Digestive Diseases and Sciences

, Volume 60, Issue 3, pp 734–747 | Cite as

Hereditary and Common Familial Colorectal Cancer: Evidence for Colorectal Screening

  • N. Jewel Samadder
  • Kory Jasperson
  • Randall W. Burt


Colorectal cancer (CRC) is the fourth most common cancer among men and women. Between 3 and 6 % of all CRCs are attributed to well-defined inherited syndromes, including Lynch syndrome, familial adenomatous polyposis, MUTYH-associated polyposis and several hamartomatous conditions. Up to 30 % of CRC cases exhibit common familial risk, likely related to a combination of inherited factors and environment. Identification of these patients through family history and appropriate genetic testing can provide estimates of cancer risk that inform appropriate cancer screening, surveillance and/or preventative interventions. This article examines the colon cancer syndromes, their genetic basis, clinical management and evidence supporting colorectal screening. It also deals with the category of common (non-syndromic) familial risk including risk determination and screening guidelines.


Colorectal cancer Familial Hereditary Screening Lynch FAP 



The study was funded by the National Cancer Institute, American College of Gastroenterology, American Society for Gastrointestinal Endoscopy and the Huntsman Cancer Foundation. The funding sources did not play a role in the design, conduct or reporting of the study or in the decision to submit the manuscript for publication.

Conflict of interest

RWB is a consultant for Myriad Genetics and NJS is a consultant for Cook Medical. No other authors have a conflict of interest to disclose.


Support for this project was provided by NCI grants P01-CA073992 (RWB), R01-CA040641 (RWB), an Endoscopic Research Award from the American Society for Gastrointestinal Endoscopy (NJS) and a Junior Faculty Career Development Award from the American College of Gastroenterology (NJS). Partial support for the Utah Population Database and this project was provided by the Huntsman Cancer Institute Cancer Center Support Grant P30CA042014 from the National Cancer institute and the Huntsman Cancer Foundation. Support for the Utah Cancer Registry is provided by Contract #HHSN 261201000026C from the National Cancer Institute with additional support from the Utah Department of Health and the University of Utah.


  1. 1.
    Siegel R, Naishadham D, Jemal A. Cancer statistics, 2013. CA Cancer J Clin. 2013;63:11–30.PubMedGoogle Scholar
  2. 2.
    Burt RW, DiSario JA, Cannon-Albright L. Genetics of colon cancer: impact of inheritance on colon cancer risk. Annu Rev Med. 1995;46:371–379.PubMedGoogle Scholar
  3. 3.
    Network. NCC. NCCN Clinical Practice Guidelines in Oncology. Volume 2014., 2013.
  4. 4.
    Quehenberger F, Vasen HF, van Houwelingen HC. Risk of colorectal and endometrial cancer for carriers of mutations of the hMLH1 and hMSH2 gene: correction for ascertainment. J Med Genet. 2005;42:491–496.PubMedCentralPubMedGoogle Scholar
  5. 5.
    Jenkins MA, Baglietto L, Dowty JG, et al. Cancer risks for mismatch repair gene mutation carriers: a population-based early onset case-family study. Clin Gastroenterol Hepatol. 2006;4:489–498.PubMedGoogle Scholar
  6. 6.
    Stoffel E, Mukherjee B, Raymond VM, et al. Calculation of risk of colorectal and endometrial cancer among patients with Lynch syndrome. Gastroenterology. 2009;137:1621–1627.PubMedCentralPubMedGoogle Scholar
  7. 7.
    Aarnio M, Sankila R, Pukkala E, et al. Cancer risk in mutation carriers of DNA-mismatch-repair genes. Int J Cancer. 1999;81:214–218.PubMedGoogle Scholar
  8. 8.
    Vasen HF, Mecklin JP, Khan PM, et al. The International Collaborative Group on Hereditary Non-Polyposis Colorectal Cancer (ICG-HNPCC). Dis Colon Rectum. 1991;34:424–425.PubMedGoogle Scholar
  9. 9.
