Guidelines for Colonoscopy Surveillance After Cancer Resection: A Consensus Update by the American Cancer Society and the US Multi-Society Task Force on Colorectal Cancer

Article Outline

• Abstract
• Methodology and Literature Search
• Discussion of Evidence and Rationale for the Recommendations
  • Limitations in the Selected Studies
  • Candidates for Postcancer Resection Surveillance Colonoscopy
  • Goals of Surveillance: Detection of Recurrent Cancer Versus Metachronous Cancers and Adenomas
  • Distinguishing Rectal Cancer Versus Colon Cancer Follow-up
  • Detection of Metachronous Neoplasms
• Alternatives to Colonoscopy for Surveillance
  • Key Research Questions
• References
• Copyright

Patients with resected colorectal cancer are at risk for recurrent cancer and metachronous neoplasms in the colon. This joint update of guidelines by the American Cancer Society and the US Multi-Society Task Force on Colorectal Cancer addresses only the use of endoscopy in the surveillance of these patients. Patients with endoscopically resected Stage I colorectal cancer, surgically resected Stages II and III cancers, and Stage IV cancer resected for cure (isolated hepatic or pulmonary metastasis) are candidates for endoscopic surveillance. The colorectum should be carefully cleared of synchronous neoplasia in the perioperative period. In nonobstructed colons, colonoscopy should be performed preoperatively. In obstructed colons, double-contrast barium enema or computed tomography colonography should be performed preoperatively, and colonoscopy should be performed 3 to 6 months after surgery. These steps complete the process of clearing synchronous disease. After clearing for synchronous disease, another colonoscopy should be performed in 1 year to look for metachronous lesions. This recommendation is based on reports of a high incidence of apparently metachronous second cancers in the first 2 years after resection. If the examination at 1 year is normal, then the interval before the next subsequent examination should be 3 years. If that examination is normal, then the interval before the next subsequent examination should be 5 years. Shorter intervals may be indicated by associated adenoma findings (see “Guidelines for Colonoscopy Surveillance After Polypectomy: A Consensus Update by the US Multi-Society Task Force on Colorectal Cancer and the American Cancer Society”). Shorter intervals also are indicated if the patient’s age, family history, or tumor testing indicate definite or probable hereditary nonpolyposis colorectal cancer. Patients undergoing low anterior resection of rectal cancer generally have higher rates of local cancer recurrence compared with those with colon cancer. Although effectiveness is not proven, performance of endoscopic ultrasound or flexible sigmoidoscopy at 3- to 6-month intervals for the first 2 years after resection can be considered for the purpose of detecting a surgically curable recurrence of the original rectal cancer.

Recommendations (Table 1) on the use of surveillance colonoscopy after resection of colorectal cancer were produced jointly by the US Multi-Society Task Force on Colorectal Cancer and the American Cancer Society (ACS). They constitute the updated recommendations of both organizations. The rationale for combined guidelines by organizations is discussed in the accompanying joint recommendations on postpolypectomy surveillance.¹ These guidelines were endorsed by the Colorectal Cancer Advisory Committee of the ACS and by the governing boards of the American College of Gastroenterology, the American Gastroenterological Association Institute, and the American Society for Gastrointestinal Endoscopy.

Table 1. Postcancer Resection Surveillance Colonoscopy Recommendations

1.Patients with colon and rectal cancer should undergo high-quality perioperative clearing. In the case of nonobstructing tumors, this can be done by preoperative colonoscopy. In the case of obstructing colon cancers, computed tomography colonography with intravenous contrast or double-contrast barium enema can be used to detect neoplasms in the proximal colon. In these cases, a colonoscopy to clear the colon of synchronous disease should be considered 3 to 6 months after the resection if no unresectable metastases are found during surgery. Alternatively, colonoscopy can be performed intraoperatively.

2.Patients undergoing curative resection for colon or rectal cancer should undergo a colonoscopy 1 year after the resection (or 1 year following the performance of the colonoscopy that was performed to clear the colon of synchronous disease). This colonoscopy at 1 year is in addition to the perioperative colonoscopy for synchronous tumors.

3.If the examination performed at 1 year is normal, then the interval before the next subsequent examination should be 3 years. If that colonoscopy is normal, then the interval before the next subsequent examination should be 5 years.

4.Following the examination at 1 year, the intervals before subsequent examinations may be shortened if there is evidence of hereditary nonpolyposis colorectal cancer or if adenoma findings warrant earlier colonoscopy.1

5.Periodic examination of the rectum for the purpose of identifying local recurrence, usually performed at 3- to 6-month intervals for the first 2 or 3 years, may be considered after low anterior resection of rectal cancer. The techniques utilized are typically rigid proctoscopy, flexible proctoscopy, or rectal endoscopic ultrasound. These examinations are independent of the colonoscopic examinations described above for detection of metachronous disease.

Table 2 summarizes the differences in this guideline from previous guidelines on postcancer resection surveillance colonoscopy.

