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Endoscopy 2019; 51(11): 1082-1093
DOI: 10.1055/a-1016-4977
Guideline
© Georg Thieme Verlag KG Stuttgart · New York

Endoscopic management of Lynch syndrome and of familial risk of colorectal cancer: European Society of Gastrointestinal Endoscopy (ESGE) Guideline

Monique E. van Leerdam
 1   Department of Gastroenterology and Hepatology, Netherlands Cancer Institute, Amsterdam, The Netherlands
 2   Department of Gastroenterology and Hepatology, Leiden University Medical Center, Leiden, The Netherlands, Foundation for the Detection of Hereditary Tumours, Leiden, The Netherlands
,
Victorine H. Roos
 3   Department of Gastroenterology and Hepatology, Amsterdam University Medical Centers, University of Amsterdam, Cancer Center Amsterdam, Amsterdam, The Netherlands
,
Jeanin E. van Hooft
 3   Department of Gastroenterology and Hepatology, Amsterdam University Medical Centers, University of Amsterdam, Cancer Center Amsterdam, Amsterdam, The Netherlands
,
Francesc Balaguer
 4   Gastroenterology Department, Hospital Clínic de Barcelona, Barcelona, Spain
 5   Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBERehd), Institut d’Investigacions Biomediques August Pi i Sunyer (IDIBAPS), Universitat de Barcelona, Barcelona, Spain
,
Evelien Dekker
 3   Department of Gastroenterology and Hepatology, Amsterdam University Medical Centers, University of Amsterdam, Cancer Center Amsterdam, Amsterdam, The Netherlands
,
Michal F. Kaminski
 6   Department of Cancer Prevention, The Maria Sklodowska-Curie Memorial Cancer Center and Institute of Oncology, Warsaw, Poland
 7   Department of Gastroenterology, Hepatology and Clinical Oncology, Medical Centre for Postgraduate Education, Warsaw, Poland
 8   Department of Health Management and Health Economics, University of Oslo, Oslo, Norway
,
Andrew Latchford
 9   Polyposis Registry, St. Mark’s Hospital, Harrow, United Kingdom
10   Department of Surgery and Cancer, Imperial College London, London, United Kingdom
,
Helmut Neumann
11   Department of Medicine I, University Medical Center Mainz, Mainz, Germany
,
Luigi Ricciardiello
12   Department of Medical and Surgical Sciences, University of Bologna, Bologna, Italy
,
Maria Rupińska
 6   Department of Cancer Prevention, The Maria Sklodowska-Curie Memorial Cancer Center and Institute of Oncology, Warsaw, Poland
 7   Department of Gastroenterology, Hepatology and Clinical Oncology, Medical Centre for Postgraduate Education, Warsaw, Poland
,
Jean-Christophe Saurin
13   Gastroenterology and Endoscopy Unit, Hospices Civils de Lyon, Hôpital E. Herriot, Lyon, France
,
Pieter J. Tanis
14   Department of Surgery, Amsterdam University Medical Centers, University of Amsterdam, Cancer Center Amsterdam, , Amsterdam, The Netherlands
,
Anja Wagner
15   Department of Clinical Genetics, Erasmus University Medical Center, Erasmus MC Cancer Institute, Rotterdam, The Netherlands
,
Rodrigo Jover
16   Department of Gastroenterology, Hospital General Universitario de Alicante, Instituto de Investigación Sanitaria y Biomédica de Alicante, ISABIAL, Alicante, Spain
,
Maria Pellisé
 4   Gastroenterology Department, Hospital Clínic de Barcelona, Barcelona, Spain
 5   Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBERehd), Institut d’Investigacions Biomediques August Pi i Sunyer (IDIBAPS), Universitat de Barcelona, Barcelona, Spain
› Author Affiliations
Further Information

Publication History

Publication Date:
09 October 2019 (online)

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Main Recommendations

ESGE recommends that individuals with Lynch syndrome should be followed in dedicated units that practice monitoring of compliance and endoscopic performance measures.

Strong recommendation, low quality evidence, level of agreement 100 %.

ESGE recommends starting colonoscopy surveillance at the age of 25 years for MLH1 and MSH2 mutation carriers and at the age of 35 years for MSH6 and PMS2 mutation carriers.

