2015-04-13 02:40:21 UTC

Colonoscopy After Cancer Resection

Colonoscopy Surveillance After Cancer Resection

Download PDF

 

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.1x1Winawer, S.J., Zauber, A.G., Fletcher, R.H., Stillman, J.S., O'Brien, M.J., Levin, B., Smith, R.A., Lieberman, D.A., Burt, R.W., Levin, T.R., Bond, J.H., Brooks, D., Byers, T., Hyman, N., Kirk, L., Thorson, A., Simmang, C., Johnson, D., and Rex, D.K. 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

Abstract | Full Text | Full Text PDF | PubMed | Scopus (450)
See all References
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 1Postcancer 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.1x1Winawer, S.J., Zauber, A.G., Fletcher, R.H., Stillman, J.S., O'Brien, M.J., Levin, B., Smith, R.A., Lieberman, D.A., Burt, R.W., Levin, T.R., Bond, J.H., Brooks, D., Byers, T., Hyman, N., Kirk, L., Thorson, A., Simmang, C., Johnson, D., and Rex, D.K. 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

Abstract | Full Text | Full Text PDF | PubMed | Scopus (450)
See all References
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 2Differences Between This Guideline and Previous Guidelines on Postcancer Resection Surveillance Colonoscopy
In addition to careful perioperative clearing of the colorectum for synchronous lesions, a colonoscopy is recommended 1 year after surgical resection because of high yields of detecting early second, apparently metachronous cancers
Clinicians can consider periodic examination of the rectum for the purpose of identifying local recurrence after low anterior resection of rectal cancer

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.2x2Barillari, P., Ramacciato, G., Manetti, G., Bovino, A., Sammartino, P., and 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

CrossRef | PubMed | Scopus (49)
See all References
, 3x3Barrier, A., Houry, S., and Huguier, M. The appropriate use of colonoscopy in the curative management of colorectal cancer. Int J Colorectal Dis. 1998; 13: 93—98

CrossRef | PubMed | Scopus (25)
See all References
, 4x4Carlsson, G., Petrelli, N.J., Nava, H., Herrera, L., and Mittelman, A. The value of colonoscopic surveillance after curative resection for colorectal cancer or synchronous adenomatous polyps. Arch Surg. 1987; 122: 1261—1263

CrossRef | PubMed
See all References
, 5x5Castells, A., Bessa, X., Daniels, M., Ascaso, C., Lacy, A.M., Garcia-Valdecasas, J.C., Gargallo, L., Novell, F., Astudillo, E., Filella, X., and Pique, J.M. Value of postoperative surveillance after radical surgery for colorectal cancer (results of a cohort study) . Dis Colon Rectum. 1998; 41: 714—724

CrossRef | PubMed | Scopus (81)
See all References
, 6x6Chen, F. and Stuart, M. Colonoscopic follow-up of colorectal carcinoma. Dis Colon Rectum. 1994; 37: 568—572

CrossRef | PubMed | Scopus (48)
See all References
, 7x7Eckardt, V.F., Stamm, H., Kanzler, G., and Bernhard, G. Improved survival after colorectal cancer in patients complying with a postoperative endoscopic surveillance program. Endoscopy. 1994; 26: 523—527

CrossRef | PubMed
See all References
, 8x8Granqvist, S. and Karlsson, T. Postoperative follow-up of patients with colorectal carcinoma by colonoscopy. Eur J Surg. 1992; 158: 307—312

PubMed
See all References
, 9x9Green, R.J., Metlay, J.P., Propert, K., Catalano, P.J., Macdonald, J.S., Mayer, R.J., and Haller, D.G. Surveillance for second primary colorectal cancer after adjuvant chemotherapy (an analysis of Intergroup 0089) . Ann Intern Med. 2002; 136: 261—269

CrossRef | PubMed
See all References
, 10x10Juhl, G., Larson, G.M., Mullins, R., Bond, S., and Polk, H.C. Jr. Six-year results of annual colonoscopy after resection of colorectal cancer. World J Surg. 1990; 14: 255—261

CrossRef | PubMed | Scopus (51)
See all References
, 11x11Khoury, D.A., Opelka, F.G., Beck, D.E., Hicks, T.C., Timmcke, A.E., and Gathright, J.B. Jr. Colon surveillance after colorectal cancer surgery. Dis Colon Rectum. 1996; 39: 252—256

CrossRef | PubMed | Scopus (35)
See all References
, 12x12Kjeldsen, B.J., Kronborg, O., Fenger, C., and Jorgensen, O.D. A prospective randomized study of follow-up after radical surgery for colorectal cancer. Br J Surg. 1997; 84: 666—669

CrossRef | PubMed
See all References
, 13x13Kronborg, O., Hage, E., and 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

CrossRef | PubMed | Scopus (29)
See all References
, 14x14Makela, J.T., Laitinen, S.O., and Kairaluoma, M.I. Five-year follow-up after radical surgery for colorectal cancer. Results of a prospective randomized trial. Arch Surg. 1995; 130: 1062—1067

CrossRef | PubMed
See all References
, 15x15McFarland, R.J., Becciolini, C., and Lallemand, R.C. The value of colonoscopic surveillance following a diagnosis of colorectal cancer or adenomatous polyp. Eur J Surg Oncol. 1991; 17: 514—518

PubMed
See all References
, 16x16Obrand, D.I. and Gordon, P.H. Incidence and patterns of recurrence following curative resection for colorectal carcinoma. Dis Colon Rectum. 1997; 40: 15—24

CrossRef | PubMed | Scopus (190)
See all References
, 17x17Ohlsson, B., Breland, U., Ekberg, H., Graffner, H., and Tranberg, K.G. Follow-up after curative surgery for colorectal carcinoma. Randomized comparison with no follow-up. Dis Colon Rectum. 1995; 38: 619—626

CrossRef | PubMed | Scopus (236)
See all References
, 18x18Patchett, S.E., Mulcahy, H.E., and O'Donoghue, D.P. Colonoscopic surveillance after curative resection for colorectal cancer. Br J Surg. 1993; 80: 1330—1332

CrossRef | PubMed | Scopus (34)
See all References
, 19x19Pietra, N., Sarli, L., Costi, R., Ouchemi, C., Grattarola, M., and 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

CrossRef | PubMed | Scopus (225)
See all References
, 20x20Schoemaker, D., Black, R., Giles, L., and Toouli, J. Yearly colonoscopy, liver CT, and chest radiography do not influence 5-year survival of colorectal cancer patients. Gastroenterology. 1998; 114: 7—14

Abstract | Full Text | Full Text PDF | PubMed | Scopus (276)
See all References
, 21x21Skaife, P., Seow-Choen, F., Eu, K.W., and Tang, C.L. A novel indicator for surveillance colonoscopy following colorectal cancer resection. Colorectal Dis. 2003; 5: 45—48

CrossRef | PubMed | Scopus (16)
See all References
, 22x22Stigliano, V., Fracasso, P., Grassi, A., Lapenta, R., Citarda, F., Tomaselli, G., Giannarelli, D., and Casale, V. Endoscopic follow-up in resected colorectal cancer patients. J Exp Clin Cancer Res. 2000; 19: 145—148

PubMed
See all References
, 23x23Togashi, K., Konishi, F., Ozawa, A., Sato, T., Shito, K., Kashiwagi, H., Okada, M., and Nagai, H. Predictive factors for detecting colorectal carcinomas in surveillance colonoscopy after colorectal cancer surgery. Dis Colon Rectum. 2000; 43: S47—S53

CrossRef | PubMed
See all References
, 24x24Weber, C.A., Deveney, K.E., Pellegrini, C.A., and Way, L.W. Routine colonoscopy in the management of colorectal carcinoma. Am J Surg. 1986; 152: 87—92

Abstract | Full Text PDF | PubMed | Scopus (16)
See all References
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.25x25Benson, A.B. 3rd, Desch, C.E., Flynn, P.J., Krause, C., Loprinzi, C.L., Minsky, B.D., Petrelli, N.J., Pfister, D.G., Smith, T.J., and Somerfield, M.R. 2000 update of American Society of Clinical Oncology colorectal cancer surveillance guidelines. J Clin Oncol. 2000; 18: 3586—3588

PubMed
See all References
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.26x26Renehan, A.G., Egger, M., Saunders, M.P., and O'Dwyer, S.T. 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

CrossRef | PubMed
See all References
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 colonoscopy20x20Schoemaker, D., Black, R., Giles, L., and Toouli, J. Yearly colonoscopy, liver CT, and chest radiography do not influence 5-year survival of colorectal cancer patients. Gastroenterology. 1998; 114: 7—14

Abstract | Full Text | Full Text PDF | PubMed | Scopus (276)
See all References
nor meta-analyses of these trials26x26Renehan, A.G., Egger, M., Saunders, M.P., and O'Dwyer, S.T. 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

CrossRef | PubMed
See all References
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.2x2Barillari, P., Ramacciato, G., Manetti, G., Bovino, A., Sammartino, P., and 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

CrossRef | PubMed | Scopus (49)
See all References
, 3x3Barrier, A., Houry, S., and Huguier, M. The appropriate use of colonoscopy in the curative management of colorectal cancer. Int J Colorectal Dis. 1998; 13: 93—98