Table 2. Differences Between This Guideline and Previous Guidelines on Postcancer Resection Surveillance Colonoscopy

Back to Article Outline

Methodology and Literature Search 

The literature search sought to identify randomized controlled trials and cohort studies in which patients with resected colorectal cancer and perioperative clearing of synchronous neoplasia by colonoscopy were followed to detect recurrent and/or metachronous neoplasms.

We searched the medical literature using MEDLINE (1966 to January 17, 2005), the Cochrane Database of Systematic Reviews (4th quarter 2004 update), and the Database of Abstracts of Reviews of Effects (4th quarter 2004 update). In MEDLINE, subject headings for colorectal neoplasms were combined with subheadings and key words for “surgery,” “resection,” “colonoscopy,” “surveillance,” and “follow-up” to identify relevant citations. Only studies published in the English language were included. Surveillance studies in patients with inflammatory bowel disease or hereditary nonpolyposis colorectal cancer specifically were excluded. Key word searches also were performed in the Cochrane Database of Systematic Reviews and the Database of Abstracts of Reviews of Effects to identify any additional systematic reviews. In addition, a manual search was performed using references from retrieved reports, review articles, guidelines, meta-analyses, editorials, and textbooks of gastroenterology.

We excluded articles if there was no evidence of perioperative colonoscopic clearing, or if a modality other than colonoscopy (flexible sigmoidoscopy, barium enema) was used for perioperative clearing.

A total of 66 studies were retrieved for detailed evaluation, and 43 were excluded: 26 because of incomplete perioperative colonoscopic clearing or because this was accomplished with modalities other than colonoscopy, 13 did not pertain to the focus of our paper, 3 were reports of works in progress that were published in final form in other studies included in our analysis, and 1 reported the preliminary results of an ongoing trial. The remaining 23 studies were included in our analysis.², ³, ⁴, ⁵, ⁶, ⁷, ⁸, ⁹, ¹⁰, ¹¹, ¹², ¹³, ¹⁴, ¹⁵, ¹⁶, ¹⁷, ¹⁸, ¹⁹, ²⁰, ²¹, ²², ²³, ²⁴

Evidence tables were created to summarize the studies and were circulated to members of the US Multi-Society Task Force and the ACS Colorectal Cancer Advisory Committee. The evidence was reviewed and recommendations developed at a joint meeting.

Back to Article Outline

Discussion of Evidence and Rationale for the Recommendations 

Limitations in the Selected Studies 

Some limitations were identified in interpreting the selected studies on postcancer surveillance colonoscopy literature.², ³, ⁴, ⁵, ⁶, ⁷, ⁸, ⁹, ¹⁰, ¹¹, ¹², ¹³, ¹⁴, ¹⁵, ¹⁶, ¹⁷, ¹⁸, ¹⁹, ²⁰, ²¹, ²², ²³, ²⁴ For example, the term “metachronous cancer” had variable definitions. In some instances it was based on the site of tumor appearance within the colon and in others it was based on time after resection of the initial primary. Many studies made no mention of whether patients may have had hereditary nonpolyposis colorectal cancer. In some cohorts, there was incomplete follow-up evaluation of patients. Surveillance intervals were different across studies. Some studies did not clearly separate metachronous tumors from anastomotic recurrences or anastomotic from local or regional recurrences. In some cases there also was a failure to report the stage of metachronous cancers and whether or not they were resectable for cure at the time they were diagnosed. In some studies, it was not clear whether colonoscopies were routine procedures in asymptomatic surveillance patients vs diagnostic procedures based on symptoms or laboratory findings. Colonoscopy completion rates and complication rates were commonly not reported, and there was also frequently a lack of information on mortality rates. Despite these limitations, a number of clinically relevant trends are evident regarding colorectal cancer recurrence, metachronous cancer, and the utility of surveillance procedures in patients with resected colorectal cancer.

Candidates for Postcancer Resection Surveillance Colonoscopy 

In general, patients who undergo surgical resection of Stage I, II, or III colon and rectal cancers or curative-intent resection of Stage IV cancers are candidates for surveillance colonoscopy. Patients who undergo curative endoscopic resection of Stage I colon cancers are also candidates for surveillance colonoscopy. Patients with Stage IV colon or rectal cancer that is unresectable for cure are generally not candidates for surveillance colonoscopy because their chance of survival from their primary cancer is low, and the risks of surveillance outweigh any potential benefit.

