Appropriateness of colonoscopy in Europe (EPAGE II) – Screening for colorectal cancer

C. Arditi; I. Peytremann-Bridevaux; B. Burnand; V. F. Eckardt; P. Bytzer; L. Agréus; R. W. Dubois; J.-P. Vader; F. Froehlich; V. Pittet; S. Schusselé Filliettaz; P. Juillerat; J.-J. Gonvers; null and the EPAGE II Study Group

doi:10.1055/s-0028-1119626

Endoscopy 2009; 41(3): 200-208
DOI: 10.1055/s-0028-1119626

Original article

Appropriateness of colonoscopy in Europe (EPAGE II) – Screening for colorectal cancer

C. Arditi¹ , I. Peytremann-Bridevaux¹ , B. Burnand¹ , V. F. Eckardt² , P. Bytzer³ , L. Agréus⁴ , R. W. Dubois⁵ , J.-P. Vader¹ , F. Froehlich^6, ⁷ , V. Pittet¹ , S. Schusselé Filliettaz¹ , P. Juillerat⁶ , J.-J. Gonvers⁶ , and the EPAGE II Study Group⁸

¹Healthcare Evaluation Unit, Institute of Social and Preventive Medicine (IUMSP), Centre Hospitalier Universitaire Vaudois and University of Lausanne, Lausanne, Switzerland
²Gastroenterology Department, Deutsche Klinik für Diagnostik, Wiesbaden, Germany
³Department of Medical Gastroenterology, Køge University Hospital and Copenhagen University, Copenhagen, Denmark
⁴Center for Family and Community Medicine, Karolinska Institutet, Huddinge, Sweden
⁵Cerner LifeSciences, Beverly Hills, USA
⁶Department of Gastroenterology and Hepatology, Centre Hospitalier Universitaire Vaudois and University of Lausanne, Lausanne, Switzerland
⁷Department of Gastroenterology, University of Basle, Basle, Switzerland
⁸The EPAGE II Study Group[*]

Abstract

Background and study aims: To summarize the published literature on assessment of appropriateness of colonoscopy for screening for colorectal cancer (CRC) in asymptomatic individuals without personal history of CRC or polyps, and report appropriateness criteria developed by an expert panel, the 2008 European Panel on the Appropriateness of Gastrointestinal Endoscopy, EPAGE II.

Methods: A systematic search of guidelines, systematic reviews, and primary studies regarding colonoscopy for screening for colorectal cancer was performed. The RAND/UCLA Appropriateness Method was applied to develop appropriateness criteria for colonoscopy in these circumstances.

Results: Available evidence for CRC screening comes from small case-controlled studies, with heterogeneous results, and from indirect evidence from randomized controlled trials (RCTs) on fecal occult blood test (FOBT) screening and studies on flexible sigmoidoscopy screening. Most guidelines recommend screening colonoscopy every 10 years starting at age 50 in average-risk individuals. In individuals with a higher risk of CRC due to family history, there is a consensus that it is appropriate to offer screening colonoscopy at < 50 years. EPAGE II considered screening colonoscopy appropriate above 50 years in average-risk individuals. Panelists deemed screening colonoscopy appropriate for younger patients, with shorter surveillance intervals, where family or personal risk of colorectal cancer is higher. A positive FOBT or the discovery of adenomas at sigmoidoscopy are considered appropriate indications.

Conclusions: Despite the lack of evidence based on randomized controlled trials (RCTs), colonoscopy is recommended by most published guidelines and EPAGE II criteria available online (http://www.epage.ch), as a screening option for CRC in individuals at average risk of CRC, and undisputedly as the main screening tool for CRC in individuals at moderate and high risk of CRC.

