Originally published as JCO Early Release 10.1200/JCO.2005.04.0063 on October 31 2005

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Colorectal Cancer Surveillance: 2005 Update of an American Society of Clinical Oncology Practice Guideline

From the American Society of Clinical Oncology, Alexandria, VA

Address reprint requests to Mark R. Somerfield, American Society of Clinical Oncology, 1900 Duke St, Suite 200, Alexandria, VA 22314; e-mail: guidelines{at}asco.org

	ABSTRACT

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PURPOSE: To update the 2000 American Society of Clinical Oncology guideline on colorectal cancer surveillance.

RECOMMENDATIONS: Based on results from three independently reported meta-analyses of randomized controlled trials that compared low-intensity and high-intensity programs of colorectal cancer surveillance, and on recent analyses of data from major clinical trials in colon and rectal cancer, the Panel recommends annual computed tomography (CT) of the chest and abdomen for 3 years after primary therapy for patients who are at higher risk of recurrence and who could be candidates for curative-intent surgery; pelvic CT scan for rectal cancer surveillance, especially for patients with several poor prognostic factors, including those who have not been treated with radiation; colonoscopy at 3 years after operative treatment, and, if results are normal, every 5 years thereafter; flexible proctosigmoidoscopy every 6 months for 5 years for rectal cancer patients who have not been treated with pelvic radiation; history and physical examination every 3 to 6 months for the first 3 years, every 6 months during years 4 and 5, and subsequently at the discretion of the physician; and carcinoembryonic antigen every 3 months postoperatively for at least 3 years after diagnosis, if the patient is a candidate for surgery or systemic therapy. Chest x-rays, CBCs, and liver function tests are not recommended, and molecular or cellular markers should not influence the surveillance strategy based on available evidence.

	INTRODUCTION

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The American Society of Clinical Oncology (ASCO) published an update of the clinical practice guidelines on colorectal cancer surveillance in 2000. ASCO updates a guideline when data or publications might change a prior recommendation or when the Panel feels clarifications are required for the oncology community.

A subset of the original Expert Panel met in June 2004 and May 2005 to consider the evidence for each of the recommendations from 2000. Additional meetings were conducted via teleconference. The guideline update was circulated in draft form to the full Expert Panel for review and approval. These recommendations represent the Panel's attempt to extract practical guidelines from a combination of published evidence and expert opinion where the literature falls short.

Update Methodology
For the 2005 update, the Expert Panel completed the review and analysis of data published since 1999. Computerized literature searches of MEDLINE and the Cochrane Collaboration Library were performed. The searches of the English-language literature from 1999 to June 2005 combined the terms "colonic neoplasms," "colorectal neoplasms," and "rectal neoplasms," with the MeSH term, "follow-up studies" and the text words "surveillance" and "follow-up." The set of articles yielded from this initial search was supplemented by articles identified from searches on each of the tests or procedures addressed in the original guideline (eg, history and physical examination, liver function tests, carcinoembryonic antigen), in combination with "surveillance," "follow-up studies," and "follow-up." Supplementary searches were done to address positron emission tomography and magnetic resonance imaging. The searches were limited to human-only studies and to specific study design or publication type: randomized clinical trial, meta-analysis, practice guideline, systematic overview, or systematic review. The literature review centered on randomized clinical trials, and meta-analyses of data from randomized clinical trials.

The updated review reflects evidence on both specific methods of surveillance and risk stratification. There have been three recent, independently reported, meta-analyses,^1-3 all of which have evaluated either five or six of the randomized trials that compared low-intensity and high-intensity programs of surveillance for patients after curative-intent surgery for adenocarcinoma of the colon and rectum.^4-9 The individual randomized trials differed in the actual tests that were evaluated and the interval between tests, representing discrepancies that were mentioned in the previous update of this guideline.¹⁰

Further, the Panel considered recent analyses of data from major clinical trials in colon and rectal cancer. These analyses provide indirect empirical guidance to inform recommendations related to risk assessment in colorectal surveillance, and to support recommendations relating to the schedule of clinical visits and the frequency of specific tests. Two major pooled analyses of data from colon cancer clinical trials,^11,12 and the final analysis of an Intergroup clinical trial in rectal cancer were identified as relevant.¹³

The 2005 guidelines are now organized to provide recommendations for the stage II or III colon cancer patient. Aside from endoscopic follow-up, this guideline does not apply to patients with stage I colorectal cancer, where the risk of recurrence is very low. Where follow-up strategies for rectal cancer should differ from colon cancer, specific recommendations for those deviations are provided. In addition, the guideline has organized the recommendations into five broad categories: (1) history and physical examination and risk assessment; (2) laboratory tests; (3) imaging procedures; (4) endoscopic surveillance techniques; and (5) a new category of laboratory-based prognostic and predictive factors.