Goals of Surveillance: Detection of Recurrent Cancer Versus Metachronous Cancers and Adenomas 

There are 2 fundamental goals of surveillance of patients with resected colon or rectal cancer. One goal is the detection of early recurrences of the initial primary cancer at a stage that would allow curative treatment. The second goal is detection of metachronous colorectal neoplasms. In regard to detection of recurrences of the initial primary cancer, serial measurements of carcinoembryonic antigen are used widely.²⁵ In addition, recent meta-analyses of randomized controlled trials suggest that annual chest x-rays and computed tomography (CT) scans of the liver can improve survival from the original primary cancer by early detection of surgically curable recurrences.²⁶ The roles of serial performance of serum carcinoembryonic antigen measurements, serial chest radiographs, and CT scans of the liver are not reviewed here. Neither individual randomized controlled trials of intensive surveillance with colonoscopy²⁰ nor meta-analyses of these trials²⁶ have shown a survival benefit from the original primary tumor by performing colonoscopy at annual or shorter intervals. The failure of surveillance endoscopic examinations to improve survival from recurrent colorectal cancer appears to result from relatively low rates of anastomotic or intraluminal recurrence and the observation that anastomotic or intraluminal recurrences are generally associated with intra-abdominal or pelvic disease that is unresectable for cure.², ³, ⁴, ⁵, ⁶, ⁷, ⁸, ⁹, ¹⁰, ¹¹, ¹², ¹³, ¹⁴, ¹⁵, ¹⁶, ¹⁷, ¹⁸, ¹⁹, ²⁰, ²¹, ²², ²³, ²⁴, ²⁶, ²⁷ In summary, performance of annual colonoscopy for the purpose of detecting recurrent disease does not have an established survival benefit for patients with colorectal cancer. (However, as noted below, there is a rationale for surveillance of the rectum after resection of rectal cancer for the detection of local recurrence.) The primary goal of surveillance colonoscopy after resection of colorectal cancer is the detection of metachronous neoplasms.

Distinguishing Rectal Cancer Versus Colon Cancer Follow-up 

Although there is no established benefit from endoscopic surveillance for the purpose of detecting early recurrences of the original cancer, in clinical practice many clinicians distinguish between rectal and colon cancer in this regard. The distinction is based on differences in the rates of local recurrence of rectal vs colon cancer. Specifically, in the case of colon cancer, recurrence at the anastomosis occurs in only 2%–4% of patients.², ³, ⁴, ⁵, ⁶, ⁷, ⁸, ⁹, ¹⁰, ¹¹, ¹², ¹³, ¹⁴, ¹⁵, ¹⁶, ¹⁷, ¹⁸, ¹⁹, ²⁰, ²¹, ²², ²³, ²⁴ Because the overwhelming majority of patients with endoscopically detected anastomotic recurrences in the colon are unresectable for cure, surveillance colonoscopy for this purpose generally should not be undertaken. On the other hand, local recurrence rates of rectal cancer can be 10 or more times higher.²⁸, ²⁹, ³⁰, ³¹, ³², ³³

High recurrence rates of rectal cancer are partly a function of surgical technique and volume.²⁸, ²⁹, ³⁰, ³¹, ³², ³³ Specifically, recurrence rates less than 10% have been reported consistently when patients undergo surgery by a technique called total mesorectal excision.³⁴, ³⁵, ³⁶ This technique involves sharp dissection of the rectum and its surrounding adventitia along the first plane outside the adventitia (the mesorectal fascia).³⁵, ³⁶ The technique can be performed using either an open or laparoscopic-assisted approach³⁷, ³⁸, ³⁹, ⁴⁰ and has been reported to allow higher rates of successful low anterior resection⁴⁰ and lower rates of postoperative sexual dysfunction in men.⁴¹

Local recurrence rates of rectal cancer can also be reduced by administration of chemotherapy and radiation therapy,³⁴ which have been most effectively administered in the neoadjuvant (preoperative) setting to patients with locally advanced disease. Patients with rectal cancer typically undergo preoperative staging, either by endoscopic ultrasound⁴², ⁴³, ⁴⁴ or magnetic resonance imaging,⁴⁵, ⁴⁶, ⁴⁷, ⁴⁸ followed by neoadjuvant chemoradiation in selected patients.⁴⁹ The combination of neoadjuvant chemoradiation and resection by surgeons trained in total mesorectal excision has resulted in very low recurrence rates for rectal cancer.³⁴ Because local recurrence rates for rectal cancer across the United States are generally higher than those achieved in series using total mesorectal excision, there is a rationale for performing periodic examinations of the rectum by rigid or flexible proctoscopy or endoscopic ultrasound. These techniques have not been shown to improve survival and the only rationale for their use is high rates of local recurrence.

When colon or rectal cancer is resected endoscopically and surgical resection is not planned because of favorable histology⁵⁰ and/or increased surgical risk, a follow-up endoscopic examination to inspect and biopsy the resection site is reasonable.⁵¹ The follow-up examination is considered standard in the case of a sessile malignant polyp removed by piecemeal resection.¹ These examinations typically are performed 3–6 months after the initial endoscopic resection.

Detection of Metachronous Neoplasms 

A second potential benefit of surveillance colonoscopy is the detection of metachronous cancers at a surgically curable stage, as well as the prevention of metachronous cancers via identification and removal of adenomatous polyps. The incidence of metachronous cancers, the timing at which metachronous cancers occur, and the stage of these cancers at presentation or identification by surveillance colonoscopy should determine the optimal intervals for performance of surveillance colonoscopy directed toward metachronous disease. The evidence from published studies of postcancer resection surveillance in colonoscopy was reviewed to determine what these rates and timing of metachronous cancers are (Table 3). Limitations in interpretation of this literature were described earlier.

