should include a thorough personal and family cancer history. A recent survey demonstrated that knowledge of hereditary colorectal cancer syndromes was deficient among general surgeons and gastroenterologists.45 Increased education about the importance of family history as a risk factor for colorectal cancer is being approached in the province of Ontario as a component of a new government-funded genetic testing program for HNPCC. Along with the availability of genetic counseling and testing, the Ministry of Health is preparing education tools for distribution to all primary care physicians, general surgeons, and oncologists in the province.

In which cancer patients should a TAC-IR be considered at the initial resection? TAC-IR is the recommended initial procedure for HNPCC patients known to carry germline mismatch-repair gene mutations2–4 and should be considered in anyone with a family history that satisfies the Amsterdam criteria. Moreover, many cases with intermediate familial risk cancer histories seem to fall within the spectrum of HNPCC on the basis of the presence of germline mismatch-repair gene mutations.5,13–16,18,19,33 Although only 1% to 2% of colorectal cancer patients have family histories that satisfy the Amsterdam criteria, it is likely that many more newly diagnosed cases are at high risk of metachronous cancer on the basis of genetic abnormalities. For young patients, the risk of developing a metachronous lesion in their remaining lifetime is high, and the adverse functional consequences of a TAC-IR are low. In addition, young age at presentation and family history are not independent factors.8,9 It is the opinion of the authors that subtotal colectomy should be considered in young colorectal patients, particularly those with a family history of colorectal cancer and polyps. New techniques, such as preoperative immunohistochemistry of the tumor to screen for mismatch-repair protein loss and microsatellite instability, may allow better identification of patients who would benefit from a more aggressive initial surgical resection and promise to affect surgical decision-making in the future.46

In conclusion, young age (<50 years) and a personal history of synchronous or metachronous polyps or cancer increased the likelihood of having a TAC-IR as the initial curative surgical resection by surgeons in Ontario. A strong family history of colorectal cancer was not associated with a more extensive resection. We have demonstrated the broad utility of a population-based familial cancer registry such as the OFCCR for unbiased studies of colorectal cancer health services research. Similar analyses by other international registries within the National Institutes of Health/National Cancer Institute Cooperative Familial Registries for Colorectal Cancer Studies should lead to interesting insights into surgical practice patterns and decision-making for cancer patients in other parts of the world.


   Acknowledgments
 
The authors thank OCR health records technicians Carmen Radolovich, Doreen Pieszko, and Pat Gawat, as well as Giao Buchan at Cancer Care Ontario. Supported by the Division of Cancer Epidemiology and Genetics, National Cancer Institute, US National Institutes of Health (grant CA74783-03), the National Cancer Institute of Canada (grant 008034), and the Ontario Cancer Genetics Network, Cancer Care Ontario.

Received for publication September 5, 2001. Accepted for publication January 23, 2002.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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J. Clin. Oncol., May 1, 2005; 23(13): 3112 - 3124.
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C. A. Townsley, K. Naidoo, G. R. Pond, W. Melnick, S. E. Straus, and L. L. Siu
Are Older Cancer Patients Being Referred to Oncologists? A Mail Questionnaire of Ontario Primary Care Practitioners to Evaluate Their Referral Patterns
J. Clin. Oncol., December 15, 2003; 21(24): 4627 - 4635.
[Abstract] [Full Text] [PDF]

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