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

 

 Buy Article Permissions and Reprints

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.

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
  CrossrefPubMedGoogle Scholar
• 2 Jemal A, Siegel R, Ward E. et al . Cancer statistics, 2007.  CA Cancer J Clin. 2007;  57 43-66
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 5 Winawer S J, Fletcher R H, Miller L. et al . Colorectal cancer screening – clinical guidelines and rationale.  Gastroenterology. 1997;  112 594-642
  CrossrefPubMedGoogle Scholar
• 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
  Article in Thieme ConnectPubMedGoogle Scholar
• 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
  Article in Thieme ConnectPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  Article in Thieme ConnectPubMedGoogle Scholar
• 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
  PubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  PubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  PubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 32 Davila R E, Rajan E, Baron T H. et al . ASGE guideline: colorectal cancer screening and surveillance.  Gastrointest Endosc. 2006;  63 546-557
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 41 Sonnenberg A, Delco F. Cost-effectiveness of a single colonoscopy in screening for colorectal cancer.  Arch Intern Med. 2002;  162 163-168
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  Google Scholar
• 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
  Google Scholar
• 45 Kaiser Permanente Care Management Institute .Colorectal cancer screening clinical practice guideline. Oakland, California; Kaiser Permanente Care Management Institute 2006
  Google Scholar
• 46 Levin B, Burt R W, Drelichman E. et al .Colorectal cancer screening. National Comprehensive Cancer Network 2007
  Google Scholar
• 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
  Google Scholar
• 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
  PubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 50 US Preventive Services Task Force . Screening for colorectal cancer: recommendation and rationale.  Ann Intern Med. 2002;  137 129-131
  PubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 53 Lieberman D A, Weiss D G, Harford W V. et al . Five-year colon surveillance after screening colonoscopy.  Gastroenterology. 2007;  133 1077-1085
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  PubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  PubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  PubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 69 Lieberman D A, Smith F W. Screening for colon malignancy with colonoscopy.  Am J Gastroenterol. 1991;  86 946-951
  PubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  PubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  PubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 83 Mulhall B P, Veerappan G R, Jackson J L. Meta-analysis: computed tomographic colonography.  Ann Int Med. 2005;  142 635-650
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 89 Rex D K. Colonoscopy: a review of its yield for cancers and adenomas by indication.  Am J Gastroenterol. 1995;  90 353-365
  PubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  Google Scholar
• 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
  Google Scholar
• 95 Cairns S, Scholefield J H. Guidelines for colorectal cancer screening in high risk groups.  Gut. 2002;  51 Suppl 5 V1-V2
  CrossrefPubMedGoogle Scholar
• 96 Scottish Intercollegiate Guidelines Network .Management of colorectal cancer. A national clinical guideline. Edinburgh (Scotland); Scottish Intercollegiate Guidelines Network (SIGN) 2003
  Google Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  PubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar
• 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
  CrossrefPubMedGoogle Scholar

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