Table 3. Metachronous Cancers in Postcancer Resection Surveillance Colonoscopy Studies

From 2% to 7% of patients with colorectal cancer have 1 or more synchronous cancers in the colon and rectum at the time of initial diagnosis.³, ⁴, ¹³, ²⁴, ⁵², ⁵³ From a practical perspective, it is impossible to differentiate whether apparent metachronous cancers appearing in the interval shortly after resection of colorectal cancer are true metachronous lesions or missed synchronous lesions. Provided that appropriate clearing of the colon is achieved in the perioperative period, all subsequently identified cancers are, for practical purposes, metachronous lesions.

Among 23 studies in which patients underwent perioperative clearing by colonoscopy, there were 9029 patients in whom 137 apparent metachronous cancers developed.², ³, ⁴, ⁵, ⁶, ⁷, ⁸, ⁹, ¹⁰, ¹¹, ¹², ¹³, ¹⁴, ¹⁵, ¹⁶, ¹⁷, ¹⁸, ¹⁹, ²⁰, ²¹, ²², ²³, ²⁴ Among studies in which the number of colonoscopies performed could be determined, 9407 colonoscopies were performed to detect 60 metachronous cancers in 2706 patients.⁴, ⁸, ¹⁰, ¹¹, ¹³, ¹⁵, ²⁰, ²¹, ²³, ²⁴ This is a rate of 157 colonoscopies per metachronous cancer detected, which compares favorably with the rate of prevalent cancers detected during screening colonoscopy. Thus, among 4 screening colonoscopy studies in patients age 50 and older,⁵⁴, ⁵⁵, ⁵⁶, ⁵⁷ the number of colonoscopies needed to detect 1 invasive cancer was 135. Excluding reference 55, which was performed in male veterans (a group expected to have a higher prevalence of neoplasia), 156 colonoscopies were performed per invasive cancer detected in the remaining 3 studies.⁵⁴, ⁵⁶, ⁵⁷

Among studies of postcancer resection surveillance colonoscopy, there were 57 metachronous cancers in the first 2 years after resection of the initial primary, with an incidence rate of .7% over this interval. This estimate is consistent with a review of tumor registries in Nebraska, which calculated an annual incidence for metachronous cancers of .35% per year.⁵⁸ When reported, 69 of 106 (65%) metachronous cancers were Dukes’ stage A or B,², ⁸, ⁹, ¹⁰, ¹³, ²⁰, ²³, ²⁴ 29 of 52 (56%) were asymptomatic,², ⁶, ⁸, ¹⁰, ¹², ¹⁸, ²⁰ and 62 of 71 (87%) had surgery for cure.², ⁶, ⁸, ¹⁰, ¹², ¹³, ¹⁴, ²³, ²⁴ Taken together, these findings were considered sufficient to warrant a colonoscopy 1 year after resection or after the perioperative clearing colonoscopy for the purpose of identification of apparently metachronous colorectal neoplasms. The recommendation to perform a colonoscopy at 1 year does not diminish the need for high quality in the performance of the perioperative clearing examination(s) for synchronous neoplasms.

Back to Article Outline

Alternatives to Colonoscopy for Surveillance 

Colonoscopy is considered the test of choice for detection of metachronous neoplasms in the postcancer resection surveillance colonoscopy setting (Table 4). Double-contrast barium enema was less sensitive than colonoscopy for large and small polyp detection after resection of adenomas.⁵⁹

Table 4. Additional Recommendations Regarding Postcancer Resection Surveillance Colonoscopy

1.These recommendations assume that colonoscopy is complete to the cecum and that bowel preparation is adequate

2.There is clear evidence that the quality of examinations is highly variable; continuous quality improvement process is critical to the effective application of colonoscopy in colorectal cancer prevention50

3.Endoscopists should make clear recommendations to primary care physicians about when the next colonoscopy is indicated

4.Performance of fecal occult blood text is discouraged in patients undergoing colonoscopic surveillance

5.Discontinuation of surveillance colonoscopy should be considered in persons with advanced age or comorbidities (<10 years life expectancy), according to the clinician’s judgment

6.Surveillance guidelines are intended for asymptomatic people; new symptoms may need diagnostic work-up

7.Chromoendoscopy (dye-spraying) and magnification endoscopy are not established as essential to screening or surveillance

8.Computed tomography colonography (virtual colonoscopy) is not established as a surveillance modality

CT colonography has not been evaluated adequately in the surveillance setting, and results for polyp detection are quite mixed.⁶⁰, ⁶¹, ⁶², ⁶³ Guaiac-based fecal occult blood testing generally has been considered to have very low positive predictive value after clearing colonoscopy. This was confirmed for the first 5 years after colonoscopy in a recent large study.⁶⁴ Immunochemical fecal occult blood testing warrants additional evaluation as an adjunct to colonoscopy⁶⁵ in this setting. Fecal DNA testing⁶⁶ has not been evaluated for postcancer resection surveillance and is not recommended for this indication.