Strong recommendation, moderate quality evidence, level of agreement 100 %.

ESGE recommends the routine use of high-definition endoscopy systems in individuals with Lynch syndrome.

Strong recommendation, high quality evidence, level of agreement 100 %.

ESGE suggests the use of chromoendoscopy may be of benefit in individuals with Lynch syndrome undergoing colonoscopy; however routine use must be balanced against costs, training, and practical considerations.

Weak recommendation, moderate quality evidence, level of agreement 89 %.

ESGE recommends definition of familial risk of colorectal cancer as the presence of at least two first-degree relatives with colorectal cancer or at least one first-degree relative with colorectal cancer before the age of 50 years.

Strong recommendation, moderate quality evidence, level of agreement 92 %.

ESGE recommends colonoscopy surveillance in first-degree relatives of colorectal cancer patients in families that fulfill the definition of familial risk of colorectal cancer.

Strong recommendation, moderate quality evidence, level of agreement 100 %.

Appendices 1s, 2s

 

  • References

  • 1 Bray F, Ferlay J, Soerjomataram I. et al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2018; 68: 394-424
    CrossrefPubMedGoogle Scholar
  • 2 Lichtenstein P, Holm NV, Verkasalo PK. et al. Environmental and heritable factors in the causation of cancer – analyses of cohorts of twins from Sweden, Denmark, and Finland. N Engl J Med 2000; 343: 78-85
    CrossrefPubMedGoogle Scholar
  • 3 Jasperson KW, Tuohy TM, Neklason DW. et al. Hereditary and familial colon cancer. Gastroenterology 2010; 138: 2044-2058
    CrossrefPubMedGoogle Scholar
  • 4 Hampel H, Frankel WL, Martin E. et al. Feasibility of screening for Lynch syndrome among patients with colorectal cancer. J Clin Oncol 2008; 26: 5783-5788
    CrossrefPubMedGoogle Scholar
  • 5 van Leerdam ME, Roos VH, van Hooft JE. et al. Endoscopic management of polyposis syndromes: European Society of Gastrointestinal Endoscopy (ESGE) Guideline. Endoscopy 2019; 51: 877-895
    Article in Thieme ConnectPubMedGoogle Scholar
  • 6 Armelao F, de Pretis G. Familial colorectal cancer: a review. World J Gastroenterol 2014; 20: 9292-9298
    PubMedGoogle Scholar
  • 7 Atkins D, Best D, Briss PA. et al. Grading quality of evidence and strength of recommendations. BMJ 2004; 328: 1490
    CrossrefPubMedGoogle Scholar
  • 8 Dumonceau JM, Hassan C, Riphaus A. et al. European Society of Gastrointestinal Endoscopy (ESGE) guideline development policy. Endoscopy 2012; 44: 626-629
    Article in Thieme ConnectPubMedGoogle Scholar
  • 9 Linstone HA, Turoff M. The Delphi method: Techniques and applications. Addison-Wesley Educational Publishers Inc; 1975
    Google Scholar
  • 10 Jones J, Hunter D. Consensus methods for medical and health services research. BMJ 1995; 311: 376-380
    CrossrefPubMedGoogle Scholar
  • 11 Likert R. A technique for the measurement of attitudes. Arch Psychol 1932; 22: 5-55
    PubMedGoogle Scholar
  • 12 Moreira L, Balaguer F, Lindor N. et al. Identification of Lynch syndrome among patients with colorectal cancer. JAMA 2012; 308: 1555-1565
    CrossrefPubMedGoogle Scholar
  • 13 Win AK, Jenkins MA, Dowty JG. et al. Prevalence and penetrance of major genes and polygenes for colorectal cancer. Cancer Epidemiol Biomarkers Prev 2017; 26: 404-412
    CrossrefPubMedGoogle Scholar
  • 14 Ramsoekh D, Wagner A, van Leerdam ME. et al. Cancer risk in MLH1, MSH2 and MSH6 mutation carriers; different risk profiles may influence clinical management. Hered Cancer Clin Pract 2009; 7: 17