Full Text

References

1 Ferlay J, Autier P, Boniol M. et al . Estimates of the cancer incidence and mortality in Europe in 2006. Ann Oncol. 2007; 18 581-592
2 Jemal A, Siegel R, Ward E. et al . Cancer statistics, 2007. CA Cancer J Clin. 2007; 57 43-66
3 Fleshner P, Slater G, Aufses jr A H. Age and sex distribution of patients with colorectal cancer. Dis Colon Rectum. 1989; 32 107-111
4 Sant M, Capocaccia R, Verdecchia A. et al . Comparisons of colon-cancer survival among European countries: The Eurocare Study. Int J Cancer. 1995; 63 43-48
5 Winawer S J, Fletcher R H, Miller L. et al . Colorectal cancer screening – clinical guidelines and rationale. Gastroenterology. 1997; 112 594-642
6 Burnand B, Bochud M, Froehlich F. et al . 14. Appropriateness of colonoscopy: screening for colorectal cancer in asymptomatic individuals. Endoscopy. 1999; 31 673-683
7 Juillerat P, Peytremann-Bridevaux I, Vader J P. et al . Appropriateness of colonoscopy in Europe (EPAGE II) Presentation of methodology, general results, and analysis of complications. Endoscopy. 2009; 41 240-246
8 Rex D K, Cutler C S, Lemmel G T. et al . Colonoscopic miss rates of adenomas determined by back-to-back colonoscopies. Gastroenterology. 1997; 112 24-28
9 Harris J K, Froehlich F, Wietlisbach V. et al . Factors associated with the technical performance of colonoscopy: An EPAGE Study. Dig Liver Dis. 2007; 39 678-689
10 Pickhardt P J, Choi J R, Hwang I. et al . Computed tomographic virtual colonoscopy to screen for colorectal neoplasia in asymptomatic adults. N Engl J Med. 2003; 349 2191-2200
11 van Gelder R E, Nio C Y, Florie J. et al . Computed tomographic colonography compared with colonoscopy in patients at increased risk for colorectal cancer. Gastroenterology. 2004; 127 41-48
12 Adler A, Roll S, Marowski B. et al . Appropriateness of colonoscopy in the era of colorectal cancer screening: a prospective, multicenter study in a private-practice setting (Berlin Colonoscopy Project 1, BECOP 1). Dis Colon Rectum. 2007; 50 1628-1638
13 Byeon J S, Yang S K, Kim T I. et al . Colorectal neoplasm in asymptomatic Asians: a prospective multinational multicenter colonoscopy survey. Gastrointest Endosc. 2007; 65 1015-1022
14 Eisele R, Vogelsang E, Kraft K. et al . Screening for colorectal lesions with high-resolution video colonoscopes in a German male average-risk population at 40 to 59 years of age. Z Gastroenterol. 2007; 45 952-957
15 Gonvers J J, Harris J K, Wietlisbach V. et al . A European view of diagnostic yield and appropriateness of colonoscopy. Hepatogastroenterology. 2007; 54 729-735
16 Imperiale T F, Wagner D R, Lin C Y. et al . Results of screening colonoscopy among persons 40 to 49 years of age. N Engl J Med. 2002; 346 1781-1785
17 Lieberman D A, Weiss D G, Bond J H. et al . Use of colonoscopy to screen asymptomatic adults for colorectal cancer. Veterans Affairs Cooperative Study Group 380. N Engl J Med. 2000; 343 162-168
18 Morikawa T, Kato J, Yamaji Y. et al . A comparison of the immunochemical fecal occult blood test and total colonoscopy in the asymptomatic population. Gastroenterology. 2005; 129 422-428
19 Regula J, Rupinski M, Kraszewska E. et al . Colonoscopy in colorectal-cancer screening for detection of advanced neoplasia. N Engl J Med. 2006; 355 1863-1872
20 Schoenfeld P, Cash B, Flood A. et al . Colonoscopic screening of average-risk women for colorectal neoplasia. N Engl J Med. 2005; 352 2061-2068
21 Strul H, Kariv R, Leshno M. et al . The prevalence rate and anatomic location of colorectal adenoma and cancer detected by colonoscopy in average-risk individuals aged 40–80 years. Am J Gastroenterol. 2006; 101 255-262
22 Sung J J, Chan F K, Leung W K. et al . Screening for colorectal cancer in Chinese: comparison of fecal occult blood test, flexible sigmoidoscopy, and colonoscopy. Gastroenterology. 2003; 124 608-614