Key Research Questions 

There are a number of questions that cannot be addressed fully by currently available evidence. Some of these key research questions are listed in Table 5.⁵⁵

Table 5. Key Research Questions Regarding Surveillance of the Colorectum After Resection of Colorectal Cancer

1.What clinical, genetic, or biologic markers predict development of metachronous cancers (ie, stratify risk) in colorectal cancer patients without hereditary nonpolyposis colorectal cancer?

2.Are new colorectal cancers in the short-term interval after surgical resection true metachronous cancers or missed synchronous lesions?

3.Do follow-up procedures (flexible sigmoidoscopy, endoscopic ultrasound) after resection of rectal cancer improve any outcomes?

4.Should the treatment of rectal cancer (eg, neoadjuvant chemoradiation, total mesorectal excision) influence whether follow-up evaluation for local recurrence is justified?

5.Should adjunctive testing (eg, immunochemical fecal occult blood testing) be added to colonoscopy in the surveillance of patients who have undergone resection of colorectal cancer?

Back to Article Outline

References 

1. Winawer SJ, Zauber AG, Fletcher RH, Stillman JS, O’Brien MJ, Levin B, et al. Guidelines for Colonoscopy Surveillance After Polypectomy (a consensus update by the US Multi-Society Task Force on Colorectal Cancer and the American Cancer Society) . Gastroenterology . 2006;130:1872–1885
   • View In Article
   • Abstract
   • Full Text
   • Full-Text PDF (251 KB)
   • CrossRef
2. Barillari P , Ramacciato G , Manetti G , Bovino A , Sammartino P , Stipa V . Surveillance of colorectal cancer (effectiveness of early detection of intraluminal recurrences on prognosis and survival of patients treated for cure) . Dis Colon Rectum . 1996;39:388–393
   • View In Article
   • MEDLINE
   • CrossRef
3. Barrier A , Houry S , Huguier M . The appropriate use of colonoscopy in the curative management of colorectal cancer . Int J Colorectal Dis . 1998;13:93–98
   • View In Article
   • MEDLINE
   • CrossRef
4. Carlsson G , Petrelli NJ , Nava H , Herrera L , Mittelman A . The value of colonoscopic surveillance after curative resection for colorectal cancer or synchronous adenomatous polyps . Arch Surg . 1987;122:1261–1263
   • View In Article
   • MEDLINE
5. Castells A, Bessa X, Daniels M, Ascaso C, Lacy AM, Garcia-Valdecasas JC, et al. Value of postoperative surveillance after radical surgery for colorectal cancer (results of a cohort study) . Dis Colon Rectum . 1998;41:714–724
   • View In Article
   • MEDLINE
   • CrossRef
6. Chen F , Stuart M . Colonoscopic follow-up of colorectal carcinoma . Dis Colon Rectum . 1994;37:568–572
   • View In Article
   • MEDLINE
   • CrossRef
7. Eckardt VF , Stamm H , Kanzler G , Bernhard G . Improved survival after colorectal cancer in patients complying with a postoperative endoscopic surveillance program . Endoscopy . 1994;26:523–527
   • View In Article
   • MEDLINE
   • CrossRef
8. Granqvist S , Karlsson T . Postoperative follow-up of patients with colorectal carcinoma by colonoscopy . Eur J Surg . 1992;158:307–312
   • View In Article
   • MEDLINE
9. Green RJ, Metlay JP, Propert K, Catalano PJ, Macdonald JS, Mayer RJ, et al. Surveillance for second primary colorectal cancer after adjuvant chemotherapy (an analysis of Intergroup 0089) . Ann Intern Med . 2002;136:261–269
   • View In Article
10. Juhl G , Larson GM , Mullins R , Bond S , Polk HC . Six-year results of annual colonoscopy after resection of colorectal cancer . World J Surg . 1990;14:255–261
    • View In Article
    • MEDLINE
    • CrossRef
11. Khoury DA , Opelka FG , Beck DE , Hicks TC , Timmcke AE , Gathright JB . Colon surveillance after colorectal cancer surgery . Dis Colon Rectum . 1996;39:252–256
    • View In Article
    • MEDLINE
    • CrossRef
12. Kjeldsen BJ , Kronborg O , Fenger C , Jorgensen OD . A prospective randomized study of follow-up after radical surgery for colorectal cancer . Br J Surg . 1997;84:666–669
    • View In Article
    • MEDLINE
    • CrossRef
13. Kronborg O , Hage E , Deichgraeber E . The remaining colon after radical surgery for colorectal cancer. The first three years of a prospective study . Dis Colon Rectum . 1983;26:172–176
    • View In Article
    • MEDLINE
    • CrossRef