    CrossrefPubMedGoogle Scholar
  • 15 Moller P, Seppala T, Bernstein I. et al. Cancer incidence and survival in Lynch syndrome patients receiving colonoscopic and gynaecological surveillance: first report from the prospective Lynch syndrome database. Gut 2017; 66: 464-472
    CrossrefPubMedGoogle Scholar
  • 16 Moller P, Seppala TT, Bernstein I. et al. Cancer risk and survival in path_MMR carriers by gene and gender up to 75 years of age: a report from the Prospective Lynch Syndrome Database. Gut 2018; 67: 1306-1316
    CrossrefPubMedGoogle Scholar
  • 17 Edelstein DL, Axilbund J, Baxter M. et al. Rapid development of colorectal neoplasia in patients with Lynch syndrome. Clin Gastroenterol Hepatol 2011; 9: 340-343
    CrossrefPubMedGoogle Scholar
  • 18 Jarvinen HJ, 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
  • 19 de Jong AE, Hendriks YM, Kleibeuker JH. et al. Decrease in mortality in Lynch syndrome families because of surveillance. Gastroenterology 2006; 130: 665-671
    CrossrefPubMedGoogle Scholar
  • 20 Jarvinen HJ, Mecklin JP, Sistonen P. Screening reduces colorectal cancer rate in families with hereditary nonpolyposis colorectal cancer. Gastroenterology 1995; 108: 1405-1411
    CrossrefPubMedGoogle Scholar
  • 21 Barrow P, Khan M, Lalloo F. et al. Systematic review of the impact of registration and screening on colorectal cancer incidence and mortality in familial adenomatous polyposis and Lynch syndrome. Br J Surg 2013; 100: 1719-1731
    CrossrefPubMedGoogle Scholar
  • 22 Rutter MD, Beintaris I, Valori R. et al. World Endoscopy Organization consensus statements on post-colonoscopy and post-imaging colorectal cancer. Gastroenterology 2018; 155: 909-925.e3
    CrossrefPubMedGoogle Scholar
  • 23 Ahadova A, von Knebel DoeberitzM, Blaker H. et al. CTNNB1-mutant colorectal carcinomas with immediate invasive growth: a model of interval cancers in Lynch syndrome. Fam Cancer 2016; 15: 579-586
    CrossrefPubMedGoogle Scholar
  • 24 Haanstra JF, Vasen HF, Sanduleanu S. et al. Quality colonoscopy and risk of interval cancer in Lynch syndrome. Int J Colorectal Dis 2013; 28: 1643-1649
    CrossrefPubMedGoogle Scholar
  • 25 Vale Rodrigues R, Claro I, Lage P. et al. Colorectal cancer surveillance in Portuguese families with lynch syndrome: a cohort study. Int J Colorectal Dis 2018; 33: 695-702
    CrossrefPubMedGoogle Scholar
  • 26 Newton K, Green K, Lalloo F. et al. Colonoscopy screening compliance and outcomes in patients with Lynch syndrome. Colorectal Dis 2015; 17: 38-46
    PubMedGoogle Scholar
  • 27 de Vos tot Nederveen Cappel WH, Nagengast FM, Griffioen G. et al. Surveillance for hereditary nonpolyposis colorectal cancer: a long-term study on 114 families. Dis Colon Rectum 2002; 45: 1588-1594
    CrossrefPubMedGoogle Scholar
  • 28 Vasen HF, Abdirahman M, Brohet R. et al. One to 2-year surveillance intervals reduce risk of colorectal cancer in families with Lynch syndrome. Gastroenterology 2010; 138: 2300-2306
    CrossrefPubMedGoogle Scholar
  • 29 van Vugt van Pinxteren MW, van Kouwen MC, van Oijen MG. et al. A prospective study of bowel preparation for colonoscopy with polyethylene glycol-electrolyte solution versus sodium phosphate in Lynch syndrome: a randomized trial. Fam Cancer 2012; 11: 337-341
    CrossrefPubMedGoogle Scholar
  • 30 Argillander TE, Koornstra JJ, van Kouwen M. et al. Features of incident colorectal cancer in Lynch syndrome. United European Gastroenterol J 2018; 6: 1215-1222