CrossRef | PubMed | Scopus (25)
See all References
, 4x4Carlsson, G., Petrelli, N.J., Nava, H., Herrera, L., and Mittelman, A. The value of colonoscopic surveillance after curative resection for colorectal cancer or synchronous adenomatous polyps. Arch Surg. 1987; 122: 1261—1263

CrossRef | PubMed
See all References
, 5x5Castells, A., Bessa, X., Daniels, M., Ascaso, C., Lacy, A.M., Garcia-Valdecasas, J.C., Gargallo, L., Novell, F., Astudillo, E., Filella, X., and Pique, J.M. Value of postoperative surveillance after radical surgery for colorectal cancer (results of a cohort study) . Dis Colon Rectum. 1998; 41: 714—724

CrossRef | PubMed | Scopus (81)
See all References
, 6x6Chen, F. and Stuart, M. Colonoscopic follow-up of colorectal carcinoma. Dis Colon Rectum. 1994; 37: 568—572

CrossRef | PubMed | Scopus (48)
See all References
, 7x7Eckardt, V.F., Stamm, H., Kanzler, G., and Bernhard, G. Improved survival after colorectal cancer in patients complying with a postoperative endoscopic surveillance program. Endoscopy. 1994; 26: 523—527

CrossRef | PubMed
See all References
, 8x8Granqvist, S. and Karlsson, T. Postoperative follow-up of patients with colorectal carcinoma by colonoscopy. Eur J Surg. 1992; 158: 307—312

PubMed
See all References
, 9x9Green, R.J., Metlay, J.P., Propert, K., Catalano, P.J., Macdonald, J.S., Mayer, R.J., and Haller, D.G. Surveillance for second primary colorectal cancer after adjuvant chemotherapy (an analysis of Intergroup 0089) . Ann Intern Med. 2002; 136: 261—269

CrossRef | PubMed
See all References
, 10x10Juhl, G., Larson, G.M., Mullins, R., Bond, S., and Polk, H.C. Jr. Six-year results of annual colonoscopy after resection of colorectal cancer. World J Surg. 1990; 14: 255—261

CrossRef | PubMed | Scopus (51)
See all References
, 11x11Khoury, D.A., Opelka, F.G., Beck, D.E., Hicks, T.C., Timmcke, A.E., and Gathright, J.B. Jr. Colon surveillance after colorectal cancer surgery. Dis Colon Rectum. 1996; 39: 252—256

CrossRef | PubMed | Scopus (35)
See all References
, 12x12Kjeldsen, B.J., Kronborg, O., Fenger, C., and Jorgensen, O.D. A prospective randomized study of follow-up after radical surgery for colorectal cancer. Br J Surg. 1997; 84: 666—669

CrossRef | PubMed
See all References
, 13x13Kronborg, O., Hage, E., and 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

CrossRef | PubMed | Scopus (29)
See all References
, 14x14Makela, J.T., Laitinen, S.O., and Kairaluoma, M.I. Five-year follow-up after radical surgery for colorectal cancer. Results of a prospective randomized trial. Arch Surg. 1995; 130: 1062—1067

CrossRef | PubMed
See all References
, 15x15McFarland, R.J., Becciolini, C., and Lallemand, R.C. The value of colonoscopic surveillance following a diagnosis of colorectal cancer or adenomatous polyp. Eur J Surg Oncol. 1991; 17: 514—518

PubMed
See all References
, 16x16Obrand, D.I. and Gordon, P.H. Incidence and patterns of recurrence following curative resection for colorectal carcinoma. Dis Colon Rectum. 1997; 40: 15—24

CrossRef | PubMed | Scopus (190)
See all References
, 17x17Ohlsson, B., Breland, U., Ekberg, H., Graffner, H., and Tranberg, K.G. Follow-up after curative surgery for colorectal carcinoma. Randomized comparison with no follow-up. Dis Colon Rectum. 1995; 38: 619—626

CrossRef | PubMed | Scopus (236)
See all References
, 18x18Patchett, S.E., Mulcahy, H.E., and O'Donoghue, D.P. Colonoscopic surveillance after curative resection for colorectal cancer. Br J Surg. 1993; 80: 1330—1332

CrossRef | PubMed | Scopus (34)
See all References
, 19x19Pietra, N., Sarli, L., Costi, R., Ouchemi, C., Grattarola, M., and 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

CrossRef | PubMed | Scopus (225)
See all References
, 20x20Schoemaker, D., Black, R., Giles, L., and Toouli, J. Yearly colonoscopy, liver CT, and chest radiography do not influence 5-year survival of colorectal cancer patients. Gastroenterology. 1998; 114: 7—14

Abstract | Full Text | Full Text PDF | PubMed | Scopus (276)
See all References
, 21x21Skaife, P., Seow-Choen, F., Eu, K.W., and Tang, C.L. A novel indicator for surveillance colonoscopy following colorectal cancer resection. Colorectal Dis. 2003; 5: 45—48

CrossRef | PubMed | Scopus (16)
See all References
, 22x22Stigliano, V., Fracasso, P., Grassi, A., Lapenta, R., Citarda, F., Tomaselli, G., Giannarelli, D., and Casale, V. Endoscopic follow-up in resected colorectal cancer patients. J Exp Clin Cancer Res. 2000; 19: 145—148

PubMed
See all References
, 23x23Togashi, K., Konishi, F., Ozawa, A., Sato, T., Shito, K., Kashiwagi, H., Okada, M., and Nagai, H. Predictive factors for detecting colorectal carcinomas in surveillance colonoscopy after colorectal cancer surgery. Dis Colon Rectum. 2000; 43: S47—S53

CrossRef | PubMed
See all References
, 24x24Weber, C.A., Deveney, K.E., Pellegrini, C.A., and Way, L.W. Routine colonoscopy in the management of colorectal carcinoma. Am J Surg. 1986; 152: 87—92

Abstract | Full Text PDF | PubMed | Scopus (16)
See all References
, 26x26Renehan, A.G., Egger, M., Saunders, M.P., and O'Dwyer, S.T. 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

CrossRef | PubMed
See all References
, 27x27Jeffery, G.M., Hickey, B.E., and Hider, P. Follow-up strategies for patients treated for non-metastatic colorectal cancer. Cochrane Database Syst Rev. 2002; : CD002200

PubMed
See all References
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.2x2Barillari, P., Ramacciato, G., Manetti, G., Bovino, A., Sammartino, P., and 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

CrossRef | PubMed | Scopus (49)
See all References
, 3x3Barrier, A., Houry, S., and Huguier, M. The appropriate use of colonoscopy in the curative management of colorectal cancer. Int J Colorectal Dis. 1998; 13: 93—98

CrossRef | PubMed | Scopus (25)
See all References
, 4x4Carlsson, G., Petrelli, N.J., Nava, H., Herrera, L., and Mittelman, A. The value of colonoscopic surveillance after curative resection for colorectal cancer or synchronous adenomatous polyps. Arch Surg. 1987; 122: 1261—1263

CrossRef | PubMed
See all References
, 5x5Castells, A., Bessa, X., Daniels, M., Ascaso, C., Lacy, A.M., Garcia-Valdecasas, J.C., Gargallo, L., Novell, F., Astudillo, E., Filella, X., and Pique, J.M. Value of postoperative surveillance after radical surgery for colorectal cancer (results of a cohort study) . Dis Colon Rectum. 1998; 41: 714—724

CrossRef | PubMed | Scopus (81)
See all References
, 6x6Chen, F. and Stuart, M. Colonoscopic follow-up of colorectal carcinoma. Dis Colon Rectum. 1994; 37: 568—572

CrossRef | PubMed | Scopus (48)
See all References
, 7x7Eckardt, V.F., Stamm, H., Kanzler, G., and Bernhard, G. Improved survival after colorectal cancer in patients complying with a postoperative endoscopic surveillance program. Endoscopy. 1994; 26: 523—527

CrossRef | PubMed
See all References
, 8x8Granqvist, S. and Karlsson, T. Postoperative follow-up of patients with colorectal carcinoma by colonoscopy. Eur J Surg. 1992; 158: 307—312

PubMed
See all References
, 9x9Green, R.J., Metlay, J.P., Propert, K., Catalano, P.J., Macdonald, J.S., Mayer, R.J., and Haller, D.G. Surveillance for second primary colorectal cancer after adjuvant chemotherapy (an analysis of Intergroup 0089) . Ann Intern Med. 2002; 136: 261—269

CrossRef | PubMed
See all References
, 10x10Juhl, G., Larson, G.M., Mullins, R., Bond, S., and Polk, H.C. Jr. Six-year results of annual colonoscopy after resection of colorectal cancer. World J Surg. 1990; 14: 255—261

CrossRef | PubMed | Scopus (51)
See all References
, 11x11Khoury, D.A., Opelka, F.G., Beck, D.E., Hicks, T.C., Timmcke, A.E., and Gathright, J.B. Jr. Colon surveillance after colorectal cancer surgery. Dis Colon Rectum. 1996; 39: 252—256

CrossRef | PubMed | Scopus (35)
See all References
, 12x12Kjeldsen, B.J., Kronborg, O., Fenger, C., and Jorgensen, O.D. A prospective randomized study of follow-up after radical surgery for colorectal cancer. Br J Surg. 1997; 84: 666—669

CrossRef | PubMed
See all References
, 13x13Kronborg, O., Hage, E., and 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

CrossRef | PubMed | Scopus (29)
See all References
, 14x14Makela, J.T., Laitinen, S.O., and Kairaluoma, M.I. Five-year follow-up after radical surgery for colorectal cancer. Results of a prospective randomized trial. Arch Surg. 1995; 130: 1062—1067