    Rustgi AK. The genetics of hereditary colon cancer. Genes Dev. 2007;21:2525–2538.PubMedGoogle Scholar
  10. 10.
    de la Chapelle A, Palomaki G, Hampel H. Identifying Lynch syndrome. Int J Cancer. 2009;125:1492–1493.PubMedCentralPubMedGoogle Scholar
  11. 11.
    Palomaki GE, McClain MR, Melillo S, et al. EGAPP supplementary evidence review: DNA testing strategies aimed at reducing morbidity and mortality from Lynch syndrome. Genet Med. 2009;11:42–65.PubMedCentralPubMedGoogle Scholar
  12. 12.
    Kastrinos F, Mukherjee B, Tayob N, et al. Risk of pancreatic cancer in families with Lynch syndrome. JAMA. 2009;302:1790–1795.PubMedCentralPubMedGoogle Scholar
  13. 13.
    Peltomaki P, Vasen H. Mutations associated with HNPCC predisposition—update of ICG-HNPCC/INSiGHT mutation database. Dis Markers. 2004;20:269–276.PubMedCentralPubMedGoogle Scholar
  14. 14.
    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.PubMedGoogle Scholar
  15. 15.
    Senter L, Clendenning M, Sotamaa K, et al. The clinical phenotype of Lynch syndrome due to germ-line PMS2 mutations. Gastroenterology. 2008;135:419–428.PubMedCentralPubMedGoogle Scholar
  16. 16.
    Kempers MJ, Kuiper RP, Ockeloen CW, et al. Risk of colorectal and endometrial cancers in EPCAM deletion-positive Lynch syndrome: a cohort study. Lancet Oncol. 2011;12:49–55.PubMedCentralPubMedGoogle Scholar
  17. 17.
    Kuiper RP, Vissers LE, Venkatachalam R, et al. Recurrence and variability of germline EPCAM deletions in Lynch syndrome. Hum Mutat. 2011;32:407–414.PubMedGoogle Scholar
  18. 18.
    Kovacs ME, Papp J, Szentirmay Z, et al. Deletions removing the last exon of TACSTD1 constitute a distinct class of mutations predisposing to Lynch syndrome. Hum Mutat. 2009;30:197–203.PubMedGoogle Scholar
  19. 19.
    Niessen RC, Hofstra RM, Westers H, et al. Germline hypermethylation of MLH1 and EPCAM deletions are a frequent cause of Lynch syndrome. Genes Chromosomes Cancer. 2009;48:737–744.PubMedGoogle Scholar
  20. 20.
    Ligtenberg MJ, Kuiper RP, Chan TL, et al. Heritable somatic methylation and inactivation of MSH2 in families with Lynch syndrome due to deletion of the 3′ exons of TACSTD1. Nat Genet. 2009;41:112–117.PubMedGoogle Scholar
  21. 21.
    Lindor NM, Petersen GM, Hadley DW, et al. Recommendations for the care of individuals with an inherited predisposition to Lynch syndrome: a systematic review. JAMA. 2006;296:1507–1517.PubMedGoogle Scholar
  22. 22.
    Kastrinos F, Steyerberg EW, Mercado R, et al. The PREMM(1,2,6) model predicts risk of MLH1, MSH2, and MSH6 germline mutations based on cancer history. Gastroenterology. 2011;140:73–81.PubMedCentralPubMedGoogle Scholar
  23. 23.
    Chen S, Wang W, Lee S, et al. Prediction of germline mutations and cancer risk in the Lynch syndrome. JAMA. 2006;296:1479–1487.PubMedCentralPubMedGoogle Scholar
  24. 24.
    Dinh TA, Rosner BI, Atwood JC, et al. Health benefits and cost-effectiveness of primary genetic screening for Lynch syndrome in the general population. Cancer Prev Res (Phila). 2011;4:9–22.PubMedCentralGoogle Scholar
  25. 25.
    Resnick K, Straughn JM Jr, Backes F, et al. Lynch syndrome screening strategies among newly diagnosed endometrial cancer patients. Obstet Gynecol. 2009;114:530–536.PubMedGoogle Scholar
  26. 26.