    CrossrefPubMedGoogle Scholar
  • 31 Anyla M, Lefevre JH, Creavin B. et al. Metachronous colorectal cancer risk in Lynch syndrome patients-should the endoscopic surveillance be more intensive?. Int J Colorectal Dis 2018; 33: 703-708
    CrossrefPubMedGoogle Scholar
  • 32 de Jong AE, Nagengast FM, Kleibeuker JH. et al. What is the appropriate screening protocol in Lynch syndrome?. Fam Cancer 2006; 5: 373-378
    CrossrefPubMedGoogle Scholar
  • 33 Jarvinen HJ, Renkonen-Sinisalo L, Aktan-Collan K. et al. Ten years after mutation testing for Lynch syndrome: cancer incidence and outcome in mutation-positive and mutation-negative family members. J Clin Oncol 2009; 27: 4793-4797
    CrossrefPubMedGoogle Scholar
  • 34 Engel C, Rahner N, Schulmann K. et al. Efficacy of annual colonoscopic surveillance in individuals with hereditary nonpolyposis colorectal cancer. Clin Gastroenterol Hepatol 2010; 8: 174-182
    CrossrefPubMedGoogle Scholar
  • 35 Engel C, Vasen HF, Seppala T. et al. No difference in colorectal cancer incidence or stage at detection by colonoscopy among 3 countries with different Lynch syndrome surveillance policies. Gastroenterology 2018; 155: 1400-1409.e2
    CrossrefPubMedGoogle Scholar
  • 36 Stuckless S, Green JS, Morgenstern M. et al. Impact of colonoscopic screening in male and female Lynch syndrome carriers with an MSH2 mutation. Clin Genet 2012; 82: 439-445
    CrossrefPubMedGoogle Scholar
  • 37 Stoffel EM, Mercado RC, Kohlmann W. et al. Prevalence and predictors of appropriate colorectal cancer surveillance in Lynch syndrome. American J Gastroenterol 2010; 105: 1851-1860
    PubMedGoogle Scholar
  • 38 Sjostrom O, Lindholm L, Tavelin B. et al. Decentralized colonoscopic surveillance with high patient compliance prevents hereditary and familial colorectal cancer. Fam Cancer 2016; 15: 543-551
    CrossrefPubMedGoogle Scholar
  • 39 Lecomte T, Cellier C, Meatchi T. et al. Chromoendoscopic colonoscopy for detecting preneoplastic lesions in hereditary nonpolyposis colorectal cancer syndrome. Clin Gastroenterol Hepatol 2005; 3: 897-902
    CrossrefPubMedGoogle Scholar
  • 40 Huneburg R, Lammert F, Rabe C. et al. Chromocolonoscopy detects more adenomas than white light colonoscopy or narrow band imaging colonoscopy in hereditary nonpolyposis colorectal cancer screening. Endoscopy 2009; 41: 316-322
    Article in Thieme ConnectPubMedGoogle Scholar
  • 41 Rahmi G, Lecomte T, Malka D. et al. Impact of chromoscopy on adenoma detection in patients with Lynch syndrome: a prospective, multicenter, blinded, tandem colonoscopy study. American J Gastroenterol 2015; 110: 288-298
    PubMedGoogle Scholar
  • 42 Bisschops R, Tejpar S, Willekens H. et al. Virtual chromoendoscopy (I-SCAN) detects more polyps in patients with Lynch syndrome: a randomized controlled crossover trial. Endoscopy 2017; 49: 342-350
    Article in Thieme ConnectPubMedGoogle Scholar
  • 43 East JE, Suzuki N, Stavrinidis M. et al. Narrow band imaging for colonoscopic surveillance in hereditary non-polyposis colorectal cancer. Gut 2008; 57: 65-70
    PubMedGoogle Scholar
  • 44 Stoffel EM, Turgeon DK, Stockwell DH. et al. Missed adenomas during colonoscopic surveillance in individuals with Lynch Syndrome (hereditary nonpolyposis colorectal cancer). Cancer Prev Res (Phila) 2008; 1: 470-475
    CrossrefPubMedGoogle Scholar
  • 45 Hurlstone DP, Karajeh M, Cross SS. et al. The role of high-magnification-chromoscopic colonoscopy in hereditary nonpolyposis colorectal cancer screening: a prospective “back-to-back” endoscopic study. American J Gastroenterol 2005; 100: 2167-2173
