Advertisement

The Colon Cancer Family Registry Cohort

  • Mark A. Jenkins
  • Aung K. Win
  • Noralane M. Lindor
Chapter

Abstract

The Colon Cancer Family Registry Cohort (CCFRC) was established in 1997 for NIH stated purposes of research on the genetic and environmental aetiology of colorectal cancer and the identification of individuals who, because of their high risk, could benefit from preventive strategies. A case-control-family design was utilised to enhance genetic as well as environmental research, including gene discovery and characterisation, and to evaluate modifiers of genetic risk. The 42,489 study participants from 15,049 families were recruited between 1998 and 2012 in the USA, Canada, Australia and New Zealand including recently diagnosed colorectal cancer cases from population-based cancer registries, controls from population-based sources, patients from family cancer clinics with a strong family history of colorectal cancer or young-onset disease and their relatives, both those affected and those unaffected by cancer. At baseline, participants provided a blood/buccal wash sample and access to medical records and tumour specimens and completed a detailed risk factor questionnaire (height, weight, alcohol use, smoking, physical activity, medication use, diet, screening, cancer diagnoses, detailed family history of cancer). Every 4–5 years after baseline, all population-based case-families and clinic-based families were followed up for updates on their personal and family history of cancer as well as history of surgery, cancer screening and some risk factors. The total follow-up of 37,436 participants covers 339,000 person-years (277,000 via direct survey of participants and 62,000 via interview of participating relatives). During follow-up, 824 (2.2%) participants were diagnosed with a colorectal cancer and 3582 (9.5%) were diagnosed with a non-colorectal cancer. Participants have had germline testing for major colorectal cancer genetic syndromes (Lynch syndrome and MUTYH) and undergone genome-wide SNP genotyping. Colorectal cancer cases were tested for major somatic alterations, for clinically relevant molecular subtypes, including tumour microsatellite instability, mismatch repair protein loss in immunohistochemistry, the common somatic KRAS and BRAF variants, MLH1 methylation and CpG island methylator phenotype (CIMP). Data and biospecimens are available for collaborative research and have been utilised for over 400 publications and approximately 300 projects (53% are external investigator-driven projects) – see http://www.coloncfr.org/.

Keywords

Colorectal cancer Family study Lynch syndrome Risk factors Cohort Family history 

Notes

Acknowledgements

This work was supported by grant UM1 CA167551 from the National Cancer Institute and through cooperative agreements with the following CCFRC sites: Australasian Colorectal Cancer Family Registry (U01 CA074778 and U01/U24 CA097735), Mayo Clinic Cooperative Family Registry for Colon Cancer Studies (U01/U24 CA074800), Ontario Familial Colorectal Cancer Registry (U01/U24 CA074783), Seattle Colorectal Cancer Family Registry (U01/U24 CA074794), University of Hawaii Colorectal Cancer Family Registry (U01/U24 CA074806) and USC Consortium Colorectal Cancer Family Registry (U01/U24 CA074799). The targeted minority recruitment was supported by grant R01 CA104132. The genome-wide association studies (GWAS) were supported by grants U01 CA 122839, R01 CA143237 and U19 CA148107. The CIMP and KRAS mutation testing was supported by R01 CA118699.

Additional support for case ascertainment was provided from the Surveillance, Epidemiology, and End Results (SEER) Program of the National Cancer Institute to Fred Hutchinson Cancer Research Center (Control Nos. N01-CN-67009 and N01-PC-35142 and Contract No. HHSN2612013000121), the Hawaii Department of Health (Control Nos. N01-PC-67001 and N01-PC-35137 and Contract No. HHSN26120100037C) and the California Department of Public Health (contracts HHSN261201000035C awarded to the University of Southern California and HHSN261201000140C awarded to the Cancer Prevention Institute of California), by the following US state cancer registries, AZ, CO, MN, NC, and NH, and by the Victorian Cancer Registry, Australia and the Ontario Cancer Registry, Canada. AKW is an Australian National Health and Medical Research Council (NHMRC) Early Career Fellow. MAJ is an NHMRC Senior Research Fellow.