    Backes FJ, Leon ME, Ivanov I, et al. Prospective evaluation of DNA mismatch repair protein expression in primary endometrial cancer. Gynecol Oncol. 2009;114:486–490.PubMedGoogle Scholar
  27. 27.
    Backes FJ, Hampel H, Backes KA, et al. Are prediction models for Lynch syndrome valid for probands with endometrial cancer? Fam Cancer. 2009;8:483–487.PubMedGoogle Scholar
  28. 28.
    Rodriguez-Bigas MA, Boland CR, Hamilton SR, et al. A National Cancer Institute workshop on hereditary nonpolyposis colorectal cancer syndrome: meeting highlights and Bethesda guidelines. J Natl Cancer Inst. 1997;89:1758–1762.PubMedGoogle Scholar
  29. 29.
    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.PubMedCentralPubMedGoogle Scholar
  30. 30.
    Ladabaum U, Wang G, Terdiman J, et al. Strategies to identify the Lynch syndrome among patients with colorectal cancer: a cost-effectiveness analysis. Ann Intern Med. 2011;155:69–79.PubMedCentralPubMedGoogle Scholar
  31. 31.
    Mange S, Bellcross C, Cragun D, et al. Creation of a network to promote universal screening for lynch syndrome: the lynch syndrome screening network. J Genet Couns. 2014 (in press).Google Scholar
  32. 32.
    Love RR, Morrissey JF. Colonoscopy in asymptomatic individuals with a family history of colorectal cancer. Arch Intern Med. 1984;144:2209–2211.PubMedGoogle Scholar
  33. 33.
    Mecklin JP, Jarvinen HJ, Aukee S, et al. Screening for colorectal carcinoma in cancer family syndrome kindreds. Scand J Gastroenterol. 1987;22:449–453.PubMedGoogle Scholar
  34. 34.
    Vasen HF, Taal BG, Nagengast FM, et al. Hereditary nonpolyposis colorectal cancer: results of long-term surveillance in 50 families. Eur J Cancer. 1995;31A:1145–1148.PubMedGoogle Scholar
  35. 35.
    Vasen HF, den Hartog JFC, Menko FH, et al. Screening for hereditary non-polyposis colorectal cancer: a study of 22 kindreds in The Netherlands. Am J Med. 1989;86:278–281.PubMedGoogle Scholar
  36. 36.
    Jarvinen HJ, Mecklin JP, Sistonen P. Screening reduces colorectal cancer rate in families with hereditary nonpolyposis colorectal cancer. Gastroenterology. 1995;108:1405–1411.PubMedGoogle Scholar
  37. 37.
    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.PubMedGoogle Scholar
  38. 38.
    Renkonen-Sinisalo L, Aarnio M, Mecklin JP, et al. Surveillance improves survival of colorectal cancer in patients with hereditary nonpolyposis colorectal cancer. Cancer Detect Prev. 2000;24:137–142.PubMedGoogle Scholar
  39. 39.
    Arrigoni A, Sprujevnik T, Alvisi V, et al. Clinical identification and long-term surveillance of 22 hereditary non-polyposis colon cancer Italian families. Eur J Gastroenterol Hepatol. 2005;17:213–219.PubMedGoogle Scholar
  40. 40.
    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.Google Scholar
  41. 41.
    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.PubMedCentralPubMedGoogle Scholar
  42. 42.
    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.PubMedGoogle Scholar
  43. 43.
    Burton-Chase AM, Hovick SR, Peterson SK, et al. Changes in screening behaviors and attitudes toward screening from pre-test genetic counseling to post-disclosure in Lynch syndrome families. Clin Genet. 2013;83:215–220.PubMedGoogle Scholar
  44. 44.
    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.PubMedGoogle Scholar
  45. 45.
    Hampel H, Stephens JA, Pukkala E, et al. Cancer risk in hereditary nonpolyposis colorectal cancer syndrome: later age of onset. Gastroenterology. 2005;129:415–421.PubMedGoogle Scholar
  46. 46.
    de Jong AE, Nagengast FM, Kleibeuker JH, et al. What is the appropriate screening protocol in Lynch syndrome? Fam Cancer. 2006;5:373–378.PubMedGoogle Scholar
  47. 47.