Summary of Literature Review Results
Since data show that some patients with colorectal cancer are cured following the resection of metastatic disease, several clinical trials have been performed examining the usefulness of various surveillance strategies and tests. At least one article noted substantial advances in survival and resectability during the last 30 years, supporting more aggressive follow-up after diagnosis and treatment.¹⁴

The Expert Panel did not complete an independent meta-analysis of the data from available randomized clinical trials given the availability of three high-quality and recent meta-analyses identified through the literature search.^1-3 (The quality of the three meta-analyses was evaluated using the Oxman-Guyatt Overview Quality Assessment Questionnaire for assessing the quality of systematic reviews and meta-analyses. All three meta-analyses had "minimal flaws," the highest quality rating within this system.)¹⁵ These meta-analyses report a 20% to 33% reduction in risk of death from all causes for those individuals who received more intensive follow-up (the absolute risk difference was 7%; Table 1). Table 2 summarizes the testing strategies and results of the low- and high-intensity strategies by individual study. In the trials, only two of the six randomized studies suggested significant improvement in survival for those receiving intensive follow-up.^5,9 In addition, those with more intensive surveillance had earlier documentation of recurrences, though the number of recurrences was similar comparing the control and intensive surveillance groups. Patients with more intensive surveillance were more likely to have surgery for metastatic or recurrent disease with curative intent.

	ASCO COLORECTAL CANCER FOLLOW-UP GUIDELINES

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1. History and Physical Examination and Risk Assessment
Current recommendation. Coordinating physician visits should occur every 3 to 6 months for the first 3 years, every 6 months during years 4 and 5, and subsequently at the discretion of the physician. Physician visits should focus on the initial risk assessment, followed by the implementation of a surveillance strategy and periodic counseling based on estimated risk and feasibility of surgical interventions like hepatic resection.

2005 literature update and discussion. The Panel acknowledges that the frequency, duration, and benefit of the follow-up visit itself have never been formally tested. Nevertheless, without periodic visits, the chance of detecting asymptomatic recurrences, communicating advances in genetic testing, and responding to queries within the purview of the specialist could never be done. Therefore, this discussion focuses on the interaction between the patient and doctor, the assessment of recurrence risk, as well as the system of care available to schedule and implement the plan.

While this recommendation does not represent a major departure from previous versions, the concept of a risk-based plan, and the tools to formulate it, have improved. A recently reported analysis of individual patient data from large adjuvant colon cancer randomized trials, including more than 12,915 patients, noted that 85% percent of colon cancer recurrences are diagnosed within the first 3 years after surgical resection of the primary tumor.¹² Thus, it is appropriate for the coordinating physician visits to occur every 3 to 6 months for the first 3 years after treatment, with decreased frequency thereafter for 2 years for colon cancer patients. These physician visits offer the opportunity to determine symptoms, to coordinate follow-up, and to offer counseling. Longer follow-up may be appropriate for locally advanced rectal cancer patients with poor prognostic factors based on data from two recent studies^13,16 that showed continuing risk of recurrence after 5 years. After 5 years, the need for future tests and visits are left to the discretion of the patient and physician.

During the initial discussions between patient and physician to determine an agreed-upon surveillance strategy, risk assessment should be reviewed. Recent modifications of the TNM staging system for colorectal cancer^17,18 were necessary to recognize the significant differences in survival for patients within a given stage subset. The survival difference resulting from easily measured clinical factors from several adjuvant chemotherapy trials, permitted the creation of a model able to estimate individual prognosis for individuals with stage II and III colon cancer.¹¹ Table 3 uses a Web-based adaptation of that model (available to all clinicians at http://www.mayoclinic.com/calcs)¹⁹ to estimate 5-year relapse-free survival both with and without treatment using data available on most pathology reports. While other Web-based predictive tools are available, all of them use a limited set of clinical factors to make predictions about outcome and treatment effect.²⁰

2. Laboratory Tests
Carcinoembryonic antigen: Current recommendation. Postoperative serum CEA testing should be performed every 3 months in patients with stage II or III disease for at least 3 years after diagnosis, if the patient is a candidate for surgery or systemic therapy. (Note: Adapted from the 2005 ASCO Clinical Practice Guidelines for the Use of Tumor Markers in Gastrointestinal Cancer). Since fluorouracil-based therapy may falsely elevate CEA values²⁴ waiting until adjuvant treatment is finished to initiate surveillance is advised.