23 Thiis-Evensen E, Hoff G S, Sauar J. et al . Flexible sigmoidoscopy or colonoscopy as a screening modality for colorectal adenomas in older age groups? Findings in a cohort of the normal population aged 63 – 72 years. Gut. 1999; 45 834-839
24 Brenner H, Arndt V, Sturmer T. et al . Long-lasting reduction of risk of colorectal cancer following screening endoscopy. Br J Cancer. 2001; 85 972-976
25 Cotterchio M, Manno M, Klar N. et al . Colorectal screening is associated with reduced colorectal cancer risk: a case–control study within the population-based Ontario Familial Colorectal Cancer Registry. Cancer Causes Control. 2005; 16 865-875
26 Singh H, Turner D, Xue L. et al . Risk of developing colorectal cancer following a negative colonoscopy examination: evidence for a 10-year interval between colonoscopies. JAMA. 2006; 295 2366-2373
27 Muller A D, Sonnenberg A. Prevention of colorectal cancer by flexible endoscopy and polypectomy. A case–control study of 32,702 veterans. Ann Int Med. 1995; 123 904-910
28 Muller A D, Sonnenberg A. Protection by endoscopy against death from colorectal cancer. A case–control study among veterans. Arch Intern Med. 1995; 155 1741-1748
29 Kronborg O, Jorgensen O D, Fenger C, Rasmussen M. Randomized study of biennial screening with a faecal occult blood test: results after nine screening rounds. Scand J Gastroenterol. 2004; 39 846-851
30 Mandel J S, Church T R, Ederer F, Bond J H. Colorectal cancer mortality: effectiveness of biennial screening for fecal occult blood. JNCI. 1999; 91 434-437
31 Scholefield J H, Moss S, Sufi F. et al . Effect of faecal occult blood screening on mortality from colorectal cancer: results from a randomised controlled trial. Gut. 2002; 50 840-844
32 Davila R E, Rajan E, Baron T H. et al . ASGE guideline: colorectal cancer screening and surveillance. Gastrointest Endosc. 2006; 63 546-557
33 Imperiale T F, Wagner D R, Lin C Y. et al . Risk of advanced proximal neoplasms in asymptomatic adults according to the distal colorectal findings. N Engl J Med. 2000; 343 169-174
34 Lieberman D A, Weiss D G. One-time screening for colorectal cancer with combined fecal occult-blood testing and examination of the distal colon. N Engl J Med. 2001; 345 555-560
35 Bertario L, Russo A, Sala P. et al . Predictors of metachronous colorectal neoplasms in sporadic adenoma patients. Int J Cancer. 2003; 105 82-87
36 Citarda F, Tomaselli G, Capocaccia R. et al . Efficacy in standard clinical practice of colonoscopic polypectomy in reducing colorectal cancer incidence. Gut. 2001; 48 812-815
37 Jorgensen O D, Kronborg O, Fenger C, Rasmussen M. Influence of long-term colonoscopic surveillance on incidence of colorectal cancer and death from the disease in patients with precursors (adenomas). Acta Oncol (Stockholm, Sweden). 2007; 46 355-360
38 Thiis-Evensen E, Hoff G S, Sauar J. et al . Population-based surveillance by colonoscopy: effect on the incidence of colorectal cancer. Telemark Polyp Study I. Scand J Gastroenterol. 1999; 34 414-420
39 Winawer S J, Zauber A G, Ho M N. et al . Prevention of colorectal cancer by colonoscopic polypectomy (The National Polyp Study Workgroup). N Engl J Med. 1993; 329 1977-1981
40 Frazier A L, Colditz G A, Fuchs C S, Kuntz K M. Cost-effectiveness of screening for colorectal cancer in the general population. JAMA. 2000; 284 1954-1961
41 Sonnenberg A, Delco F. Cost-effectiveness of a single colonoscopy in screening for colorectal cancer. Arch Intern Med. 2002; 162 163-168
42 Vijan S, Hwang E W, Hofer T P, Hayward R A. Which colon cancer screening test? A comparison of costs, effectiveness, and compliance. Am J Med. 2001; 111 593-601
43 Australian Cancer Network Colorectal Cancer Guidelines Revision Committee .Guidelines for the prevention, early detection and management of colorectal cancer. Sydney; The Cancer Council Australia and Australian Cancer Network 2005