    Mecklin JP, Aarnio M, Laara E, et al. Development of colorectal tumors in colonoscopic surveillance in Lynch syndrome. Gastroenterology. 2007;133:1093–1098.PubMedGoogle Scholar
  48. 48.
    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.PubMedGoogle Scholar
  49. 49.
    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.PubMedGoogle Scholar
  50. 50.
    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.PubMedGoogle Scholar
  51. 51.
    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. Am J Gastroenterol. 2005;100:2167–2173.PubMedGoogle Scholar
  52. 52.
    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.PubMedGoogle Scholar
  53. 53.
    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.Google Scholar
  54. 54.
    Rijcken FE, Mourits MJ, Kleibeuker JH, et al. Gynecologic screening in hereditary nonpolyposis colorectal cancer. Gynecol Oncol. 2003;91:74–80.PubMedGoogle Scholar
  55. 55.
    Schmeler KM, Lynch HT, Chen LM, et al. Prophylactic surgery to reduce the risk of gynecologic cancers in the Lynch syndrome. N Engl J Med. 2006;354:261–269.PubMedGoogle Scholar
  56. 56.
    Kwon JS, Sun CC, Peterson SK, et al. Cost-effectiveness analysis of prevention strategies for gynecologic cancers in Lynch syndrome. Cancer. 2008;113:326–335.PubMedGoogle Scholar
  57. 57.
    Burn J, Bishop DT, Mecklin JP, et al. Effect of aspirin or resistant starch on colorectal neoplasia in the Lynch syndrome. N Engl J Med. 2008;359:2567–2578.PubMedGoogle Scholar
  58. 58.
    Burn J, Mathers JC, Bishop DT. Chemoprevention in Lynch syndrome. Fam Cancer. 2013;12:707–718.PubMedGoogle Scholar
  59. 59.
    Burt RW, Leppert MF, Slattery ML, et al. Genetic testing and phenotype in a large kindred with attenuated familial adenomatous polyposis. Gastroenterology. 2004;127:444–451.PubMedGoogle Scholar
  60. 60.
    Nielsen M, Hes FJ, Nagengast FM, et al. Germline mutations in APC and MUTYH are responsible for the majority of families with attenuated familial adenomatous polyposis. Clin Genet. 2007;71:427–433.PubMedGoogle Scholar
  61. 61.
    Grover S, Kastrinos F, Steyerberg EW, et al. Prevalence and phenotypes of APC and MUTYH mutations in patients with multiple colorectal adenomas. JAMA. 2012;308:485–492.PubMedCentralPubMedGoogle Scholar
  62. 62.
    Jasperson KW. Genetic testing by cancer site: colon (polyposis syndromes). Cancer J. 2012;18:328–333.PubMedGoogle Scholar
  63. 63.
    Nieuwenhuis MH, Vasen HF. Correlations between mutation site in APC and phenotype of familial adenomatous polyposis (FAP): a review of the literature. Crit Rev Oncol Hematol. 2007;61:153–161.PubMedGoogle Scholar
  64. 64.
    Sieber OM, Lipton L, Crabtree M, et al. Multiple colorectal adenomas, classic adenomatous polyposis, and germ-line mutations in MYH. N Engl J Med. 2003;348:791–799.PubMedGoogle Scholar
  65. 65.
    Alm T. Surgical treatment of hereditary adenomatosis of the colon and rectum in Sweden during the last 20 years. Part II. Patients with prophylactic operations, primary and late results. Discussion and summary. Acta Chir Scand. 1975;141:228–237.PubMedGoogle Scholar
  66. 66.
    Bulow S. Clinical features in familial polyposis coli. Results of the Danish Polyposis Register. Dis Colon Rectum. 1986;29:102–107.PubMedGoogle Scholar
  67. 67.