Carcinoembryonic antigen: 2005 literature update and discussion. ASCO's Gastrointestinal Cancer Tumor Markers Panel will publish the rationale for this guideline (American Society of Clinical Oncology: Guideline recommendations for the use of tumor markers in gastrointestinal cancer [submitted]). The current Panel modified the frequency slightly to correspond with the suggested frequency of visits and tests.

Blood tests: Current recommendation. No change from the last update of the guideline. Routine blood tests (ie, CBCs or liver function tests) are not recommended.

Blood tests: 2005 Literature update. No relevant studies were identified from the review of the literature conducted for the update for CBCs or liver function tests.

Fecal occult blood test: Current recommendation. No change from the last update of the guideline. Periodic fecal occult blood testing is not recommended.

Fecal occult blood test: 2005 literature update. No relevant studies were identified from the review of the literature conducted for the update for fecal occult blood testing.

3. Imaging Procedures
Computed tomography (CT) in colon and rectal cancer surveillance: Current recommendation. Patients who are at higher risk of recurrence, and who could be candidates for curative-intent surgery, should undergo annual CT of the chest and abdomen for 3 years after primary therapy for colon and rectal cancer. A pelvic CT scan should be considered for rectal cancer surveillance, especially for patients who have not been treated with radiotherapy.

Computed tomography in colon and rectal cancer surveillance: 2005 Literature update and discussion. Prior ASCO guidelines recommended against CT scanning; accordingly, this update represents a significant change. The major reason why CT scanning is now recommended is that all three meta-analyses cited here in the Summary of Literature Review Results section, showed a survival benefit for CT scanning or "liver imaging." Specifically, there is a 25% lower mortality in patients undergoing liver imaging compared with nonimaging strategies. The benefit derives from the usefulness of liver resections for metastatic cancer of limited extent.

Corroborating these analyses is the recent publication by Chau et al.²⁵ These authors reported on the surveillance of 530 patients who participated in a randomized, adjuvant chemotherapy clinical trial for stage II and III colon cancer patients, who received CEA and CT scans of the chest, abdomen, and pelvis as a component of protocol-specific follow-up. A nearly identical number of relapses were detected by CEA (45 relapses) and CT scan (49 relapses), and 14 were detected by both tests. Compared with those whose relapses were detected by symptoms (65) the CT-detected group had improved survival (P = .0046). Patients who were able to undergo potentially curative surgery had improved survival and were best detected by either CT scan (26.5%) or CEA (17.8%) compared with those with symptoms (3.1%, CT v symptomatic, P < .001; CEA v symptomatic, P < .015). For comparison, Table 4 shows guidelines developed by other groups regarding liver imaging.

The cost of adding CT scanning to recurrence surveillance is not insignificant; therefore, four qualifications are important. First, there are no data that specify the frequency of CT scanning. Annual studies for three years seem reasonable based on the Chau study,²⁵ although one-third of the recurrences that occurred in the first two years presented only with symptoms (despite yearly CT scanning and CEA testing every three months). Second, CT scanning should not be routinely ordered in patients who would or could not undergo curative liver or pulmonary resection. Third, while CT scans of the abdomen and pelvis are frequently ordered together, the data do not justify routine pelvic imaging. Very few patients in the two studies that addressed this issue had curative resection based findings from a screening pelvic CT scan, even for rectal cancer.⁵ However, the Panel felt (albeit without complete agreement) that a pelvic CT should be considered for rectal cancer patients with several negative prognostic factors, especially those patients who had not undergone radiation therapy.

Fourth, the Panel did not rigidly define "higher risk." While this usually refers to a patient with a node-positive, the risk-based plan developed by the doctor and patient at the beginning of the follow-up period cannot be underemphasized. Occasionally, stage II patients with several poor risk factors will want aggressive surveillance and even higher risk patients will not. Patients with lower risk cancers who want aggressive surveillance should receive physician counseling, not more tests.

Chest X-Ray
Current recommendation. No change From the last update of the guideline. Yearly chest x-rays are not recommended.

2005 literature update and discussion. In prior versions of this guideline, there was controversy among the Panel members about the value of chest x-rays since missing resectable metastases would be unfortunate. However, since the Panel has recommended annual CT scanning of the chest and abdomen for high-risk patients who are candidates for resection, routine chest x-rays are probably not relevant.