44 Coombs A, Jones-McLean E, Le Petit C. et al .Technical report for the National Committee on Colorectal Cancer Screening; 2002. http://Available at: www.phac-aspc.gc.ca/publicat/ncccs-cndcc/ackn-eng.php
45 Kaiser Permanente Care Management Institute .Colorectal cancer screening clinical practice guideline. Oakland, California; Kaiser Permanente Care Management Institute 2006
46 Levin B, Burt R W, Drelichman E. et al .Colorectal cancer screening. National Comprehensive Cancer Network 2007
47 McLeod R S. with the Canadian Task Force on Preventive Health Care .Screening strategies for colorectal cancer. Systematic review and recommendations. Canadian Task Force on Preventive Health Care 2001
48 Rex D K, Johnson D A, Lieberman D A. et al . Colorectal cancer prevention 2000: screening recommendations of the American College of Gastroenterology. American College of Gastroenterology. Am J Gastroenterol. 2000; 95 868-877
49 Smith R A, Cokkinides V, Eyre H J. American Cancer Society guidelines for the early detection of cancer, 2006. CA Cancer J Clin. 2006; 56 11-25
50 US Preventive Services Task Force . Screening for colorectal cancer: recommendation and rationale. Ann Intern Med. 2002; 137 129-131
51 Winawer S, Fletcher R, Rex D. et al . Colorectal cancer screening and surveillance: clinical guidelines and rationale – update based on new evidence. Gastroenterology. 2003; 124 544-560
52 Levin B, Lieberman D A, McFarland B. et al . Screening and surveillance for the early detection of colorectal cancer and adenomatous polyps, 2008: a joint guideline from the American Cancer Society, the US Multi-Society Task Force on Colorectal Cancer, and the American College of Radiology. Gastroenterology. 2008; 134 1570-1595
53 Lieberman D A, Weiss D G, Harford W V. et al . Five-year colon surveillance after screening colonoscopy. Gastroenterology. 2007; 133 1077-1085
54 Rex D K, Cummings O W, Helper D J. et al . 5-year incidence of adenomas after negative colonoscopy in asymptomatic average-risk persons. Gastroenterology. 1996; 111 1178-1181
55 Allison J E, Sakoda L C, Levin T R. et al . Screening for colorectal neoplasms with new fecal occult blood tests: update on performance characteristics. JNCI. 2007; 99 1462-1470
56 Allison J E, Tekawa I S, Ransom L J, Adrain A L. A comparison of fecal occult blood tests for colorectal cancer screening. N Engl J Med. 1996; 334 155-159
57 Greenberg P D, Bertario L, Gnauck R. et al . A prospective multicenter evaluation of new fecal occult blood tests in patients undergoing colonoscopy. Am J Gastroenterol. 2000; 95 1331-1338
58 Brevinge H, Lindholm E, Buntzen S, Kewenter J. Screening for colorectal neoplasia with faecal occult blood testing compared with flexible sigmoidoscopy directly in a 55–56 years old population. Int J Colorect Dis. 1997; 12 291-295
59 Hardcastle J D, Chamberlain J O, Robinson M H. et al . Randomised controlled trial of faecal-occult-blood screening for colorectal cancer. Lancet. 1996; 348 1472-1477
60 Jorgensen O D, Kronborg O, Fenger C. A randomised study of screening for colorectal cancer using faecal occult blood testing: results after 13 years and seven biennial screening rounds. Gut. 2002; 50 29-32
61 Kewenter J, Brevinge H, Engaras B. et al . Follow-up after screening for colorectal neoplasms with fecal occult blood testing in a controlled trial. Dis Colon Rectum. 1994; 37 115-119
62 Kronborg O, Fenger C, Olsen J. et al . Randomised study of screening for colorectal cancer with faecal occult blood test. Lancet. 1996; 348 1467-1471
63 Mandel J S, Bond J H, Church T R. et al . Reducing mortality from colorectal cancer by screening for fecal occult blood. Minnesota Colon Cancer Control Study. N Engl J Med. 1993; 328 1365-1371