    Jarvinen HJ, Husa A, Aukee S, et al. Finnish registry for familial adenomatosis coli. Scand J Gastroenterol. 1984;19:941–946.PubMedGoogle Scholar
  68. 68.
    Vasen HF, Griffioen G, Offerhaus GJ, et al. The value of screening and central registration of families with familial adenomatous polyposis. A study of 82 families in The Netherlands. Dis Colon Rectum. 1990;33:227–230.PubMedGoogle Scholar
  69. 69.
    Rhodes M, Chapman PD, Burn J, et al. Role of a regional register for familial adenomatous polyposis: experience in the northern region. Br J Surg. 1991;78:451–452.PubMedGoogle Scholar
  70. 70.
    Morton DG, Macdonald F, Haydon J, et al. Screening practice for familial adenomatous polyposis: the potential for regional registers. Br J Surg. 1993;80:255–258.PubMedGoogle Scholar
  71. 71.
    Gibbons DC, Sinha A, Phillips RK, et al. Colorectal cancer: no longer the issue in familial adenomatous polyposis? Fam Cancer. 2011;10:11–20.PubMedGoogle Scholar
  72. 72.
    Mallinson EK, Newton KF, Bowen J, et al. The impact of screening and genetic registration on mortality and colorectal cancer incidence in familial adenomatous polyposis. Gut. 2010;59:1378–1382.PubMedGoogle Scholar
  73. 73.
    Bulow S. Results of national registration of familial adenomatous polyposis. Gut. 2003;52:742–746.PubMedCentralPubMedGoogle Scholar
  74. 74.
    Jarvinen HJ. Epidemiology of familial adenomatous polyposis in Finland: impact of family screening on the colorectal cancer rate and survival. Gut. 1992;33:357–360.PubMedCentralPubMedGoogle Scholar
  75. 75.
    Macrae FA, StJohn DJ, Muir EP, et al. Impact of a hospital-based register on the management of familial adenomatous polyposis. Med J Aust. 1989;151:552–557.PubMedGoogle Scholar
  76. 76.
    Gebert HF, Jagelman DG, McGannon E. Familial polyposis coli. Am Fam Physician. 1986;33:127–137.PubMedGoogle Scholar
  77. 77.
    Kinney AY, Hicken B, Simonsen SE, et al. Colorectal cancer surveillance behaviors among members of typical and attenuated FAP families. Am J Gastroenterol. 2007;102:153–162.PubMedGoogle Scholar
  78. 78.
    Heald RJ, Bussey HJ. Clinical experiences at St. Mark’s Hospital with multiple synchronous cancers of the colon and rectum. Dis Colon Rectum. 1975;18:6–10.PubMedGoogle Scholar
  79. 79.
    Ruttenberg D, Elliot MS, Bolding E. Severe colonic dysplasia in a child with familial adenomatous polyposis. Int J Colorectal Dis. 1991;6:169–170.PubMedGoogle Scholar
  80. 80.
    Jerkic S, Rosewich H, Scharf JG, et al. Colorectal cancer in two pre-teenage siblings with familial adenomatous polyposis. Eur J Pediatr. 2005;164:306–310.PubMedGoogle Scholar
  81. 81.
    Boskovic A, Djuricic S, Grujic B, et al. Early onset of dysplasia in polyps in children with familial adenomatous polyposis: case report and literature review. Arab J Gastroenterol. 2014;15:88–90.PubMedGoogle Scholar
  82. 82.
    Cruz-Correa M, Hylind LM, Romans KE, et al. Long-term treatment with sulindac in familial adenomatous polyposis: a prospective cohort study. Gastroenterology. 2002;122:641–645.PubMedGoogle Scholar
  83. 83.
    Giardiello FM, Hamilton SR, Krush AJ, et al. Treatment of colonic and rectal adenomas with sulindac in familial adenomatous polyposis. N Engl J Med. 1993;328:1313–1316.PubMedGoogle Scholar
  84. 84.
    Giardiello FM, Yang VW, Hylind LM, et al. Primary chemoprevention of familial adenomatous polyposis with sulindac. N Engl J Med. 2002;346:1054–1059.PubMedCentralPubMedGoogle Scholar
  85. 85.