CrossRef | PubMed
See all References
, 15x15McFarland, R.J., Becciolini, C., and Lallemand, R.C. The value of colonoscopic surveillance following a diagnosis of colorectal cancer or adenomatous polyp. Eur J Surg Oncol. 1991; 17: 514—518

PubMed
See all References
, 16x16Obrand, D.I. and Gordon, P.H. Incidence and patterns of recurrence following curative resection for colorectal carcinoma. Dis Colon Rectum. 1997; 40: 15—24

CrossRef | PubMed | Scopus (190)
See all References
, 17x17Ohlsson, B., Breland, U., Ekberg, H., Graffner, H., and Tranberg, K.G. Follow-up after curative surgery for colorectal carcinoma. Randomized comparison with no follow-up. Dis Colon Rectum. 1995; 38: 619—626

CrossRef | PubMed | Scopus (236)
See all References
, 18x18Patchett, S.E., Mulcahy, H.E., and O'Donoghue, D.P. Colonoscopic surveillance after curative resection for colorectal cancer. Br J Surg. 1993; 80: 1330—1332

CrossRef | PubMed | Scopus (34)
See all References
, 19x19Pietra, N., Sarli, L., Costi, R., Ouchemi, C., Grattarola, M., and 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

CrossRef | PubMed | Scopus (225)
See all References
, 20x20Schoemaker, D., Black, R., Giles, L., and Toouli, J. Yearly colonoscopy, liver CT, and chest radiography do not influence 5-year survival of colorectal cancer patients. Gastroenterology. 1998; 114: 7—14

Abstract | Full Text | Full Text PDF | PubMed | Scopus (276)
See all References
, 21x21Skaife, P., Seow-Choen, F., Eu, K.W., and Tang, C.L. A novel indicator for surveillance colonoscopy following colorectal cancer resection. Colorectal Dis. 2003; 5: 45—48

CrossRef | PubMed | Scopus (16)
See all References
, 22x22Stigliano, V., Fracasso, P., Grassi, A., Lapenta, R., Citarda, F., Tomaselli, G., Giannarelli, D., and Casale, V. Endoscopic follow-up in resected colorectal cancer patients. J Exp Clin Cancer Res. 2000; 19: 145—148

PubMed
See all References
, 23x23Togashi, K., Konishi, F., Ozawa, A., Sato, T., Shito, K., Kashiwagi, H., Okada, M., and Nagai, H. Predictive factors for detecting colorectal carcinomas in surveillance colonoscopy after colorectal cancer surgery. Dis Colon Rectum. 2000; 43: S47—S53

CrossRef | PubMed
See all References
, 24x24Weber, C.A., Deveney, K.E., Pellegrini, C.A., and Way, L.W. Routine colonoscopy in the management of colorectal carcinoma. Am J Surg. 1986; 152: 87—92

Abstract | Full Text PDF | PubMed | Scopus (16)
See all References
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.28x28Holm, T., Johansson, H., Cedermark, B., Ekelund, G., and Rutqvist, L.E. 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

CrossRef | PubMed
See all References
, 29x29Porter, G.A., Soskolne, C.L., Yakimets, W.W., and Newman, S.C. Surgeon-related factors and outcome in rectal cancer. Ann Surg. 1998; 227: 157—167

CrossRef | PubMed | Scopus (456)
See all References
, 30x30McArdle, C.S. and Hole, D. Impact of variability among surgeons on postoperative morbidity and mortality and ultimate survival. Br Med J. 1991; 302: 1501—1505

CrossRef | PubMed
See all References
, 31x31Steele, R.J. The influence of surgeon case volume on outcome in site-specific cancer surgery. Eur J Surg Oncol. 1996; 22: 211—213

Abstract | Full Text PDF | PubMed
See all References
, 32x32Harmon, J.W., Tang, D.G., Gordon, T.A., Bowman, H.M., Choti, M.A., Kaufman, H.S., Bender, J.S., Duncan, M.D., Magnuson, T.H., Lillemoe, K.D., and Cameron, J.L. Hospital volume can serve as a surrogate for surgeon volume for achieving excellent outcomes in colorectal resection. Ann Surg. 1999; 230: 404—413

CrossRef | PubMed | Scopus (277)
See all References
, 33x33Panageas, K.S., Schrag, D., Riedel, E., Bach, P.B., and Begg, C.B. The effect of clustering of outcomes on the association of procedure volume and surgical outcomes. Ann Intern Med. 2003; 139: 658—665

CrossRef | PubMed
See all References

High recurrence rates of rectal cancer are partly a function of surgical technique and volume.28x28Holm, T., Johansson, H., Cedermark, B., Ekelund, G., and Rutqvist, L.E. 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

CrossRef | PubMed
See all References
, 29x29Porter, G.A., Soskolne, C.L., Yakimets, W.W., and Newman, S.C. Surgeon-related factors and outcome in rectal cancer. Ann Surg. 1998; 227: 157—167

CrossRef | PubMed | Scopus (456)
See all References
, 30x30McArdle, C.S. and Hole, D. Impact of variability among surgeons on postoperative morbidity and mortality and ultimate survival. Br Med J. 1991; 302: 1501—1505

CrossRef | PubMed
See all References
, 31x31Steele, R.J. The influence of surgeon case volume on outcome in site-specific cancer surgery. Eur J Surg Oncol. 1996; 22: 211—213

Abstract | Full Text PDF | PubMed
See all References
, 32x32Harmon, J.W., Tang, D.G., Gordon, T.A., Bowman, H.M., Choti, M.A., Kaufman, H.S., Bender, J.S., Duncan, M.D., Magnuson, T.H., Lillemoe, K.D., and Cameron, J.L. Hospital volume can serve as a surrogate for surgeon volume for achieving excellent outcomes in colorectal resection. Ann Surg. 1999; 230: 404—413

CrossRef | PubMed | Scopus (277)
See all References
, 33x33Panageas, K.S., Schrag, D., Riedel, E., Bach, P.B., and Begg, C.B. The effect of clustering of outcomes on the association of procedure volume and surgical outcomes. Ann Intern Med. 2003; 139: 658—665

CrossRef | PubMed
See all References
Specifically, recurrence rates less than 10% have been reported consistently when patients undergo surgery by a technique called total mesorectal excision.34x34Kapiteijn, E., Marijnen, C.A., Nagtegaal, I.D., Putter, H., Steup, W.H., Wiggers, T., Rutten, H.J., Pahlman, L., Glimelius, B., van Krieken, J.H., Leer, J.W., and van de Velde, C.J. Dutch Colorectal Cancer G Preoperative radiotherapy combined with total mesorectal excision for resectable rectal cancer. N Engl J Med. 2001; 345: 638—646

CrossRef | PubMed | Scopus (2163)
See all References
, 35x35Heald, R.J., Husband, E.M., and Ryall, R.D. The mesorectum in rectal cancer surgery—the clue to pelvic recurrence?. Br J Surg. 1982; 69: 613—616

CrossRef | PubMed
See all References
, 36x36Cawthorn, S.J., Parums, D.V., Gibbs, N.M., A'Hern, R.P., Caffarey, S.M., Broughton, C.I., and Marks, C.G. Extent of mesorectal spread and involvement of lateral resection margin as prognostic factors after surgery for rectal cancer. Lancet. 1990; 335: 1055—1059

Abstract | PubMed | Scopus (234)
See all References
This technique involves sharp dissection of the rectum and its surrounding adventitia along the first plane outside the adventitia (the mesorectal fascia).35x35Heald, R.J., Husband, E.M., and Ryall, R.D. The mesorectum in rectal cancer surgery—the clue to pelvic recurrence?. Br J Surg. 1982; 69: 613—616

CrossRef | PubMed
See all References
, 36x36Cawthorn, S.J., Parums, D.V., Gibbs, N.M., A'Hern, R.P., Caffarey, S.M., Broughton, C.I., and Marks, C.G. Extent of mesorectal spread and involvement of lateral resection margin as prognostic factors after surgery for rectal cancer. Lancet. 1990; 335: 1055—1059

Abstract | PubMed | Scopus (234)
See all References
The technique can be performed using either an open or laparoscopic-assisted approach37x37Fleshman, J.W., Wexner, S.D., Anvari, M., LaTulippe, J.F., Birnbaum, E.H., Kodner, I.J., Read, T.E., Nogueras, J.J., and Weiss, E.G. Laparoscopic vs. open abdominoperineal resection for cancer. Dis Colon Rectum. 1999; 42: 930—939

CrossRef | PubMed | Scopus (115)
See all References
, 38x38Kwok, S.P., Lau, W.Y., Carey, P.D., Kelly, S.B., Leung, K.L., and Li, A.K. Prospective evaluation of laparoscopic-assisted large bowel excision for cancer. Ann Surg. 1996; 223: 170—176

CrossRef | PubMed | Scopus (139)
See all References
, 39x39Leung, K.L., Kwok, S.P., Lam, S.C., Lee, J.F., Yiu, R.Y., Ng, S.S., Lai, P.B., and Lau, W.Y. Laparoscopic resection of rectosigmoid carcinoma (prospective randomised trial) . Lancet. 2004; 363: 1187—1192