    PubMedGoogle Scholar
  • 46 Ramsoekh D, Haringsma J, Poley JW. et al. A back-to-back comparison of white light video endoscopy with autofluorescence endoscopy for adenoma detection in high-risk subjects. Gut 2010; 59: 785-793
    CrossrefPubMedGoogle Scholar
  • 47 Schneider JL, Goddard KAB, Muessig KR. et al. Patient and provider perspectives on adherence to and care coordination of lynch syndrome surveillance recommendations: findings from qualitative interviews. Hered Cancer Clin Pract 2018; 16: 11
    CrossrefPubMedGoogle Scholar
  • 48 Kaminski MF, Thomas-Gibson S, Bugajski M. et al. Performance measures for lower gastrointestinal endoscopy: a European Society of Gastrointestinal Endoscopy (ESGE) Quality Improvement Initiative. Endoscopy 2017; 49: 378-397
    Article in Thieme ConnectPubMedGoogle Scholar
  • 49 Kaminski MF, Hassan C, Bisschops R. et al. Advanced imaging for detection and differentiation of colorectal neoplasia: European Society of Gastrointestinal Endoscopy (ESGE) Guideline. Endoscopy 2014; 46: 435-449
    Article in Thieme ConnectPubMedGoogle Scholar
  • 50 Ten Broeke SW, van der Klift HM, Tops CMJ. et al. Cancer risks for PMS2-associated Lynch syndrome. J Clin Oncol 2018; 36: 2961-2968
    CrossrefPubMedGoogle Scholar
  • 51 Hendriks YM, Wagner A, Morreau H. et al. Cancer risk in hereditary nonpolyposis colorectal cancer due to MSH6 mutations: impact on counseling and surveillance. Gastroenterology 2004; 127: 17-25
    CrossrefPubMedGoogle Scholar
  • 52 Plaschke J, Engel C, Kruger S. et al. Lower incidence of colorectal cancer and later age of disease onset in 27 families with pathogenic MSH6 germline mutations compared with families with MLH1 or MSH2 mutations: the German Hereditary Nonpolyposis Colorectal Cancer Consortium. J Clin Oncol 2004; 22: 4486-4494
    CrossrefPubMedGoogle Scholar
  • 53 Sanchez A, Navarro M, Ocaña T. et al. Colorectal cancer incidence in Lynch syndrome patients: first report of a multicenter nation-wide study. Gastroenterology 2017; 152: S552
    PubMedGoogle Scholar
  • 54 Jenkins MA, Dowty JG, Ait OuakrimD. et al. Short-term risk of colorectal cancer in individuals with lynch syndrome: a meta-analysis. J Clin Oncol 2015; 33: 326-331
    PubMedGoogle Scholar
  • 55 Lamba M, Ebel R, Hamilton SM. et al. 828 – What’s my risk of cancer doctor? Interval colorectal cancer risk in Lynch syndrome: Results from the New Zealand National Registry. Gastroenterology 2019; 156: S-179
    CrossrefPubMedGoogle Scholar
  • 56 Seppala T, Pylvanainen K, Evans DG. et al. Colorectal cancer incidence in path_MLH1 carriers subjected to different follow-up protocols: a prospective Lynch syndrome database report. Hered Cancer Clin Pract 2017; 15: 18
    CrossrefPubMedGoogle Scholar
  • 57 Stupart DA, Goldberg PA, Algar U. et al. Surveillance colonoscopy improves survival in a cohort of subjects with a single mismatch repair gene mutation. Colorectal Dis 2009; 11: 126-130
    CrossrefPubMedGoogle Scholar
  • 58 Lee G, Lee W, Park Y. et al. The surveillance of colorectal adenoma and carcinoma after colectomy for hereditary nonpolyposis colorectal cancer in a positive DNA mismatch repair gene mutation test. Dis Colon Rectum 2012; 55: e213
    PubMedGoogle Scholar
  • 59 Ten Broeke SW, van Bavel TC, Jansen AML. et al. Molecular background of colorectal tumors from patients with Lynch syndrome associated with germline variants in PMS2. Gastroenterology 2018; 155: 844-851
    CrossrefPubMedGoogle Scholar