    Aziz O, Athanasiou T, Fazio VW, et al. Meta-analysis of observational studies of ileorectal versus ileal pouch-anal anastomosis for familial adenomatous polyposis. Br J Surg. 2006;93:407–417.PubMedGoogle Scholar
  86. 86.
    Gismondi V, Meta M, Bonelli L, et al. Prevalence of the Y165C, G382D and 1395delGGA germline mutations of the MYH gene in Italian patients with adenomatous polyposis coli and colorectal adenomas. Int J Cancer. 2004;109:680–684.PubMedGoogle Scholar
  87. 87.
    Nielsen M, Franken PF, Reinards TH, et al. Multiplicity in polyp count and extracolonic manifestations in 40 Dutch patients with MYH associated polyposis coli (MAP). J Med Genet. 2005;42:e54.PubMedCentralPubMedGoogle Scholar
  88. 88.
    Lubbe SJ, Di Bernardo MC, Chandler IP, et al. Clinical implications of the colorectal cancer risk associated with MUTYH mutation. J Clin Oncol. 2009;27:3975–3980.PubMedGoogle Scholar
  89. 89.
    Cleary SP, Cotterchio M, Jenkins MA, et al. Germline MutY human homologue mutations and colorectal cancer: a multisite case–control study. Gastroenterology. 2009;136:1251–1260.PubMedCentralPubMedGoogle Scholar
  90. 90.
    Boparai KS, Dekker E, Van Eeden S, et al. Hyperplastic polyps and sessile serrated adenomas as a phenotypic expression of MYH-associated polyposis. Gastroenterology. 2008;135:2014–2018.PubMedGoogle Scholar
  91. 91.
    Jenkins MA, Croitoru ME, Monga N, et al. Risk of colorectal cancer in monoallelic and biallelic carriers of MYH mutations: a population-based case-family study. Cancer Epidemiol Biomark Prev. 2006;15:312–314.Google Scholar
  92. 92.
    Theodoratou E, Campbell H, Tenesa A, et al. A large-scale meta-analysis to refine colorectal cancer risk estimates associated with MUTYH variants. Br J Cancer. 2010;103:1875–1884.PubMedCentralPubMedGoogle Scholar
  93. 93.
    Balaguer F, Castellvi-Bel S, Castells A, et al. Identification of MYH mutation carriers in colorectal cancer: a multicenter, case–control, population-based study. Clin Gastroenterol Hepatol. 2007;5:379–387.PubMedGoogle Scholar
  94. 94.
    Burt RW, Cannon JA, David DS, et al. National Comprehensive cancer network. J Natl Compr Cancer Netw. 2013;11:1538–1575.Google Scholar
  95. 95.
    Guarinos C, Juarez M, Egoavil C, et al. Prevalence and characteristics of MUTYH-associated polyposis in patients with multiple adenomatous and serrated polyps. Clin Cancer Res. 2014;20:1158–1168.PubMedGoogle Scholar
  96. 96.
    Aretz S, Uhlhaas S, Goergens H, et al. MUTYH-associated polyposis: 70 of 71 patients with biallelic mutations present with an attenuated or atypical phenotype. Int J Cancer. 2006;119:807–814.PubMedGoogle Scholar
  97. 97.
    Nielsen M, Poley JW, Verhoef S, et al. Duodenal carcinoma in MUTYH-associated polyposis. J Clin Pathol. 2006;59:1212–1215.PubMedCentralPubMedGoogle Scholar
  98. 98.
    Giardiello FM, Trimbath JD. Peutz–Jeghers syndrome and management recommendations. Clin Gastroenterol Hepatol. 2006;4:408–415.PubMedGoogle Scholar
  99. 99.
    van Lier MG, Wagner A, Mathus-Vliegen EM, et al. High cancer risk in Peutz–Jeghers syndrome: a systematic review and surveillance recommendations. Am J Gastroenterol. 2010;105:1258–1264; author reply 1265.Google Scholar
  100. 100.