Abstract | Full Text | Full Text PDF | PubMed | Scopus (565)
See all References
, 40x40Stockholm Colorectal Cancer Study Group, Basingstoke Bowel Cancer Research Project, Martling, A.L., Holm, T., Rutqvist, L.E., Moran, B.J., Heald, R.J., and Cedemark, B. Effect of a surgical training programme on outcome of rectal cancer in the County of Stockholm. Lancet. 2000; 356: 93—96

Abstract | Full Text | Full Text PDF | PubMed
See all References
and has been reported to allow higher rates of successful low anterior resection40x40Stockholm Colorectal Cancer Study Group, Basingstoke Bowel Cancer Research Project, Martling, A.L., Holm, T., Rutqvist, L.E., Moran, B.J., Heald, R.J., and Cedemark, B. Effect of a surgical training programme on outcome of rectal cancer in the County of Stockholm. Lancet. 2000; 356: 93—96

Abstract | Full Text | Full Text PDF | PubMed
See all References
and lower rates of postoperative sexual dysfunction in men.41x41Maurer, C.A., Z'Graggen, K., Renzulli, P., Schilling, M.K., Netzer, P., and Buchler, M.W. Total mesorectal excision preserves male genital function compared with conventional rectal cancer surgery. Br J Surg. 2001; 88: 1501—1505

CrossRef | PubMed | Scopus (101)
See all References

Local recurrence rates of rectal cancer can also be reduced by administration of chemotherapy and radiation therapy,34x34Kapiteijn, E., Marijnen, C.A., Nagtegaal, I.D., Putter, H., Steup, W.H., Wiggers, T., Rutten, H.J., Pahlman, L., Glimelius, B., van Krieken, J.H., Leer, J.W., and van de Velde, C.J. Dutch Colorectal Cancer G Preoperative radiotherapy combined with total mesorectal excision for resectable rectal cancer. N Engl J Med. 2001; 345: 638—646

CrossRef | PubMed | Scopus (2163)
See all References
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 ultrasound42x42Fleshman, J.W., Myerson, R.J., Fry, R.D., and Kodner, I.J. Accuracy of transrectal ultrasound in predicting pathologic stage of rectal cancer before and after preoperative radiation therapy. Dis Colon Rectum. 1992; 35: 823—829

CrossRef | PubMed
See all References
, 43x43Gualdi, G.F., Casciani, E., Guadalaxara, A., d'Orta, C., Polettini, E., and 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

CrossRef | PubMed
See all References
, 44x44Hunerbein, M., Pegios, W., Rau, B., Vogl, T.J., Felix, R., and Schlag, P.M. 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

CrossRef | PubMed | Scopus (92)
See all References
or magnetic resonance imaging,45x45Mathur, P., Smith, J.J., Ramsey, C., Owen, M., Thorpe, A., Karim, S., Burke, C., Ramesh, S., and Dawson, P.M. 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

CrossRef | PubMed | Scopus (70)
See all References
, 46x46Beets-Tan, R.G. MRI in rectal cancer (the T stage and circumferential resection margin) . Colorectal Dis. 2003; 5: 392—395

CrossRef | PubMed | Scopus (58)
See all References
, 47x47Radcliffe, A. and Brown, G. Will MRI provide maps of lines of excision for rectal cancer?. Lancet. 2001; 357: 495—496

Abstract | Full Text | Full Text PDF | PubMed | Scopus (23)
See all References
, 48x48Beets-Tan, R.G., Beets, G.L., Vliegen, R.F., Kessels, A.G., Van Boven, H., De Bruine, A., von Meyenfeldt, M.F., Baeten, C.G., and van Engelshoven, J.M. Accuracy of magnetic resonance imaging in prediction of tumour-free resection margin in rectal cancer surgery. Lancet. 2001; 357: 497—504

Abstract | Full Text | Full Text PDF | PubMed | Scopus (498)
See all References
followed by neoadjuvant chemoradiation in selected patients.49x49Sauer, R., Becker, H., Hohenberger, W., Rodel, C., Wittekind, C., Fietkau, R., Martus, P., Tschmelitsch, J., Hager, E., Hess, C.F., Karstens, J.H., Liersch, T., Schmidberger, H., Raab, R., and German Rectal Cancer Study G. Preoperative versus postoperative chemoradiotherapy for rectal cancer. N Engl J Med. 2004; 351: 1731—1740

CrossRef | PubMed | Scopus (2354)
See all References
The combination of neoadjuvant chemoradiation and resection by surgeons trained in total mesorectal excision has resulted in very low recurrence rates for rectal cancer.34x34Kapiteijn, E., Marijnen, C.A., Nagtegaal, I.D., Putter, H., Steup, W.H., Wiggers, T., Rutten, H.J., Pahlman, L., Glimelius, B., van Krieken, J.H., Leer, J.W., and van de Velde, C.J. Dutch Colorectal Cancer G Preoperative radiotherapy combined with total mesorectal excision for resectable rectal cancer. N Engl J Med. 2001; 345: 638—646

CrossRef | PubMed | Scopus (2163)
See all References
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 histology50x50Rex, D., Cummings, O., and Ulbright, T. Coming to terms with pathologists over colon polyps with cancer or high-grade dysplasia. J Clin Gastroenterol. 2005; 39: 1—3

CrossRef | PubMed
See all References
and/or increased surgical risk, a follow-up endoscopic examination to inspect and biopsy the resection site is reasonable.51x51Practice parameters Committee of the American College of Gastroenterology and Bond, J.H. Polyp guideline (diagnosis, treatment, and surveillance for patients with colorectal polyps) . Am J Gastroenterol. 2000; 95: 3053—3063

CrossRef | PubMed
See all References
The follow-up examination is considered standard in the case of a sessile malignant polyp removed by piecemeal resection.1x1Winawer, S.J., Zauber, A.G., Fletcher, R.H., Stillman, J.S., O'Brien, M.J., Levin, B., Smith, R.A., Lieberman, D.A., Burt, R.W., Levin, T.R., Bond, J.H., Brooks, D., Byers, T., Hyman, N., Kirk, L., Thorson, A., Simmang, C., Johnson, D., and Rex, D.K. 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

Abstract | Full Text | Full Text PDF | PubMed | Scopus (450)
See all References
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 3Metachronous Cancers in Postcancer Resection Surveillance Colonoscopy Studies
Study N Colonoscopies Metachronous CRCs (all) Metachronous CRCs (within 24 mo) Dukes' A or B Number asymptomatic Reoperation for cure
Barillari 481   12 6a 9 6b 7
Barrier 61c   0        
Carlsson 129 546 1 0 NS NS NS
Castells 199   0        
Chen 231   4 0 NS 4 4
Eckardt 212   0        
Granqvist 390 600 12 7 5d 6d 10
Green 3278   42 24 23 NS NS
Juhl 133 316 4 0 4 4 4
Khoury 389 3889 2 1 NS NS NS
Kjeldsen 597   10 NS NS 8 8
Kronborg 239 710 4 3 4 NS 4
Makela 106   1 NS NS NS 1
McFarland 74 237 0        
Obrand 444   0        
Ohlsson 53e   0        
Patchett 132   2 NS NS 0 NS
Pietra 207   1 NS NS NS NS
Schoemaker 325 733 8 5 5 1 NS
Skaife 611 609f 5 1 NS NS NS
Stigliano 322   5 0 NS NS NS
Togashi 341 1570 22 9 17 NS 22
Weber 75 197 2 1 2 NS 2
Total 9029 9407 137 57 69 29 62
aReport states that "more than one half" arose in first 24 months.
bReports 46 combined local recurrences with metachronous tumors, of which 22 were asymptomatic; number calculated assumes similar proportion for metachronous cancers.
cSubgroup who underwent perioperative colonoscopy.
dReports 26 combined local recurrences with metachronous tumors, of which 10 were Dukes' A or B and 14 were asymptomatic; numbers calculated assume similar proportion for metachronous cancers.
eIntensive surveillance subgroup (control group did not undergo routine colonoscopy).
fTwo patients underwent barium enema for completion of incomplete colonoscopy.

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.3x3Barrier, A., Houry, S., and Huguier, M. The appropriate use of colonoscopy in the curative management of colorectal cancer. Int J Colorectal Dis. 1998; 13: 93—98

CrossRef | PubMed | Scopus (25)
See all References
, 4x4Carlsson, G., Petrelli, N.J., Nava, H., Herrera, L., and Mittelman, A. The value of colonoscopic surveillance after curative resection for colorectal cancer or synchronous adenomatous polyps. Arch Surg. 1987; 122: 1261—1263

CrossRef | PubMed
See all References
, 13x13Kronborg, O., Hage, E., and 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

CrossRef | PubMed | Scopus (29)
See all References
, 24x24Weber, C.A., Deveney, K.E., Pellegrini, C.A., and Way, L.W. Routine colonoscopy in the management of colorectal carcinoma. Am J Surg. 1986; 152: 87—92

Abstract | Full Text PDF | PubMed | Scopus (16)
See all References
, 52x52Langevin, J.M. and Nivatvongs, S. The true incidence of synchronous cancer of the large bowel. A prospective study. Am J Surg. 1984; 147: 330—333

Abstract | Full Text PDF | PubMed | Scopus (77)
See all References
, 53x53Pagana, T.J., Ledesma, E.J., Mittelman, A., and Nava, H.R. The use of colonoscopy in the study of synchronous colorectal neoplasms. Cancer. 1984; 53: 356—359