  • 60 Perrod G, Samaha E, Rahmi G. et al. Impact of an optimized colonoscopic screening program for patients with Lynch syndrome: 6-year results of a specialized French network. Therap Adv Gastroenterol 2018; 11: 1756284818775058
    Google Scholar
  • 61 Haanstra JF, Dekker E, Cats A. et al. Effect of chromoendoscopy in the proximal colon on colorectal neoplasia detection in Lynch syndrome: a multicenter randomized controlled trial. Gastrointest Endosc 2019; DOI: 10.1016/j.gie.2019.04.227. [Epub ahead of print]
    CrossrefPubMedGoogle Scholar
  • 62 Rivero-Sánchez L, Arnau-Collell C, Herrero J. et al. White-light endoscopy is adequate for Lynch syndrome surveillance in a randomized and non-inferiority study. Gastroenterology 2019; DOI: 10.1053/j.gastro.2019.09.003. [Epub ahead of print]
    CrossrefPubMedGoogle Scholar
  • 63 Samaha E, Bellanger J, Dhooge M. et al. Sa1900 Comparison of colonoscopy with virtual chromoendoscopy using third generation narrow band imaging system to chromoendoscopy with indigo carmine in Lynch syndrome patients (the lynch-chromo study). Gastrointest Endosc 2018; 87: AB241
    PubMedGoogle Scholar
  • 64 Barrow E, Hill J, Gareth Evans D. Cancer risk in Lynch syndrome. Fam Cancer 12: 229-240
    PubMedGoogle Scholar
  • 65 Fornasarig M, Magris R, De Re V. et al. Molecular and pathological features of gastric cancer in Lynch Syndrome and familial adenomatous polyposis. Int J Mol Sci 2018; DOI: 10.3390/ijms19061682.
    CrossrefPubMedGoogle Scholar
  • 66 Capelle LG, Van Grieken NC, Lingsma HF. et al. Risk and epidemiological time trends of gastric cancer in Lynch syndrome carriers in the Netherlands. Gastroenterology 2010; 138: 487-492
    CrossrefPubMedGoogle Scholar
  • 67 Aarnio M, Salovaara R, Aaltonen LA. et al. Features of gastric cancer in hereditary non-polyposis colorectal cancer syndrome. Int J Cancer 1997; 74: 551-555
    CrossrefPubMedGoogle Scholar
  • 68 Soer EC, Leicher LW, Langers AM. et al. Equivalent Helicobacter pylori infection rates in Lynch syndrome mutation carriers with and without a first-degree relative with gastric cancer. Int J Colorectal Dis 2016; 31: 693-697
    CrossrefPubMedGoogle Scholar
  • 69 Galiatsatos P, Labos C, Jeanjean M. et al. Low yield of gastroscopy in patients with Lynch syndrome. Turk J Gastroenterol 2017; 28: 434-438
    CrossrefPubMedGoogle Scholar
  • 70 Renkonen-Sinisalo L, Sipponen P, Aarnio M. et al. No support for endoscopic surveillance for gastric cancer in hereditary non-polyposis colorectal cancer. Scand J Gastroenterol 2002; 37: 574-547
    CrossrefPubMedGoogle Scholar
  • 71 Fuccio L, Zagari RM, Minardi ME. et al. Systematic review: Helicobacter pylori eradication for the prevention of gastric cancer. Aliment Pharmacol Ther 2007; 25: 133-141
    PubMedGoogle Scholar
  • 72 Lansdorp-Vogelaar I, Sharp L. Cost-effectiveness of screening and treating Helicobacter pylori for gastric cancer prevention. Best Pract Res Clin Gastroenterol 2013; 27: 933-947
    CrossrefPubMedGoogle Scholar
  • 73 Koornstra JJ, Kleibeuker JH, Vasen HF. Small-bowel cancer in Lynch syndrome: is it time for surveillance?. Lancet Oncol 2008; 9: 901-905
    CrossrefPubMedGoogle Scholar
  • 74 Barrow E, Robinson L, Alduaij W. et al. Cumulative lifetime incidence of extracolonic cancers in Lynch syndrome: a report of 121 families with proven mutations. Clin Genet 2009; 75: 141-149
    CrossrefPubMedGoogle Scholar
  • 75 Bonadona V, Bonaiti B, Olschwang S. et al. Cancer risks associated with germline mutations in MLH1, MSH2, and MSH6 genes in Lynch syndrome. JAMA 2011; 305: 2304-2310