14. Makela JT , Laitinen SO , Kairaluoma MI . Five-year follow-up after radical surgery for colorectal cancer. Results of a prospective randomized trial . Arch Surg . 1995;130:1062–1067
    • View In Article
    • MEDLINE
15. McFarland RJ , Becciolini C , Lallemand RC . The value of colonoscopic surveillance following a diagnosis of colorectal cancer or adenomatous polyp . Eur J Surg Oncol . 1991;17:514–518
    • View In Article
    • MEDLINE
16. Obrand DI , Gordon PH . Incidence and patterns of recurrence following curative resection for colorectal carcinoma . Dis Colon Rectum . 1997;40:15–24
    • View In Article
    • MEDLINE
    • CrossRef
17. Ohlsson B , Breland U , Ekberg H , Graffner H , Tranberg KG . Follow-up after curative surgery for colorectal carcinoma. Randomized comparison with no follow-up . Dis Colon Rectum . 1995;38:619–626
    • View In Article
    • MEDLINE
    • CrossRef
18. Patchett SE , Mulcahy HE , O’Donoghue DP . Colonoscopic surveillance after curative resection for colorectal cancer . Br J Surg . 1993;80:1330–1332
    • View In Article
    • MEDLINE
    • CrossRef
19. Pietra N , Sarli L , Costi R , Ouchemi C , Grattarola M , Peracchia A . Role of follow-up in management of local recurrences of colorectal cancer (a prospective, randomized study) . Dis Colon Rectum . 1998;41:1127–1133
    • View In Article
    • MEDLINE
    • CrossRef
20. Schoemaker D , Black R , Giles L , Toouli J . Yearly colonoscopy, liver CT, and chest radiography do not influence 5-year survival of colorectal cancer patients . Gastroenterology . 1998;114:7–14
    • View In Article
    • Abstract
    • Full Text
    • Full-Text PDF (141 KB)
    • CrossRef
21. Skaife P , Seow-Choen F , Eu KW , Tang CL . A novel indicator for surveillance colonoscopy following colorectal cancer resection . Colorectal Dis . 2003;5:45–48
    • View In Article
    • MEDLINE
    • CrossRef
22. Stigliano V, Fracasso P, Grassi A, Lapenta R, Citarda F, Tomaselli G, et al. Endoscopic follow-up in resected colorectal cancer patients . J Exp Clin Cancer Res . 2000;19:145–148
    • View In Article
    • MEDLINE
23. Togashi K, Konishi F, Ozawa A, Sato T, Shito K, Kashiwagi H, et al. Predictive factors for detecting colorectal carcinomas in surveillance colonoscopy after colorectal cancer surgery . Dis Colon Rectum . 2000;43:S47–S53
    • View In Article
    • MEDLINE
    • CrossRef
24. Weber CA , Deveney KE , Pellegrini CA , Way LW . Routine colonoscopy in the management of colorectal carcinoma . Am J Surg . 1986;152:87–92
    • View In Article
    • MEDLINE
    • CrossRef
25. Benson AB, Desch CE, Flynn PJ, Krause C, Loprinzi CL, Minsky BD, et al. 2000 update of American Society of Clinical Oncology colorectal cancer surveillance guidelines . J Clin Oncol . 2000;18:3586–3588
    • View In Article
    • MEDLINE
26. Renehan AG , Egger M , Saunders MP , O’Dwyer ST . Impact on survival of intensive follow up after curative resection for colorectal cancer (systematic review and meta-analysis of randomised trials) . Br Med J . 2002;324:813
    • View In Article
27. Jeffery GM , Hickey BE , Hider P . Follow-up strategies for patients treated for non-metastatic colorectal cancer . Cochrane Database Syst Rev . 2002;CD002200
    • View In Article
28. Holm T , Johansson H , Cedermark B , Ekelund G , Rutqvist LE . Influence of hospital- and surgeon-related factors on outcome after treatment of rectal cancer with or without preoperative radiotherapy . Br J Surg . 1997;84:657–663
    • View In Article
    • MEDLINE
    • CrossRef
29. Porter GA , Soskolne CL , Yakimets WW , Newman SC . Surgeon-related factors and outcome in rectal cancer . Ann Surg . 1998;227:157–167
    • View In Article
    • MEDLINE
    • CrossRef
30. McArdle CS , Hole D . Impact of variability among surgeons on postoperative morbidity and mortality and ultimate survival . Br Med J . 1991;302:1501–1505
    • View In Article
31. Steele RJ . The influence of surgeon case volume on outcome in site-specific cancer surgery . Eur J Surg Oncol . 1996;22:211–213
    • View In Article
    • Abstract
    • Full-Text PDF (303 KB)
    • CrossRef
32. Harmon JW, Tang DG, Gordon TA, Bowman HM, Choti MA, Kaufman HS, et al. Hospital volume can serve as a surrogate for surgeon volume for achieving excellent outcomes in colorectal resection . Ann Surg . 1999;230:404–413
    • View In Article
    • MEDLINE
    • CrossRef