CrossRef | PubMed
See all References
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.2x2Barillari, P., Ramacciato, G., Manetti, G., Bovino, A., Sammartino, P., and 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

CrossRef | PubMed | Scopus (49)
See all References
, 3x3Barrier, A., Houry, S., and Huguier, M. The appropriate use of colonoscopy in the curative management of colorectal cancer. Int J Colorectal Dis. 1998; 13: 93—98

CrossRef | PubMed | Scopus (25)
See all References
, 4x4Carlsson, G., Petrelli, N.J., Nava, H., Herrera, L., and Mittelman, A. The value of colonoscopic surveillance after curative resection for colorectal cancer or synchronous adenomatous polyps. Arch Surg. 1987; 122: 1261—1263

CrossRef | PubMed
See all References
, 5x5Castells, A., Bessa, X., Daniels, M., Ascaso, C., Lacy, A.M., Garcia-Valdecasas, J.C., Gargallo, L., Novell, F., Astudillo, E., Filella, X., and Pique, J.M. Value of postoperative surveillance after radical surgery for colorectal cancer (results of a cohort study) . Dis Colon Rectum. 1998; 41: 714—724

CrossRef | PubMed | Scopus (81)
See all References
, 6x6Chen, F. and Stuart, M. Colonoscopic follow-up of colorectal carcinoma. Dis Colon Rectum. 1994; 37: 568—572

CrossRef | PubMed | Scopus (48)
See all References
, 7x7Eckardt, V.F., Stamm, H., Kanzler, G., and Bernhard, G. Improved survival after colorectal cancer in patients complying with a postoperative endoscopic surveillance program. Endoscopy. 1994; 26: 523—527

CrossRef | PubMed
See all References
, 8x8Granqvist, S. and Karlsson, T. Postoperative follow-up of patients with colorectal carcinoma by colonoscopy. Eur J Surg. 1992; 158: 307—312

PubMed
See all References
, 9x9Green, R.J., Metlay, J.P., Propert, K., Catalano, P.J., Macdonald, J.S., Mayer, R.J., and Haller, D.G. Surveillance for second primary colorectal cancer after adjuvant chemotherapy (an analysis of Intergroup 0089) . Ann Intern Med. 2002; 136: 261—269

CrossRef | PubMed
See all References
, 10x10Juhl, G., Larson, G.M., Mullins, R., Bond, S., and Polk, H.C. Jr. Six-year results of annual colonoscopy after resection of colorectal cancer. World J Surg. 1990; 14: 255—261

CrossRef | PubMed | Scopus (51)
See all References
, 11x11Khoury, D.A., Opelka, F.G., Beck, D.E., Hicks, T.C., Timmcke, A.E., and Gathright, J.B. Jr. Colon surveillance after colorectal cancer surgery. Dis Colon Rectum. 1996; 39: 252—256

CrossRef | PubMed | Scopus (35)
See all References
, 12x12Kjeldsen, B.J., Kronborg, O., Fenger, C., and Jorgensen, O.D. A prospective randomized study of follow-up after radical surgery for colorectal cancer. Br J Surg. 1997; 84: 666—669

CrossRef | PubMed
See all References
, 13x13Kronborg, O., Hage, E., and 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

CrossRef | PubMed | Scopus (29)
See all References
, 14x14Makela, J.T., Laitinen, S.O., and Kairaluoma, M.I. Five-year follow-up after radical surgery for colorectal cancer. Results of a prospective randomized trial. Arch Surg. 1995; 130: 1062—1067

CrossRef | PubMed
See all References
, 15x15McFarland, R.J., Becciolini, C., and Lallemand, R.C. The value of colonoscopic surveillance following a diagnosis of colorectal cancer or adenomatous polyp. Eur J Surg Oncol. 1991; 17: 514—518

PubMed
See all References
, 16x16Obrand, D.I. and Gordon, P.H. Incidence and patterns of recurrence following curative resection for colorectal carcinoma. Dis Colon Rectum. 1997; 40: 15—24

CrossRef | PubMed | Scopus (190)
See all References
, 17x17Ohlsson, B., Breland, U., Ekberg, H., Graffner, H., and Tranberg, K.G. Follow-up after curative surgery for colorectal carcinoma. Randomized comparison with no follow-up. Dis Colon Rectum. 1995; 38: 619—626

CrossRef | PubMed | Scopus (236)
See all References
, 18x18Patchett, S.E., Mulcahy, H.E., and O'Donoghue, D.P. Colonoscopic surveillance after curative resection for colorectal cancer. Br J Surg. 1993; 80: 1330—1332

CrossRef | PubMed | Scopus (34)
See all References
, 19x19Pietra, N., Sarli, L., Costi, R., Ouchemi, C., Grattarola, M., and 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

CrossRef | PubMed | Scopus (225)
See all References
, 20x20Schoemaker, D., Black, R., Giles, L., and Toouli, J. Yearly colonoscopy, liver CT, and chest radiography do not influence 5-year survival of colorectal cancer patients. Gastroenterology. 1998; 114: 7—14

Abstract | Full Text | Full Text PDF | PubMed | Scopus (276)
See all References
, 21x21Skaife, P., Seow-Choen, F., Eu, K.W., and Tang, C.L. A novel indicator for surveillance colonoscopy following colorectal cancer resection. Colorectal Dis. 2003; 5: 45—48

CrossRef | PubMed | Scopus (16)
See all References
, 22x22Stigliano, V., Fracasso, P., Grassi, A., Lapenta, R., Citarda, F., Tomaselli, G., Giannarelli, D., and Casale, V. Endoscopic follow-up in resected colorectal cancer patients. J Exp Clin Cancer Res. 2000; 19: 145—148

PubMed
See all References
, 23x23Togashi, K., Konishi, F., Ozawa, A., Sato, T., Shito, K., Kashiwagi, H., Okada, M., and Nagai, H. Predictive factors for detecting colorectal carcinomas in surveillance colonoscopy after colorectal cancer surgery. Dis Colon Rectum. 2000; 43: S47—S53

CrossRef | PubMed
See all References
, 24x24Weber, C.A., Deveney, K.E., Pellegrini, C.A., and Way, L.W. Routine colonoscopy in the management of colorectal carcinoma. Am J Surg. 1986; 152: 87—92

Abstract | Full Text PDF | PubMed | Scopus (16)
See all References
Among studies in which the number of colonoscopies performed could be determined, 9407 colonoscopies were performed to detect 60 metachronous cancers in 2706 patients.4x4Carlsson, G., Petrelli, N.J., Nava, H., Herrera, L., and Mittelman, A. The value of colonoscopic surveillance after curative resection for colorectal cancer or synchronous adenomatous polyps. Arch Surg. 1987; 122: 1261—1263

CrossRef | PubMed
See all References
, 8x8Granqvist, S. and Karlsson, T. Postoperative follow-up of patients with colorectal carcinoma by colonoscopy. Eur J Surg. 1992; 158: 307—312

PubMed
See all References
, 10x10Juhl, G., Larson, G.M., Mullins, R., Bond, S., and Polk, H.C. Jr. Six-year results of annual colonoscopy after resection of colorectal cancer. World J Surg. 1990; 14: 255—261

CrossRef | PubMed | Scopus (51)
See all References
, 11x11Khoury, D.A., Opelka, F.G., Beck, D.E., Hicks, T.C., Timmcke, A.E., and Gathright, J.B. Jr. Colon surveillance after colorectal cancer surgery. Dis Colon Rectum. 1996; 39: 252—256

CrossRef | PubMed | Scopus (35)
See all References
, 13x13Kronborg, O., Hage, E., and 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

CrossRef | PubMed | Scopus (29)
See all References
, 15x15McFarland, R.J., Becciolini, C., and Lallemand, R.C. The value of colonoscopic surveillance following a diagnosis of colorectal cancer or adenomatous polyp. Eur J Surg Oncol. 1991; 17: 514—518

PubMed
See all References
, 20x20Schoemaker, D., Black, R., Giles, L., and Toouli, J. Yearly colonoscopy, liver CT, and chest radiography do not influence 5-year survival of colorectal cancer patients. Gastroenterology. 1998; 114: 7—14

Abstract | Full Text | Full Text PDF | PubMed | Scopus (276)
See all References
, 21x21Skaife, P., Seow-Choen, F., Eu, K.W., and Tang, C.L. A novel indicator for surveillance colonoscopy following colorectal cancer resection. Colorectal Dis. 2003; 5: 45—48

CrossRef | PubMed | Scopus (16)
See all References
, 23x23Togashi, K., Konishi, F., Ozawa, A., Sato, T., Shito, K., Kashiwagi, H., Okada, M., and Nagai, H. Predictive factors for detecting colorectal carcinomas in surveillance colonoscopy after colorectal cancer surgery. Dis Colon Rectum. 2000; 43: S47—S53

CrossRef | PubMed
See all References
, 24x24Weber, C.A., Deveney, K.E., Pellegrini, C.A., and Way, L.W. Routine colonoscopy in the management of colorectal carcinoma. Am J Surg. 1986; 152: 87—92

Abstract | Full Text PDF | PubMed | Scopus (16)
See all References
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,54x54Rex, D., Sledge, G., Harper, P., Ulbright, T., Loehrer, P., Helper, D., Smith, J., Wiersema, M., Hawes, R., and Lehman, G. 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