    CrossrefPubMedGoogle Scholar
  • 76 Vasen HF, Stormorken A, Menko FH. et al. MSH2 mutation carriers are at higher risk of cancer than MLH1 mutation carriers: a study of hereditary nonpolyposis colorectal cancer families. J Clin Oncol 2001; 19: 4074-4080
    CrossrefPubMedGoogle Scholar
  • 77 Lynch HT, Smyrk TC, Lynch PM. et al. Adenocarcinoma of the small bowel in lynch syndrome II. Cancer 1989; 64: 2178-2183
    CrossrefPubMedGoogle Scholar
  • 78 Parc Y, Boisson C, Thomas G. et al. Cancer risk in 348 French MSH2 or MLH1 gene carriers. J Med Genet 2003; 40: 208-213
    CrossrefPubMedGoogle Scholar
  • 79 Park JG, Kim DW, Hong CW. et al. Germ line mutations of mismatch repair genes in hereditary nonpolyposis colorectal cancer patients with small bowel cancer: International Society for Gastrointestinal Hereditary Tumours Collaborative Study. Clinical Cancer Res 2006; 12: 3389-3393
    CrossrefPubMedGoogle Scholar
  • 80 Rodriguez-Bigas MA, Vasen HF, Lynch HT. et al. Characteristics of small bowel carcinoma in hereditary nonpolyposis colorectal carcinoma. International Collaborative Group on HNPCC. Cancer 1998; 83: 240-244
    CrossrefPubMedGoogle Scholar
  • 81 Schulmann K, Brasch FE, Kunstmann E. et al. HNPCC-associated small bowel cancer: clinical and molecular characteristics. Gastroenterology 2005; 128: 590-599
    CrossrefPubMedGoogle Scholar
  • 82 ten Kate GL, Kleibeuker JH, Nagengast FM. et al. Is surveillance of the small bowel indicated for Lynch syndrome families?. Gut 2007; 56: 1198-1201
    CrossrefPubMedGoogle Scholar
  • 83 Watson P, Lynch HT. Extracolonic cancer in hereditary nonpolyposis colorectal cancer. Cancer 1993; 71: 677-685
    CrossrefPubMedGoogle Scholar
  • 84 Haanstra JF, Al-Toma A, Dekker E. et al. Prevalence of small-bowel neoplasia in Lynch syndrome assessed by video capsule endoscopy. Gut 2015; 64: 1578-1583
    CrossrefPubMedGoogle Scholar
  • 85 Saurin JC, Pilleul F, Soussan EB. et al. Small-bowel capsule endoscopy diagnoses early and advanced neoplasms in asymptomatic patients with Lynch syndrome. Endoscopy 2010; 42: 1057-1062
    Article in Thieme ConnectPubMedGoogle Scholar
  • 86 Haanstra JF, Al-Toma A, Dekker E. et al. Incidence of small bowel neoplasia in Lynch syndrome assessed by video capsule endoscopy. Endosc Int Open 2017; 5: E622-E626
    Article in Thieme ConnectPubMedGoogle Scholar
  • 87 Hammoudi N, Dhooge M, Coriat R. et al. Duodenal tumor risk in Lynch syndrome. Dig Liver Dis 2019; 51: 299-303
    CrossrefPubMedGoogle Scholar
  • 88 Rex DK, Boland CR, Dominitz JA. et al. Colorectal cancer screening: recommendations for physicians and patients from the U.S. Multi-Society Task Force on Colorectal Cancer. Gastroenterology 2017; 153: 307-323
    CrossrefPubMedGoogle Scholar
  • 89 Leddin D, Lieberman DA, Tse F. et al. Clinical practice guideline on screening for colorectal cancer in individuals with a family history of nonhereditary colorectal cancer or adenoma: The Canadian Association of Gastroenterology Banff Consensus. Gastroenterology 2018; 155: 1325-1347.e3
    CrossrefPubMedGoogle Scholar
  • 90 Provenzale D, Jasperson K, Ahnen DJ. et al. Colorectal cancer screening, version 1.2015. J Natl Compr Canc Netw 2015; 13: 959-968 ; quiz 68
    CrossrefPubMedGoogle Scholar
  • 91 Wong MCS, Chan CH, Lin J. et al. Lower relative contribution of positive family history to colorectal cancer risk with increasing age: a systematic review and meta-analysis of 9.28 million individuals. American J Gastroenterol 2018; 113: 1819-1827