    Brosens LA, van Hattem A, Hylind LM, et al. Risk of colorectal cancer in juvenile polyposis. Gut. 2007;56:965–967.PubMedCentralPubMedGoogle Scholar
  101. 101.
    Howe JR, Mitros FA, Summers RW. The risk of gastrointestinal carcinoma in familial juvenile polyposis. Ann Surg Oncol. 1998;5:751–756.PubMedGoogle Scholar
  102. 102.
    O’Malley M, LaGuardia L, Kalady MF, et al. The prevalence of hereditary hemorrhagic telangiectasia in juvenile polyposis syndrome. Dis Colon Rectum. 2012;55:886–892.PubMedGoogle Scholar
  103. 103.
    Volikos E, Robinson J, Aittomaki K, et al. LKB1 exonic and whole gene deletions are a common cause of Peutz–Jeghers syndrome. J Med Genet. 2006;43:e18.PubMedCentralPubMedGoogle Scholar
  104. 104.
    Sweet K, Willis J, Zhou XP, et al. Molecular classification of patients with unexplained hamartomatous and hyperplastic polyposis. JAMA. 2005;294:2465–2473.PubMedGoogle Scholar
  105. 105.
    Giardiello FM, Brensinger JD, Tersmette AC, et al. Very high risk of cancer in familial Peutz–Jeghers syndrome. Gastroenterology. 2000;119:1447–1453.PubMedGoogle Scholar
  106. 106.
    Hearle N, Schumacher V, Menko FH, et al. Frequency and spectrum of cancers in the Peutz–Jeghers syndrome. Clin Cancer Res. 2006;12:3209–3215.PubMedGoogle Scholar
  107. 107.
    Latchford AR, Neale K, Phillips RK, et al. Peutz–Jeghers syndrome: intriguing suggestion of gastrointestinal cancer prevention from surveillance. Dis Colon Rectum. 2011;54:1547–1551.PubMedGoogle Scholar
  108. 108.
    Dunlop MG. Guidance on gastrointestinal surveillance for hereditary non-polyposis colorectal cancer, familial adenomatous polypolis, juvenile polyposis, and Peutz–Jeghers syndrome. Gut. 2002;51:V21–V27.PubMedCentralPubMedGoogle Scholar
  109. 109.
    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.PubMedGoogle Scholar
  110. 110.
    Burt RW, Bishop DT, Cannon LA, et al. Dominant inheritance of adenomatous colonic polyps and colorectal cancer. N Engl J Med. 1985;312:1540–1544.PubMedGoogle Scholar
  111. 111.
    Cannon-Albright LA, Skolnick MH, Bishop DT, et al. Common inheritance of susceptibility to colonic adenomatous polyps and associated colorectal cancers. N Engl J Med. 1988;319:533–537.PubMedGoogle Scholar
  112. 112.
    Leppert M, Burt R, Hughes JP, et al. Genetic analysis of an inherited predisposition to colon cancer in a family with a variable number of adenomatous polyps. N Engl J Med. 1990;322:904–908.PubMedGoogle Scholar
  113. 113.
    Samadder NJ, Curtin K, Wong J, et al. Epidemiology and familial risk of synchronous and metachronous colorectal cancer: a population-based study in Utah. Clin Gastroenterol Hepatol. 2014;12(12):2078–2084.Google Scholar
  114. 114.
    Tuohy TM, Rowe KG, Mineau GP, et al. Risk of colorectal cancer and adenomas in the families of patients with adenomas: a population-based study in Utah. Cancer. 2014;120:35–42.PubMedGoogle Scholar
  115. 115.
    Taylor DP, Burt RW, Williams MS, et al. Population-based family history-specific risks for colorectal cancer: a constellation approach. Gastroenterology. 2010;138:877–885.PubMedCentralPubMedGoogle Scholar
  116. 116.
    Hemminki K, Li X. Familial colorectal adenocarcinoma from the Swedish Family-Cancer Database. Int J Cancer. 2001;94:743–748.PubMedGoogle Scholar
  117. 117.
    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.PubMedGoogle Scholar
  118. 118.
    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.PubMedGoogle Scholar
  119. 119.