PubMed
See all References
, 55x55Lieberman, D., Weiss, D., Bond, J., Ahnen, D., Garewal, H., and Chejfec, G. 380. VACSG. Use of colonoscopy to screen asymptomatic adults for colorectal cancer. N Engl J Med. 2000; 343: 162—168

CrossRef | PubMed | Scopus (1250)
See all References
, 56x56Imperiale, T., Wagner, D., Lin, C., Larkin, G., Rogge, J., and Ransohoff, D. Risk of advanced proximal neoplasms in asymptomatic adults according to the distal colorectal findings. N Engl J Med. 2000; 343: 169—174

CrossRef | PubMed | Scopus (767)
See all References
, 57x57Imperiale, T.F., Ransohoff, D.F., Itzkowitz, S.H., Turnbull, B.A., Ross, M.E., and 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

CrossRef | PubMed | Scopus (470)
See all References
the number of colonoscopies needed to detect 1 invasive cancer was 135. Excluding reference 55x55Lieberman, D., Weiss, D., Bond, J., Ahnen, D., Garewal, H., and Chejfec, G. 380. VACSG. Use of colonoscopy to screen asymptomatic adults for colorectal cancer. N Engl J Med. 2000; 343: 162—168

CrossRef | PubMed | Scopus (1250)
See all References
, 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.54x54Rex, D., Sledge, G., Harper, P., Ulbright, T., Loehrer, P., Helper, D., Smith, J., Wiersema, M., Hawes, R., and Lehman, G. 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

PubMed
See all References
, 56x56Imperiale, T., Wagner, D., Lin, C., Larkin, G., Rogge, J., and Ransohoff, D. Risk of advanced proximal neoplasms in asymptomatic adults according to the distal colorectal findings. N Engl J Med. 2000; 343: 169—174

CrossRef | PubMed | Scopus (767)
See all References
, 57x57Imperiale, T.F., Ransohoff, D.F., Itzkowitz, S.H., Turnbull, B.A., Ross, M.E., and 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

CrossRef | PubMed | Scopus (470)
See all References

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.58x58Cali, R.L., Pitsch, R.M., Thorson, A.G., Watson, P., Tapia, P., Blatchford, G.J., and Christensen, M.A. Cumulative incidence of metachronous colorectal cancer. Dis Colon Rectum. 1993; 36: 388—393

CrossRef | PubMed
See all References
When reported, 69 of 106 (65%) metachronous cancers were Dukes' stage A or B,2x2Barillari, P., Ramacciato, G., Manetti, G., Bovino, A., Sammartino, P., and 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

CrossRef | PubMed | Scopus (49)
See all References
, 8x8Granqvist, S. and Karlsson, T. Postoperative follow-up of patients with colorectal carcinoma by colonoscopy. Eur J Surg. 1992; 158: 307—312

PubMed
See all References
, 9x9Green, R.J., Metlay, J.P., Propert, K., Catalano, P.J., Macdonald, J.S., Mayer, R.J., and Haller, D.G. Surveillance for second primary colorectal cancer after adjuvant chemotherapy (an analysis of Intergroup 0089) . Ann Intern Med. 2002; 136: 261—269

CrossRef | PubMed
See all References
, 10x10Juhl, G., Larson, G.M., Mullins, R., Bond, S., and Polk, H.C. Jr. Six-year results of annual colonoscopy after resection of colorectal cancer. World J Surg. 1990; 14: 255—261

CrossRef | PubMed | Scopus (51)
See all References
, 13x13Kronborg, O., Hage, E., and 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

CrossRef | PubMed | Scopus (29)
See all References
, 20x20Schoemaker, D., Black, R., Giles, L., and Toouli, J. Yearly colonoscopy, liver CT, and chest radiography do not influence 5-year survival of colorectal cancer patients. Gastroenterology. 1998; 114: 7—14

Abstract | Full Text | Full Text PDF | PubMed | Scopus (276)
See all References
, 23x23Togashi, K., Konishi, F., Ozawa, A., Sato, T., Shito, K., Kashiwagi, H., Okada, M., and Nagai, H. Predictive factors for detecting colorectal carcinomas in surveillance colonoscopy after colorectal cancer surgery. Dis Colon Rectum. 2000; 43: S47—S53

CrossRef | PubMed
See all References
, 24x24Weber, C.A., Deveney, K.E., Pellegrini, C.A., and Way, L.W. Routine colonoscopy in the management of colorectal carcinoma. Am J Surg. 1986; 152: 87—92

Abstract | Full Text PDF | PubMed | Scopus (16)
See all References
29 of 52 (56%) were asymptomatic,2x2Barillari, P., Ramacciato, G., Manetti, G., Bovino, A., Sammartino, P., and 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

CrossRef | PubMed | Scopus (49)
See all References
, 6x6Chen, F. and Stuart, M. Colonoscopic follow-up of colorectal carcinoma. Dis Colon Rectum. 1994; 37: 568—572

CrossRef | PubMed | Scopus (48)
See all References
, 8x8Granqvist, S. and Karlsson, T. Postoperative follow-up of patients with colorectal carcinoma by colonoscopy. Eur J Surg. 1992; 158: 307—312

PubMed
See all References
, 10x10Juhl, G., Larson, G.M., Mullins, R., Bond, S., and Polk, H.C. Jr. Six-year results of annual colonoscopy after resection of colorectal cancer. World J Surg. 1990; 14: 255—261

CrossRef | PubMed | Scopus (51)
See all References
, 12x12Kjeldsen, B.J., Kronborg, O., Fenger, C., and Jorgensen, O.D. A prospective randomized study of follow-up after radical surgery for colorectal cancer. Br J Surg. 1997; 84: 666—669

CrossRef | PubMed
See all References
, 18x18Patchett, S.E., Mulcahy, H.E., and O'Donoghue, D.P. Colonoscopic surveillance after curative resection for colorectal cancer. Br J Surg. 1993; 80: 1330—1332

CrossRef | PubMed | Scopus (34)
See all References
, 20x20Schoemaker, D., Black, R., Giles, L., and Toouli, J. Yearly colonoscopy, liver CT, and chest radiography do not influence 5-year survival of colorectal cancer patients. Gastroenterology. 1998; 114: 7—14

Abstract | Full Text | Full Text PDF | PubMed | Scopus (276)
See all References
and 62 of 71 (87%) had surgery for cure.2x2Barillari, P., Ramacciato, G., Manetti, G., Bovino, A., Sammartino, P., and 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

CrossRef | PubMed | Scopus (49)
See all References
, 6x6Chen, F. and Stuart, M. Colonoscopic follow-up of colorectal carcinoma. Dis Colon Rectum. 1994; 37: 568—572

CrossRef | PubMed | Scopus (48)
See all References
, 8x8Granqvist, S. and Karlsson, T. Postoperative follow-up of patients with colorectal carcinoma by colonoscopy. Eur J Surg. 1992; 158: 307—312

PubMed
See all References
, 10x10Juhl, G., Larson, G.M., Mullins, R., Bond, S., and Polk, H.C. Jr. Six-year results of annual colonoscopy after resection of colorectal cancer. World J Surg. 1990; 14: 255—261

CrossRef | PubMed | Scopus (51)
See all References
, 12x12Kjeldsen, B.J., Kronborg, O., Fenger, C., and Jorgensen, O.D. A prospective randomized study of follow-up after radical surgery for colorectal cancer. Br J Surg. 1997; 84: 666—669

CrossRef | PubMed
See all References
, 13x13Kronborg, O., Hage, E., and 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

CrossRef | PubMed | Scopus (29)
See all References
, 14x14Makela, J.T., Laitinen, S.O., and Kairaluoma, M.I. Five-year follow-up after radical surgery for colorectal cancer. Results of a prospective randomized trial. Arch Surg. 1995; 130: 1062—1067

CrossRef | PubMed
See all References
, 23x23Togashi, K., Konishi, F., Ozawa, A., Sato, T., Shito, K., Kashiwagi, H., Okada, M., and Nagai, H. Predictive factors for detecting colorectal carcinomas in surveillance colonoscopy after colorectal cancer surgery. Dis Colon Rectum. 2000; 43: S47—S53

CrossRef | PubMed
See all References
, 24x24Weber, C.A., Deveney, K.E., Pellegrini, C.A., and Way, L.W. Routine colonoscopy in the management of colorectal carcinoma. Am J Surg. 1986; 152: 87—92

Abstract | Full Text PDF | PubMed | Scopus (16)
See all References
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.