4. Endoscopic Surveillance Techniques
Colonoscopy. Current recommendation. All patients with colon and rectal cancer should have a colonoscopy for the pre- or perioperative documentation of a cancer-and polyp-free colon. Following the surgical treatment of colorectal cancer, the Panel recommends the surveillance guideline presented by the American Gastroenterology Association (AGA)²⁶—a colonoscopy at 3 years and then, if normal, once every 5 years thereafter. For colorectal cancer patients with high-risk genetic syndromes, the physician should consider the guideline published by the AGA (Table 5).

Flexible Proctosigmoidoscopy (Rectal Cancer)
Current recommendation. For patients who have not received pelvic radiation, flexible sigmoidoscopy of the rectum every six months for 5 years is recommended.

2005 literature update. Aside from minor changes in the wording, this recommendation has not changed Since 2000

5. Laboratory-Derived Prognostic and Predictive Factors (Note. This topic is new to the guideline.)
Current recommendation. Until prospective data are available, use of molecular or cellular markers should not influence the surveillance strategy.

2005 literature summary and discussion. The explosion of new prognostic and predictive markers since the last update was felt by the Panel to warrant comment on their potential influence on follow-up testing. Retrospective subset analyses have identified a number of markers for colorectal cancer patients.²³ Examples include selected categories of molecular markers including tumor suppressor genes (18q LOH), oncogenes (c-myc), apoptosis (bcl-2) and cell suicide-related genes, transforming growth factors, epidermal growth factor receptor genes, and angiogenesis-related genes (vascular endothelial growth factor).^27-29 There are several cell proteins and carbohydrates that are potential markers for colorectal cancer, including EGF-R, L-catenin, MUC-1 mucin, and somatostatin receptors.³⁰ Investigators have also evaluated other factors such as microvessel density, DNA content, and proliferation indices as other examples.³¹ There has been little multivariate analysis evidence generated and no large hypothesis-driven prospective randomized trials to confirm the utility of these markers for prognosis, predictive value, or as a tool for risk-associated surveillance strategies. Many of these markers have been integrated in current randomized clinical trial designs that will enhance the ability to generate consistent quality-controlled laboratory data linked to clinical outcome. The ASCO Gastrointestinal Cancer Tumor Markers Panel will publish guideline recommendations for selected tumor markers.

Research Issues
Recent colon and rectal cancer clinical trial data, including emerging potential prognostic factors and modifications of the TNM staging system, have provided evidence that risk-assessment models should become a new paradigm for future clinical trial design and for treatment and surveillance strategies. Rather than assume that all stage II and stage III colon or rectal cancer patients represent a uniform population, clinical trial design must include potential prognostic and predictive factors as variables linked to outcome. For example, staging subsets, number of lymph nodes sampled, and pathologic features (eg, grade, lymph/vascular invasion) should be components of the statistical analysis.²¹ Prospective clinical trials should evaluate the importance of post-treatment surveillance strategies linked to parameters of risk assessment to define the most optimal methods to detect cancer recurrence and the impact on survival. A future goal is to define molecular or other tumor of host characteristics that will allow individualized patient strategies for both treatment choice and post-treatment surveillance.

Note
ASCO guideline policy. It is important to emphasize that guidelines and technology assessments cannot always account for individual variation among patients. They are not intended to supplant physician judgment with respect to particular patients or special clinical situations, and cannot be considered inclusive of all proper methods of care or exclusive of other treatments reasonably directed at obtaining the same result. Accordingly, ASCO considers adherence to this guideline assessment to be voluntary, with the ultimate determination regarding its application to be made by the physician in light of each patient's individual circumstances. In addition, this guideline describes the use of procedures and therapies in clinical practice; it cannot be assumed to apply to the use of these interventions performed in the context of clinical trials, given that clinical studies are designed to evaluate or validate innovative approaches in a disease for which improved staging and treatment is needed. In that guideline development involves a review and synthesis of the latest literature, a practice guideline also serves to identify important questions and settings for further research.

	Authors' Disclosures of Potential Conflicts of Interest

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Although all authors completed the disclosure declaration, the following author or immediate family members indicated a financial interest. No conflict exists for drugs or devices used in a study if they are not being evaluated as part of the investigation. For a detailed description of the disclosure categories, or for more information about ASCO's conflict of interest policy, please refer to the Author Disclosure Declaration and the Disclosures of Potential Conflicts of Interest section in Information for Contributors.

Authors Employment Leadership Consultant Stock Honoraria Research Funds Testimony Other Patrick J. Flynn Genentech (A); Sanofi (A)

Dollar Amount Codes (A) < $10,000 (B) $10,000-99,999 (C) $100,000 (N/R) Not Required

	Acknowledgment

	NOTES

 
Approved by the Board on August 9, 2005.

Authors' disclosures of potential conflicts of interest are found at the end of this article.

	REFERENCES

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