33. Panageas KS , Schrag D , Riedel E , Bach PB , Begg CB . The effect of clustering of outcomes on the association of procedure volume and surgical outcomes . Ann Intern Med . 2003;139:658–665
    • View In Article
34. Kapiteijn E, Marijnen CA, Nagtegaal ID, Putter H, Steup WH, Wiggers T, et al. Dutch Colorectal Cancer G Preoperative radiotherapy combined with total mesorectal excision for resectable rectal cancer . N Engl J Med . 2001;345:638–646
    • View In Article
    • MEDLINE
    • CrossRef
35. Heald RJ , Husband EM , Ryall RD . The mesorectum in rectal cancer surgery—the clue to pelvic recurrence? . Br J Surg . 1982;69:613–616
    • View In Article
    • MEDLINE
    • CrossRef
36. Cawthorn SJ, Parums DV, Gibbs NM, A’Hern RP, Caffarey SM, Broughton CI, et al. Extent of mesorectal spread and involvement of lateral resection margin as prognostic factors after surgery for rectal cancer . Lancet . 1990;335:1055–1059
    • View In Article
    • Abstract
    • CrossRef
37. Fleshman JW, Wexner SD, Anvari M, LaTulippe JF, Birnbaum EH, Kodner IJ, et al. Laparoscopic vs. open abdominoperineal resection for cancer . Dis Colon Rectum . 1999;42:930–939
    • View In Article
    • MEDLINE
    • CrossRef
38. Kwok SP , Lau WY , Carey PD , Kelly SB , Leung KL , Li AK . Prospective evaluation of laparoscopic-assisted large bowel excision for cancer . Ann Surg . 1996;223:170–176
    • View In Article
    • MEDLINE
    • CrossRef
39. Leung KL, Kwok SP, Lam SC, Lee JF, Yiu RY, Ng SS, et al. Laparoscopic resection of rectosigmoid carcinoma (prospective randomised trial) . Lancet . 2004;363:1187–1192
    • View In Article
    • Abstract
    • Full Text
    • Full-Text PDF (107 KB)
    • CrossRef
40. Stockholm Colorectal Cancer Study Group, Basingstoke Bowel Cancer Research Project Martling AL , Holm T , Rutqvist LE , Moran BJ , Heald RJ , Cedemark B . Effect of a surgical training programme on outcome of rectal cancer in the County of Stockholm . Lancet . 2000;356:93–96
    • View In Article
    • Abstract
    • Full Text
    • Full-Text PDF (81 KB)
    • CrossRef
41. Maurer CA , Z’Graggen K , Renzulli P , Schilling MK , Netzer P , Buchler MW . Total mesorectal excision preserves male genital function compared with conventional rectal cancer surgery . Br J Surg . 2001;88:1501–1505
    • View In Article
    • MEDLINE
    • CrossRef
42. Fleshman JW , Myerson RJ , Fry RD , Kodner IJ . Accuracy of transrectal ultrasound in predicting pathologic stage of rectal cancer before and after preoperative radiation therapy . Dis Colon Rectum . 1992;35:823–829
    • View In Article
    • MEDLINE
    • CrossRef
43. Gualdi GF , Casciani E , Guadalaxara A , d’Orta C , Polettini E , Pappalardo G . Local staging of rectal cancer with transrectal ultrasound and endorectal magnetic resonance imaging (comparison with histologic findings) . Dis Colon Rectum . 2000;43:338–345
    • View In Article
    • MEDLINE
    • CrossRef
44. Hunerbein M , Pegios W , Rau B , Vogl TJ , Felix R , Schlag PM . Prospective comparison of endorectal ultrasound, three-dimensional endorectal ultrasound, and endorectal MRI in the preoperative evaluation of rectal tumors. Preliminary results . Surg Endosc . 2000;14:1005–1009
    • View In Article
    • CrossRef
45. Mathur P, Smith JJ, Ramsey C, Owen M, Thorpe A, Karim S, et al. Comparison of CT and MRI in the pre-operative staging of rectal adenocarcinoma and prediction of circumferential resection margin involvement by MRI . Colorectal Dis . 2003;5:396–401
    • View In Article
    • MEDLINE
    • CrossRef
46. Beets-Tan RG . MRI in rectal cancer (the T stage and circumferential resection margin) . Colorectal Dis . 2003;5:392–395
    • View In Article
    • MEDLINE
    • CrossRef
47. Radcliffe A , Brown G . Will MRI provide maps of lines of excision for rectal cancer? . Lancet . 2001;357:495–496
    • View In Article
    • Full Text
    • Full-Text PDF (53 KB)
    • CrossRef
48. Beets-Tan RG, Beets GL, Vliegen RF, Kessels AG, Van Boven H, De Bruine A, et al. Accuracy of magnetic resonance imaging in prediction of tumour-free resection margin in rectal cancer surgery . Lancet . 2001;357:497–504
    • View In Article
    • Abstract
    • Full Text
    • Full-Text PDF (2711 KB)
    • CrossRef
49. Sauer R, Becker H, Hohenberger W, Rodel C, Wittekind C, Fietkau R, et al. Preoperative versus postoperative chemoradiotherapy for rectal cancer . N Engl J Med . 2004;351:1731–1740