64 Mandel J S, Church T R, Bond J H. et al . The effect of fecal occult-blood screening on the incidence of colorectal cancer. N Engl J Med. 2000; 343 1603-1607
65 Hewitson P, Glasziou P, Irwig L. et al . Screening for colorectal cancer using the faecal occult blood test, Hemoccult. Cochrane Database Syst Rev. 2007; CD001216
66 Lang C A, Ransohoff D F. Fecal occult blood screening for colorectal cancer. is mortality reduced by chance selection for screening colonoscopy?. Jama. 1994; 271 1011-1013
67 Solomon M J, McLeod R S. Periodic health examination, 1994 update: 2. Screening strategies for colorectal cancer. Canadian Task Force on the Periodic Health Examination. Can Med Assoc J. 1994; 150 1961-1970
68 Foutch P G, Mai H, Pardy K. et al . Flexible sigmoidoscopy may be ineffective for secondary prevention of colorectal cancer in asymptomatic, average-risk men. Dig Dis Sci. 1991; 36 924-928
69 Lieberman D A, Smith F W. Screening for colon malignancy with colonoscopy. Am J Gastroenterol. 1991; 86 946-951
70 Anderson J C, Alpern Z, Messina C R. et al . Predictors of proximal neoplasia in patients without distal adenomatous pathology. Am J Gastroenterol. 2004; 99 472-477
71 Hoff G, Sauar J, Vatn M H. et al . Polypectomy of adenomas in the prevention of colorectal cancer: 10 years’ follow-up of the Telemark Polyp Study I. A prospective, controlled population study. Scand J Gastroenterol. 1996; 31 1006-1010
72 Thiis-Evensen E, Hoff G S, Sauar J. et al . The effect of attending a flexible sigmoidoscopic screening program on the prevalence of colorectal adenomas at 13-year follow-up. Am J Gastroenterol. 2001; 96 1901-1907
73 UK Flexible Simoidoscopy Screening Trial Investigators . Single flexible sigmoidoscopy screening to prevent colorectal cancer: baseline findings of a UK multicentre randomised trial. Lancet. 2002; 359 1291-1300
74 Atkin W S, Edwards R, Wardle J. et al . Design of a multicentre randomised trial to evaluate flexible sigmoidoscopy in colorectal cancer screening. J Med Screen. 2001; 8 137-144
75 Bretthauer M, Gondal G, Larsen K. et al . Design, organization and management of a controlled population screening study for detection of colorectal neoplasia: attendance rates in the NORCCAP study (Norwegian Colorectal Cancer Prevention). Scand J Gastroenterol. 2002; 37 568-573
76 Gondal G, Grotmol T, Hofstad B. et al . The Norwegian Colorectal Cancer Prevention (NORCCAP) screening study: baseline findings and implementations for clinical work-up in age groups 50–64 years. Scand J Gastroenterol. 2003; 38 635-642
77 Segnan N, Senore C, Andreoni B. et al . Randomized trial of different screening strategies for colorectal cancer: patient response and detection rates. JNCI. 2005; 97 347-357
78 Segnan N, Senore C, Andreoni B. et al . Baseline findings of the Italian multicenter randomized controlled trial of “once-only sigmoidoscopy” – SCORE. JNCI. 2002; 94 1763-1772
79 Segnan N, Senore C, Andreoni B. et al . Comparing attendance and detection rate of colonoscopy with sigmoidoscopy and FIT for colorectal cancer screening. Gastroenterology. 2007; 132 2304-2312
80 Weissfeld J L, Schoen R E, Pinsky P F. et al . Flexible sigmoidoscopy in the PLCO cancer screening trial: results from the baseline screening examination of a randomized trial. JNCI. 2005; 97 989-997
81 Newcomb P A, Storer B E, Morimoto L M. et al . Long-term efficacy of sigmoidoscopy in the reduction of colorectal cancer incidence. JNCI. 2003; 95 622-625
82 Slattery M L, Edwards S L, Ma K N, Friedman G D. Colon cancer screening, lifestyle, and risk of colon cancer. Cancer Causes Control. 2000; 11 555-563
83 Mulhall B P, Veerappan G R, Jackson J L. Meta-analysis: computed tomographic colonography. Ann Int Med. 2005; 142 635-650
84 Imperiale T F, Ransohoff D F, Itzkowitz S H. et al . Fecal DNA versus fecal occult blood for colorectal-cancer screening in an average-risk population. N Engl J Med. 2004; 351 2704-2714