    PubMedGoogle Scholar
  • 92 Butterworth AS, Higgins JP, 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
  • 93 Baglietto L, Jenkins MA, Severi G. et al. Measures of familial aggregation depend on definition of family history: meta-analysis for colorectal cancer. J Clin Epidemiol 2006; 59: 114-124
    CrossrefPubMedGoogle Scholar
  • 94 Johns LE, Houlston RS. A systematic review and meta-analysis of familial colorectal cancer risk. American J Gastroenterol 2001; 96: 2992-3003
    PubMedGoogle Scholar
  • 95 Roos VH, Mangas-Sanjuan C, Rodriguez-Girondo M. et al. Influence of family history on relative and absolute colorectal cancer risk: a systematic review and meta-analysis. Clin Gastroenterol Hepatol 2019; Sep 13. pii: S1542-3565(19)30995-4. DOI: 10.1016/j.cgh.2019.09.007. [Epub ahead of print]
    CrossrefPubMedGoogle Scholar
  • 96 Burt RW. Colon cancer screening. Gastroenterology 2000; 119: 837-853
    CrossrefPubMedGoogle Scholar
  • 97 Kerber RA, Neklason DW, Samowitz WS. et al. Frequency of familial colon cancer and hereditary nonpolyposis colorectal cancer (Lynch syndrome) in a large population database. Fam Cancer 2005; 4: 239-244
    CrossrefPubMedGoogle Scholar
  • 98 Dove-Edwin I, Sasieni P, Adams J. et al. Prevention of colorectal cancer by colonoscopic surveillance in individuals with a family history of colorectal cancer: 16 year, prospective, follow-up study. BMJ 2005; 331: 1047
    CrossrefPubMedGoogle Scholar
  • 99 Hatfield E, Green JS, Woods MO. et al. Impact of colonoscopic screening in familial colorectal cancer type X. Mol Genet Genomic Med 2018; 6: 1021-1030
    CrossrefPubMedGoogle Scholar
  • 100 Brenner H, Chang-Claude J, Seiler CM. et al. Long-term risk of colorectal cancer after negative colonoscopy. J Clin Oncol 2011; 29: 3761-3767
    CrossrefPubMedGoogle Scholar
  • 101 Samadder NJ, Pappas L, Boucherr KM. et al. Long-term colorectal cancer incidence after negative colonoscopy in the state of Utah: the effect of family history. Am J Gastroenterol 2017; 112: 1439-1447
    CrossrefPubMedGoogle Scholar
  • 102 Hennink SD, van der Meulen-de Jong AE, Wolterbeek R. et al. Randomized comparison of surveillance intervals in familial colorectal cancer. J Clin Oncol 2015; 33: 4188-4193
    CrossrefPubMedGoogle Scholar
  • 103 Fuchs CS, Giovannucci EL, Colditz GA. et al. A prospective study of family history and the risk of colorectal cancer. N Engl J Med 1994; 331: 1669-1674
    CrossrefPubMedGoogle Scholar
  • 104 Hemminki K, Li X. Familial colorectal adenocarcinoma from the Swedish Family-Cancer Database. Int J Cancer 2001; 94: 743-748
    CrossrefPubMedGoogle Scholar
  • 105 Andrieu N, Launoy G, Guillois R. et al. Familial relative risk of colorectal cancer: a population-based study. Eur J Cancer 2003; 39: 1904-1911
    CrossrefPubMedGoogle Scholar
  • 106 Johns LE, Kee F, Collins BJ. et al. Colorectal cancer mortality in first-degree relatives of early-onset colorectal cancer cases. Dis Colon Rectum 2002; 45: 681-686
    CrossrefPubMedGoogle Scholar
  • 107 Kune GA, Kune S, Watson LF. The role of heredity in the etiology of large bowel cancer: data from the Melbourne Colorectal Cancer Study. World J Surg 1989; 13: 124-129 ; discussion 9–31
    CrossrefPubMedGoogle Scholar
  • 108 Samadder NJ, Smith KR, Hanson H. et al. Increased risk of colorectal cancer among family members of all ages, regardless of age of index case at diagnosis. Clin Gastroenterol Hepatol 2015; 13: 2305-2311.e1-2
    CrossrefPubMedGoogle Scholar