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.59x59National Polyp Study Work Group, Winawer, S.J., Stewart, E.T., Zauber, A.G., Bond, J.H., Ansel, H., Waye, J.D., Hall, D., Hamlin, J.A., Schapiro, M., O'Brien, M.J., Sternberg, S.S., and Gottlieb, L.A. A comparison of colonoscopy and double-contrast barium enema for surveillance after polypectomy. N Engl J Med. 2000; 342: 1766—1772

CrossRef | PubMed | Scopus (440)
See all References

Table 4Additional 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 prevention50x50Rex, D., Cummings, O., and Ulbright, T. Coming to terms with pathologists over colon polyps with cancer or high-grade dysplasia. J Clin Gastroenterol. 2005; 39: 1—3

CrossRef | PubMed
See all References
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.60x60Rockey, D., Paulson, E., Favis, W. et al. Multicenter prospective comparison of colon imaging tests. (abstr)Gastroenterology. 2004; 126: A2004

See all References
, 61x61Johnson, C.D., Harmsen, W.S., Wilson, L.A., McCarty, R.L., Welch, T.J., Ilstrup, D.M., and Ahlquist, D.A. Prospective blinded evaluation of computed tomographic colonography for screen detection of colorectal polyps. Gastroenterology. 2003; 125: 311—319

Abstract | Full Text | Full Text PDF | PubMed | Scopus (292)
See all References
, 62x62Cotton, P.B., Durkalski, V.L., Pineau, B.C., Palesch, Y.Y., Mauldin, P.D., Hoffman, B., Vining, D.J., Small, W.C., Affronti, J., Rex, D.K. et al. Computed tomographic colonography (virtual colonoscopy). A multicenter comparison with standard colonoscopy for detection of colorectal neoplasia. JAMA. 2004; 291: 1713—1719

CrossRef | PubMed | Scopus (518)
See all References
, 63x63Pickhardt, P.J., Choi, J.R., Hwang, I., Butler, J.A., Puckett, M.L., Hildebrandt, H.A., Wong, R.K., Nugent, P.A., Mysliwiec, P.A., and Schindler, W.R. Computed tomographic virtual colonoscopy to screen for colorectal neoplasia in asymptomatic adults. N Engl J Med. 2003; 349: 2191—2200

CrossRef | PubMed | Scopus (1325)
See all References
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.64x64Finkelstein, S. and Bini, E.J. 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

Abstract | Full Text | Full Text PDF
See all References
Immunochemical fecal occult blood testing warrants additional evaluation as an adjunct to colonoscopy65x65Bampton, P.A., Sandford, J.J., Cole, S.R., Smith, A., Marcon, J., Cadd, B., and Young, G.P. Interval faecal occult blood testing in a colonoscopy based screening programme detects additional pathology. Gut. 2005; 54: 803—806

CrossRef | PubMed | Scopus (49)
See all References
in this setting. Fecal DNA testing66x66Imperiale, T.F., Ransohoff, D.F., Itzkowitz, S.H., Turnbull, B.A., and Ross, M.E. Fecal DNA versus fecal occult blood for colorectal-cancer screening in an average-risk population. N Engl J Med. 2004; 351: 2704—2714

CrossRef | PubMed | Scopus (507)
See all References
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 5.55x55Lieberman, D., Weiss, D., Bond, J., Ahnen, D., Garewal, H., and Chejfec, G. 380. VACSG. Use of colonoscopy to screen asymptomatic adults for colorectal cancer. N Engl J Med. 2000; 343: 162—168

CrossRef | PubMed | Scopus (1250)
See all References

Table 5Key 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?