85 Butterworth A S, Higgins J PT, Pharoah P. Relative and absolute risk of colorectal cancer for individuals with a family history: a meta-analysis. Eur J Cancer. 2006; 42 216-227
86 Johns L E, Houlston R S. A systematic review and meta-analysis of familial colorectal cancer risk. Am J Gastroenterol. 2001; 96 2992-3003
87 Cottet V, Pariente A, Nalet B. et al . Colonoscopic screening of first-degree relatives of patients with large adenomas: increased risk of colorectal tumors. Gastroenterology. 2007; 133 1086-1092
88 Guillem J G, Forde K A, Treat M R. et al . Colonoscopic screening for neoplasms in asymptomatic first- degree relatives of colon cancer patients. A controlled, prospective study. Dis Colon Rectum. 1992; 35 523-529
89 Rex D K. Colonoscopy: a review of its yield for cancers and adenomas by indication. Am J Gastroenterol. 1995; 90 353-365
90 Sauar J, Hausken T, Hoff G. et al . Colonoscopic screening examination of relatives of patients with colorectal cancer. I. A comparison with an endoscopically screened normal population. Scand J Gastroenterol. 1992; 27 661-666
91 Dowling D J, St John D J, Macrae F A, Hopper J L. Yield from colonoscopic screening in people with a strong family history of common colorectal cancer. J Gastroenterol Hepatol. 2000; 15 939-944
92 Niv Y, Dickman R, Figer A. et al . Case–control study of screening colonoscopy in relatives of patients with colorectal cancer. Am J Gastroenterol. 2003; 98 486-489
93 French National Agency for Accreditation and Evaluation in Healthcare .Clinical practice guidelines: indications for lower gastrointestinal endoscopy (excluding population screening). 2004. http://Available at: http://www.has-sante.fr/portail/upload/docs/application/pdf/Endoscopy_guidelines.pdf
94 New Zealand Guidelines Group .Surveillance and management of groups at increased risk of colorectal cancer. Wellington, New Zealand; New Zealand Guidelines Group (NZGG); 2004. http://Available at: www.nzgg.org.nz/guidelines/0048/040624_FINAL_Full_for_Web_Colorectal_Guideline1.pdf
95 Cairns S, Scholefield J H. Guidelines for colorectal cancer screening in high risk groups. Gut. 2002; 51 Suppl 5 V1-V2
96 Scottish Intercollegiate Guidelines Network .Management of colorectal cancer. A national clinical guideline. Edinburgh (Scotland); Scottish Intercollegiate Guidelines Network (SIGN) 2003
97 Vasen H F, Mecklin J P, Watson P. et al . Surveillance in hereditary nonpolyposis colorectal cancer: an international cooperative study of 165 families. The International Collaborative Group on HNPCC. Dis Colon Rectum. 1993; 36 1-4
98 Vasen H F, Moslein G, Alonso A. et al . Guidelines for the clinical management of Lynch syndrome (hereditary non-polyposis cancer). J Med Genet. 2007; 44 353-362
99 Lynch H T, Smyrk T, Lynch J. et al . Update on the differential diagnosis, surveillance and management of hereditary non-polyposis colorectal cancer. Eur J Cancer. 1995; 31A 1039-1046
100 Jarvinen H J, Aarnio M, Mustonen H. et al . Controlled 15-year trial on screening for colorectal cancer in families with hereditary nonpolyposis colorectal cancer. Gastroenterology. 2000; 118 829-834
101 Jarvinen H J, Mecklin J P, Sistonen P. Screening reduces colorectal cancer rate in families with hereditary nonpolyposis colorectal cancer. Gastroenterology. 1995; 108 1405-1411
102 Heiskanen I, Luostarinen T, Jârvinen H J. Impact of screening examinations on survival in familial adenomatous polyposis. Scand J Gastroenterol. 2000; 35 1284-1287

1 See Appendix: The EPAGE II Study Group

J.-J. GonversMD

Policlinique Médicale Universitaire (PMU/CHUV)

Rue du Bugnon 44
CH-1011 Lausanne
Switzerland

Fax: +41-21-3144718

Email: jean-jacques.gonvers@chuv.ch

Supplementary Material

Fig. e1b

Table e1

Table e2

Table e3

Table e4

Table e5

Table e6

Table e7

Table e8