    • View In Article
    • CrossRef
50. Rex D , Cummings O , Ulbright T . Coming to terms with pathologists over colon polyps with cancer or high-grade dysplasia . J Clin Gastroenterol . 2005;39:1–3
    • View In Article
    • MEDLINE
51. Practice parameters Committee of the American College of Gastroenterology Bond JH . Polyp guideline (diagnosis, treatment, and surveillance for patients with colorectal polyps) . Am J Gastroenterol . 2000;95:3053–3063
    • View In Article
    • MEDLINE
    • CrossRef
52. Langevin JM , Nivatvongs S . The true incidence of synchronous cancer of the large bowel. A prospective study . Am J Surg . 1984;147:330–333
    • View In Article
    • MEDLINE
    • CrossRef
53. Pagana TJ , Ledesma EJ , Mittelman A , Nava HR . The use of colonoscopy in the study of synchronous colorectal neoplasms . Cancer . 1984;53:356–359
    • View In Article
    • MEDLINE
    • CrossRef
54. Rex D, Sledge G, Harper P, Ulbright T, Loehrer P, Helper D, et al. Colonic neoplasia in asymptomatic persons with negative fecal occult blood tests (influence of age, gender, and family history) . Am J Gastroenterol . 1993;88:825–831
    • View In Article
    • MEDLINE
55. Lieberman D , Weiss D , Bond J , Ahnen D , Garewal H , Chejfec G . 380. VACSG. Use of colonoscopy to screen asymptomatic adults for colorectal cancer . N Engl J Med . 2000;343:162–168
    • View In Article
    • MEDLINE
    • CrossRef
56. Imperiale T , Wagner D , Lin C , Larkin G , Rogge J , Ransohoff D . Risk of advanced proximal neoplasms in asymptomatic adults according to the distal colorectal findings . N Engl J Med . 2000;343:169–174
    • View In Article
    • MEDLINE
    • CrossRef
57. Imperiale TF , Ransohoff DF , Itzkowitz SH , Turnbull BA , Ross ME  Colorectal Cancer Study G . Fecal DNA versus fecal occult blood for colorectal-cancer screening in an average-risk population . N Engl J Med . 2004;351:2704–2714
    • View In Article
    • CrossRef
58. Cali RL, Pitsch RM, Thorson AG, Watson P, Tapia P, Blatchford GJ, et al. Cumulative incidence of metachronous colorectal cancer . Dis Colon Rectum . 1993;36:388–393
    • View In Article
    • MEDLINE
    • CrossRef
59. Winawer SJ, Stewart ET, Zauber AG, Bond JH, Ansel H, Waye JD, et al. A comparison of colonoscopy and double-contrast barium enema for surveillance after polypectomy . N Engl J Med . 2000;342:1766–1772
    • View In Article
    • MEDLINE
    • CrossRef
60. Rockey D , Paulson E , Favis W , et al.   Multicenter prospective comparison of colon imaging tests . (abstr) Gastroenterology . 2004;126:A2004
    • View In Article
61. Johnson CD, Harmsen WS, Wilson LA, McCarty RL, Welch TJ, Ilstrup DM, et al. Prospective blinded evaluation of computed tomographic colonography for screen detection of colorectal polyps . Gastroenterology . 2003;125:311–319
    • View In Article
    • Abstract
    • Full Text
    • Full-Text PDF (111 KB)
    • CrossRef
62. Cotton PB, Durkalski VL, Pineau BC, Palesch YY, Mauldin PD, Hoffman B, et al  Computed tomographic colonography (virtual colonoscopy). A multicenter comparison with standard colonoscopy for detection of colorectal neoplasia . JAMA . 2004;291:1713–1719
    • View In Article
    • CrossRef
63. Pickhardt PJ, Choi JR, Hwang I, Butler JA, Puckett ML, Hildebrandt HA, et al. Computed tomographic virtual colonoscopy to screen for colorectal neoplasia in asymptomatic adults . N Engl J Med . 2003;349:2191–2200
    • View In Article
    • CrossRef
64. Finkelstein S , Bini EJ . Annual fecal occult blood testing can be safely suspended for up to 5 years after a negative colonoscopy in asymptomatic average-risk patients . Gastrointest Endosc . 2005;61:AB250
    • View In Article
    • Full Text
    • Full-Text PDF (63 KB)
    • CrossRef
65. Bampton PA, Sandford JJ, Cole SR, Smith A, Marcon J, Cadd B, et al. Interval faecal occult blood testing in a colonoscopy based screening programme detects additional pathology . Gut . 2005;54:803–806
    • View In Article
    • MEDLINE
    • CrossRef
66. Imperiale TF , Ransohoff DF , Itzkowitz SH , Turnbull BA , Ross ME . Fecal DNA versus fecal occult blood for colorectal-cancer screening in an average-risk population . N Engl J Med . 2004;351:2704–2714
    • View In Article
    • CrossRef