    Gray-McGuire C, Guda K, Adrianto I, et al. Confirmation of linkage to and localization of familial colon cancer risk haplotype on chromosome 9q22. Cancer Res. 2010;70:5409–5418.PubMedCentralPubMedGoogle Scholar
  120. 120.
    Tenesa A, Dunlop MG. New insights into the aetiology of colorectal cancer from genome-wide association studies. Nat Rev Genet. 2009;10:353–358.PubMedGoogle Scholar
  121. 121.
    Kastrinos F, Allen JI, Stockwell DH, et al. Development and validation of a colon cancer risk assessment tool for patients undergoing colonoscopy. Am J Gastroenterol. 2009;104:1508–1518.PubMedCentralPubMedGoogle Scholar
  122. 122.
    Rex DK, Johnson DA, Anderson JC, et al. American College of Gastroenterology guidelines for colorectal cancer screening 2009 [corrected]. Am J Gastroenterol. 2009;104:739–750.PubMedGoogle Scholar
  123. 123.
    Levin B, Lieberman DA, 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.PubMedGoogle Scholar
  124. 124.
    Qaseem A, Denberg TD, Hopkins RH Jr, et al. Screening for colorectal cancer: a guidance statement from the American College of Physicians. Ann Intern Med. 2012;156:378–386.PubMedGoogle Scholar
  125. 125.
    Burt RW, Barthel JS, Dunn KB, et al. NCCN clinical practice guidelines in oncology. Colorectal cancer screening. J Natl Compr Cancer Netw. 2010;8:8–61.Google Scholar
  126. 126.
    Ahnen DJ, Bray TH, Cannon JA, et al. Colorectal Cancer Screening: NCCN Clinical Practice Guidelines in Oncology (NCCN Guidelines). 2014.Google Scholar
  127. 127.
    Atkin WS, Edwards R, Kralj-Hans I, et al. Once-only flexible sigmoidoscopy screening in prevention of colorectal cancer: a multicentre randomised controlled trial. Lancet. 2010;375:1624–1633.PubMedGoogle Scholar
  128. 128.
    Winawer SJ, Flehinger BJ, Schottenfeld D, et al. Screening for colorectal cancer with fecal occult blood testing and sigmoidoscopy. J Natl Cancer Inst. 1993;85:1311–1318.PubMedGoogle Scholar
  129. 129.
    Mandel JS, Bond JH, Church TR, 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.PubMedGoogle Scholar
  130. 130.
    Baxter NN, Goldwasser MA, Paszat LF, et al. Association of colonoscopy and death from colorectal cancer. Ann Intern Med. 2009;150:1–8.PubMedGoogle Scholar
  131. 131.
    Singh H, Nugent Z, Demers AA, et al. The reduction in colorectal cancer mortality after colonoscopy varies by site of the cancer. Gastroenterology. 2010;139:1128–1137.PubMedGoogle Scholar
  132. 132.
    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.PubMedGoogle Scholar
  133. 133.
    Kahi CJ, Myers LJ, Slaven JE, et al. Lower endoscopy reduces colorectal cancer incidence in older individuals. Gastroenterology. 2014;146:718 e3–725 e3.Google Scholar
  134. 134.
    Samadder NJ, Curtin K, Tuohy TM, et al. Increased risk of colorectal neoplasia among family members of patients with colorectal cancer: a population-based study in Utah. Gastroenterology. 2014;147(4):814–821.Google Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • N. Jewel Samadder
    • 1
    • 2
  • Kory Jasperson
    • 1
    • 4
  • Randall W. Burt
    • 1
    • 2
    • 3
  1. 1.High Risk GI Cancers Program, Huntsman Cancer InstituteUniversity of UtahSalt Lake CityUSA
  2. 2.Departments of Medicine (Gastroenterology)University of UtahSalt Lake CityUSA
  3. 3.Departments of Oncological SciencesUniversity of UtahSalt Lake CityUSA
  4. 4.Genetic Counseling ResourceHuntsman Cancer InstituteSalt Lake CityUSA

Personalised recommendations