References

1Winawer, S.J., Zauber, A.G., Fletcher, R.H., Stillman, J.S., O'Brien, M.J., Levin, B., Smith, R.A., Lieberman, D.A., Burt, R.W., Levin, T.R., Bond, J.H., Brooks, D., Byers, T., Hyman, N., Kirk, L., Thorson, A., Simmang, C., Johnson, D., and Rex, D.K. 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
2Barillari, P., Ramacciato, G., Manetti, G., Bovino, A., Sammartino, P., and 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
3Barrier, A., Houry, S., and Huguier, M. The appropriate use of colonoscopy in the curative management of colorectal cancer. Int J Colorectal Dis. 1998; 13: 93—98
44Carlsson, G., Petrelli, N.J., Nava, H., Herrera, L., and Mittelman, A. The value of colonoscopic surveillance after curative resection for colorectal cancer or synchronous adenomatous polyps. Arch Surg. 1987; 122: 1261—1263
5Castells, A., Bessa, X., Daniels, M., Ascaso, C., Lacy, A.M., Garcia-Valdecasas, J.C., Gargallo, L., Novell, F., Astudillo, E., Filella, X., and Pique, J.M. Value of postoperative surveillance after radical surgery for colorectal cancer (results of a cohort study) . Dis Colon Rectum. 1998; 41: 714—724
6Chen, F. and Stuart, M. Colonoscopic follow-up of colorectal carcinoma. Dis Colon Rectum. 1994; 37: 568—572
7Eckardt, V.F., Stamm, H., Kanzler, G., and Bernhard, G. Improved survival after colorectal cancer in patients complying with a postoperative endoscopic surveillance program. Endoscopy. 1994; 26: 523—527
8Granqvist, S. and Karlsson, T. Postoperative follow-up of patients with colorectal carcinoma by colonoscopy. Eur J Surg. 1992; 158: 307—312
9Green, R.J., Metlay, J.P., Propert, K., Catalano, P.J., Macdonald, J.S., Mayer, R.J., and Haller, D.G. Surveillance for second primary colorectal cancer after adjuvant chemotherapy (an analysis of Intergroup 0089) . Ann Intern Med. 2002; 136: 261—269
10Juhl, G., Larson, G.M., Mullins, R., Bond, S., and Polk, H.C. Jr. Six-year results of annual colonoscopy after resection of colorectal cancer. World J Surg. 1990; 14: 255—261
11Khoury, D.A., Opelka, F.G., Beck, D.E., Hicks, T.C., Timmcke, A.E., and Gathright, J.B. Jr. Colon surveillance after colorectal cancer surgery. Dis Colon Rectum. 1996; 39: 252—256
12Kjeldsen, B.J., Kronborg, O., Fenger, C., and Jorgensen, O.D. A prospective randomized study of follow-up after radical surgery for colorectal cancer. Br J Surg. 1997; 84: 666—669
13Kronborg, O., Hage, E., and 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
14Makela, J.T., Laitinen, S.O., and Kairaluoma, M.I. Five-year follow-up after radical surgery for colorectal cancer. Results of a prospective randomized trial. Arch Surg. 1995; 130: 1062—1067
15McFarland, R.J., Becciolini, C., and Lallemand, R.C. The value of colonoscopic surveillance following a diagnosis of colorectal cancer or adenomatous polyp. Eur J Surg Oncol. 1991; 17: 514—518
16Obrand, D.I. and Gordon, P.H. Incidence and patterns of recurrence following curative resection for colorectal carcinoma. Dis Colon Rectum. 1997; 40: 15—24
17Ohlsson, B., Breland, U., Ekberg, H., Graffner, H., and Tranberg, K.G. Follow-up after curative surgery for colorectal carcinoma. Randomized comparison with no follow-up. Dis Colon Rectum. 1995; 38: 619—626
18Patchett, S.E., Mulcahy, H.E., and O'Donoghue, D.P. Colonoscopic surveillance after curative resection for colorectal cancer. Br J Surg. 1993; 80: 1330—1332
19Pietra, N., Sarli, L., Costi, R., Ouchemi, C., Grattarola, M., and 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
20Schoemaker, D., Black, R., Giles, L., and Toouli, J. Yearly colonoscopy, liver CT, and chest radiography do not influence 5-year survival of colorectal cancer patients. Gastroenterology. 1998; 114: 7—14
21Skaife, P., Seow-Choen, F., Eu, K.W., and Tang, C.L. A novel indicator for surveillance colonoscopy following colorectal cancer resection. Colorectal Dis. 2003; 5: 45—48
22Stigliano, V., Fracasso, P., Grassi, A., Lapenta, R., Citarda, F., Tomaselli, G., Giannarelli, D., and Casale, V. Endoscopic follow-up in resected colorectal cancer patients. J Exp Clin Cancer Res. 2000; 19: 145—148
23Togashi, K., Konishi, F., Ozawa, A., Sato, T., Shito, K., Kashiwagi, H., Okada, M., and Nagai, H. Predictive factors for detecting colorectal carcinomas in surveillance colonoscopy after colorectal cancer surgery. Dis Colon Rectum. 2000; 43: S47—S53
24Weber, C.A., Deveney, K.E., Pellegrini, C.A., and Way, L.W. Routine colonoscopy in the management of colorectal carcinoma. Am J Surg. 1986; 152: 87—92
25Benson, A.B. 3rd, Desch, C.E., Flynn, P.J., Krause, C., Loprinzi, C.L., Minsky, B.D., Petrelli, N.J., Pfister, D.G., Smith, T.J., and Somerfield, M.R. 2000 update of American Society of Clinical Oncology colorectal cancer surveillance guidelines. J Clin Oncol. 2000; 18: 3586—3588
26Renehan, A.G., Egger, M., Saunders, M.P., and O'Dwyer, S.T. 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
27Jeffery, G.M., Hickey, B.E., and Hider, P. Follow-up strategies for patients treated for non-metastatic colorectal cancer. Cochrane Database Syst Rev. 2002; : CD002200
28Holm, T., Johansson, H., Cedermark, B., Ekelund, G., and Rutqvist, L.E. 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
29Porter, G.A., Soskolne, C.L., Yakimets, W.W., and Newman, S.C. Surgeon-related factors and outcome in rectal cancer. Ann Surg. 1998; 227: 157—167
30McArdle, C.S. and Hole, D. Impact of variability among surgeons on postoperative morbidity and mortality and ultimate survival. Br Med J. 1991; 302: 1501—1505
31Steele, R.J. The influence of surgeon case volume on outcome in site-specific cancer surgery. Eur J Surg Oncol. 1996; 22: 211—213
32Harmon, J.W., Tang, D.G., Gordon, T.A., Bowman, H.M., Choti, M.A., Kaufman, H.S., Bender, J.S., Duncan, M.D., Magnuson, T.H., Lillemoe, K.D., and Cameron, J.L. Hospital volume can serve as a surrogate for surgeon volume for achieving excellent outcomes in colorectal resection. Ann Surg. 1999; 230: 404—413
33Panageas, K.S., Schrag, D., Riedel, E., Bach, P.B., and Begg, C.B. The effect of clustering of outcomes on the association of procedure volume and surgical outcomes. Ann Intern Med. 2003; 139: 658—665
34Kapiteijn, E., Marijnen, C.A., Nagtegaal, I.D., Putter, H., Steup, W.H., Wiggers, T., Rutten, H.J., Pahlman, L., Glimelius, B., van Krieken, J.H., Leer, J.W., and van de Velde, C.J. Dutch Colorectal Cancer G Preoperative radiotherapy combined with total mesorectal excision for resectable rectal cancer. N Engl J Med. 2001; 345: 638—646
35Heald, R.J., Husband, E.M., and Ryall, R.D. The mesorectum in rectal cancer surgery—the clue to pelvic recurrence?. Br J Surg. 1982; 69: 613—616
36Cawthorn, S.J., Parums, D.V., Gibbs, N.M., A'Hern, R.P., Caffarey, S.M., Broughton, C.I., and Marks, C.G. Extent of mesorectal spread and involvement of lateral resection margin as prognostic factors after surgery for rectal cancer. Lancet. 1990; 335: 1055—1059
37Fleshman, J.W., Wexner, S.D., Anvari, M., LaTulippe, J.F., Birnbaum, E.H., Kodner, I.J., Read, T.E., Nogueras, J.J., and Weiss, E.G. Laparoscopic vs. open abdominoperineal resection for cancer. Dis Colon Rectum. 1999; 42: 930—939
38Kwok, S.P., Lau, W.Y., Carey, P.D., Kelly, S.B., Leung, K.L., and Li, A.K. Prospective evaluation of laparoscopic-assisted large bowel excision for cancer. Ann Surg. 1996; 223: 170—176
39Leung, K.L., Kwok, S.P., Lam, S.C., Lee, J.F., Yiu, R.Y., Ng, S.S., Lai, P.B., and Lau, W.Y. Laparoscopic resection of rectosigmoid carcinoma (prospective randomised trial) . Lancet. 2004; 363: 1187—1192
40Stockholm Colorectal Cancer Study Group, Basingstoke Bowel Cancer Research Project, Martling, A.L., Holm, T., Rutqvist, L.E., Moran, B.J., Heald, R.J., and Cedemark, B. Effect of a surgical training programme on outcome of rectal cancer in the County of Stockholm. Lancet. 2000; 356: 93—96
41Maurer, C.A., Z'Graggen, K., Renzulli, P., Schilling, M.K., Netzer, P., and Buchler, M.W. Total mesorectal excision preserves male genital function compared with conventional rectal cancer surgery. Br J Surg. 2001; 88: 1501—1505
42Fleshman, J.W., Myerson, R.J., Fry, R.D., and Kodner, I.J. Accuracy of transrectal ultrasound in predicting pathologic stage of rectal cancer before and after preoperative radiation therapy. Dis Colon Rectum. 1992; 35: 823—829
43Gualdi, G.F., Casciani, E., Guadalaxara, A., d'Orta, C., Polettini, E., and 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
44Hunerbein, M., Pegios, W., Rau, B., Vogl, T.J., Felix, R., and Schlag, P.M. 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
45Mathur, P., Smith, J.J., Ramsey, C., Owen, M., Thorpe, A., Karim, S., Burke, C., Ramesh, S., and Dawson, P.M. 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
46Beets-Tan, R.G. MRI in rectal cancer (the T stage and circumferential resection margin) . Colorectal Dis. 2003; 5: 392—395
47Radcliffe, A. and Brown, G. Will MRI provide maps of lines of excision for rectal cancer?. Lancet. 2001; 357: 495—496
48Beets-Tan, R.G., Beets, G.L., Vliegen, R.F., Kessels, A.G., Van Boven, H., De Bruine, A., von Meyenfeldt, M.F., Baeten, C.G., and van Engelshoven, J.M. Accuracy of magnetic resonance imaging in prediction of tumour-free resection margin in rectal cancer surgery. Lancet. 2001; 357: 497—504
49Sauer, R., Becker, H., Hohenberger, W., Rodel, C., Wittekind, C., Fietkau, R., Martus, P., Tschmelitsch, J., Hager, E., Hess, C.F., Karstens, J.H., Liersch, T., Schmidberger, H., Raab, R., and German Rectal Cancer Study G. Preoperative versus postoperative chemoradiotherapy for rectal cancer. N Engl J Med. 2004; 351: 1731—1740
50Rex, D., Cummings, O., and Ulbright, T. Coming to terms with pathologists over colon polyps with cancer or high-grade dysplasia. J Clin Gastroenterol. 2005; 39: 1—3
51Practice parameters Committee of the American College of Gastroenterology and Bond, J.H. Polyp guideline (diagnosis, treatment, and surveillance for patients with colorectal polyps) . Am J Gastroenterol. 2000; 95: 3053—3063
52Langevin, J.M. and Nivatvongs, S. The true incidence of synchronous cancer of the large bowel. A prospective study. Am J Surg. 1984; 147: 330—333
53Pagana, T.J., Ledesma, E.J., Mittelman, A., and Nava, H.R. The use of colonoscopy in the study of synchronous colorectal neoplasms. Cancer. 1984; 53: 356—359
54Rex, D., Sledge, G., Harper, P., Ulbright, T., Loehrer, P., Helper, D., Smith, J., Wiersema, M., Hawes, R., and Lehman, G. 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
55Lieberman, D., Weiss, D., Bond, J., Ahnen, D., Garewal, H., and Chejfec, G. 380. VACSG. Use of colonoscopy to screen asymptomatic adults for colorectal cancer. N Engl J Med. 2000; 343: 162—168
56Imperiale, T., Wagner, D., Lin, C., Larkin, G., Rogge, J., and Ransohoff, D. Risk of advanced proximal neoplasms in asymptomatic adults according to the distal colorectal findings. N Engl J Med. 2000; 343: 169—174
57Imperiale, T.F., Ransohoff, D.F., Itzkowitz, S.H., Turnbull, B.A., Ross, M.E., and 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
58Cali, R.L., Pitsch, R.M., Thorson, A.G., Watson, P., Tapia, P., Blatchford, G.J., and Christensen, M.A. Cumulative incidence of metachronous colorectal cancer. Dis Colon Rectum. 1993; 36: 388—393
59National Polyp Study Work Group, Winawer, S.J., Stewart, E.T., Zauber, A.G., Bond, J.H., Ansel, H., Waye, J.D., Hall, D., Hamlin, J.A., Schapiro, M., O'Brien, M.J., Sternberg, S.S., and Gottlieb, L.A. A comparison of colonoscopy and double-contrast barium enema for surveillance after polypectomy. N Engl J Med. 2000; 342: 1766—1772
60Rockey, D., Paulson, E., Favis, W. et al. Multicenter prospective comparison of colon imaging tests. (abstr)Gastroenterology. 2004; 126: A2004
61Johnson, C.D., Harmsen, W.S., Wilson, L.A., McCarty, R.L., Welch, T.J., Ilstrup, D.M., and Ahlquist, D.A. Prospective blinded evaluation of computed tomographic colonography for screen detection of colorectal polyps. Gastroenterology. 2003; 125: 311—319
62Cotton, P.B., Durkalski, V.L., Pineau, B.C., Palesch, Y.Y., Mauldin, P.D., Hoffman, B., Vining, D.J., Small, W.C., Affronti, J., Rex, D.K. et al. Computed tomographic colonography (virtual colonoscopy). A multicenter comparison with standard colonoscopy for detection of colorectal neoplasia. JAMA. 2004; 291: 1713—1719
63Pickhardt, P.J., Choi, J.R., Hwang, I., Butler, J.A., Puckett, M.L., Hildebrandt, H.A., Wong, R.K., Nugent, P.A., Mysliwiec, P.A., and Schindler, W.R. Computed tomographic virtual colonoscopy to screen for colorectal neoplasia in asymptomatic adults. N Engl J Med. 2003; 349: 2191—2200
64Finkelstein, S. and Bini, E.J. 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
65Bampton, P.A., Sandford, J.J., Cole, S.R., Smith, A., Marcon, J., Cadd, B., and Young, G.P. Interval faecal occult blood testing in a colonoscopy based screening programme detects additional pathology. Gut. 2005; 54: 803—806
66Imperiale, T.F., Ransohoff, D.F., Itzkowitz, S.H., Turnbull, B.A., and Ross, M.E. Fecal DNA versus fecal occult blood for colorectal-cancer screening in an average-risk population. N Engl J Med. 2004; 351: 2704—2714

More on Colonoscopy

FUSE Outperforms Forward-viewing Colonoscopy in Detecting Dysplasia in Patients With IBD

May 23, 2017

Researchers report on the advantages of full-spectrum endoscopy (FUSE) in detecting dysplastic lesions. Read more about this study in the AGA Journals Blog.

Unsuspected Colonic Hemorrhage Found on Screening Colonoscopy

April 27, 2017

A 68-year-old man with hypertension, multiple sclerosis, and neurogenic bladder underwent an inpatient bowel cleansing owing to immobility for a routine screening colonoscopy.

An Unusual Appearance of the Colon Wall

April 26, 2017

A 64-year-old man presented for his first average-risk screening colonoscopy.