References

  1. 1.
    Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015;136(5):E359–86.  https://doi.org/10.1002/ijc.29210.CrossRefPubMedGoogle Scholar
  2. 2.
    Newcomb PA, Baron J, Cotterchio M, Gallinger S, Grove J, Haile R, et al. Colon Cancer Family Registry: an international resource for studies of the genetic epidemiology of colon cancer. Cancer Epidemiol Biomark Prev. 2007;16(11):2331–43.  https://doi.org/10.1158/1055-9965.epi-07-0648.CrossRefGoogle Scholar
  3. 3.
    Kolonel LN, Henderson BE, Hankin JH, Nomura AM, Wilkens LR, Pike MC, et al. A multiethnic cohort in Hawaii and Los Angeles: baseline characteristics. Am J Epidemiol. 2000;151(4):346–57.CrossRefGoogle Scholar
  4. 4.
    Ireland P, Jolley D, Giles G, O’Dea K, Powles J, Rutishauser I, et al. Development of the Melbourne FFQ: a food frequency questionnaire for use in an Australian prospective study involving an ethnically diverse cohort. Asia Pac J Clin Nutr. 1994;3(1):19–31.PubMedGoogle Scholar
  5. 5.
    Lum A, Le Marchand L. A simple mouthwash method for obtaining genomic DNA in molecular epidemiological studies. Cancer Epidemiol Biomark Prev. 1998;7(8):719–24.Google Scholar
  6. 6.
    Miller G. Immortalization of human lymphocytes by Epstein-Barr virus. Yale J Biol Med. 1982;55(3–4):305–10.PubMedPubMedCentralGoogle Scholar
  7. 7.
    Lindor NM, Burgart LJ, Leontovich O, Goldberg RM, Cunningham JM, Sargent DJ, et al. Immunohistochemistry versus microsatellite instability testing in phenotyping colorectal tumors. J Clin Oncol. 2002;20(4):1043–8.  https://doi.org/10.1200/jco.20.4.1043.CrossRefPubMedGoogle Scholar
  8. 8.
    Buchanan DD, Sweet K, Drini M, Jenkins MA, Win AK, English DR, et al. Risk factors for colorectal cancer in patients with multiple serrated polyps: a cross-sectional case series from genetics clinics. PLoS One. 2010;5(7):e11636. https://doi.org/10.1371/journal.pone.0011636CrossRefGoogle Scholar
  9. 9.
    Buchanan DD, Win AK, Walsh MD, Walters RJ, Clendenning M, Nagler BN, et al. Family history of colorectal cancer in BRAF p.V600E mutated colorectal cancer cases. Cancer Epidemiol Biomark Prev. 2013;22(5):917–26.  https://doi.org/10.1158/1055-9965.epi-12-1211.CrossRefGoogle Scholar
  10. 10.
    Weisenberger DJ, Levine AJ, Long TI, Buchanan DD, Walters R, Clendenning M, et al. Association of the colorectal CpG island methylator phenotype with molecular features, risk factors, and family history. Cancer Epidemiol Biomark Prev. 2015;24(3):512–9.  https://doi.org/10.1158/1055-9965.EPI-14-1161.CrossRefGoogle Scholar
  11. 11.
    Levine AJ, Win AK, Buchanan DD, Jenkins MA, Baron JA, Young JP, et al. Cancer risks for the relatives of colorectal cancer cases with a methylated MLH1 promoter region: data from the Colorectal Cancer Family Registry. Cancer Prev Res. 2012;5(2):328–35.  https://doi.org/10.1158/1940-6207.CAPR-11-0419.CrossRefGoogle Scholar
  12. 12.
    Lindor NM, Rabe K, Petersen GM, Haile R, Casey G, Baron J, et al. Lower cancer incidence in Amsterdam-I criteria families without mismatch repair deficiency: familial colorectal cancer type X. JAMA. 2005;293(16):1979–85.  https://doi.org/10.1001/jama.293.16.1979.CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    The 1000 Genomes Project Consortium. An integrated map of genetic variation from 1,092 human genomes. Nature. 2012;491(7422):56–65.  https://doi.org/10.1038/nature11632.CrossRefPubMedCentralGoogle Scholar
  14. 14.
    Dowty JG, Win AK, Buchanan DD, Lindor NM, Macrae FA, Clendenning M, et al. Cancer risks for MLH1 and MSH2 mutation carriers. Hum Mutat. 2013;34(3):490–7.  https://doi.org/10.1002/humu.22262.CrossRefGoogle Scholar
  15. 15.
    Baglietto L, Lindor NM, Dowty JG, White DM, Wagner A, Gomez Garcia EB, et al. Risks of Lynch syndrome cancers for MSH6 mutation carriers. J Natl Cancer Inst. 2010;102(3):193–201.  https://doi.org/10.1093/jnci/djp473.CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Senter L, Clendenning M, Sotamaa K, Hampel H, Green J, Potter JD, et al. The clinical phenotype of Lynch syndrome due to germ-line PMS2 mutations. Gastroenterology. 2008;135(2):419–28.  https://doi.org/10.1053/j.gastro.2008.04.026.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Win AK, Young JP, Lindor NM, Tucker KM, Ahnen DJ, Young GP, et al. Colorectal and other cancer risks for carriers and noncarriers from families with a DNA mismatch repair gene mutation: a prospective cohort study. J Clin Oncol. 2012;30(9):958–64.  https://doi.org/10.1200/jco.2011.39.5590.CrossRefGoogle Scholar
  18. 18.
    Guindalini RS, Win AK, Gulden C, Lindor NM, Newcomb PA, Haile RW, et al. Mutation spectrum and risk of colorectal cancer in African American families with Lynch syndrome. Gastroenterology. 2015;149(6):1446–53.  https://doi.org/10.1053/j.gastro.2015.07.052.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Parry S, Win AK, Parry B, Macrae FA, Gurrin LC, Church JM, et al. Metachronous colorectal cancer risk for mismatch repair gene mutation carriers: the advantage of more extensive colon surgery. Gut. 2011;60(7):950–7.  https://doi.org/10.1136/gut.2010.228056.CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Win AK, Parry S, Parry B, Kalady MF, Macrae FA, Ahnen DJ, et al. Risk of metachronous colon cancer following surgery for rectal cancer in mismatch repair gene mutation carriers. Ann Surg Oncol. 2013;20(6):1829–36.  https://doi.org/10.1245/s10434-012-2858-5.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Win AK, Lindor NM, Young JP, Macrae FA, Young GP, Williamson E, et al. Risks of primary extracolonic cancers following colorectal cancer in Lynch syndrome. J Natl Cancer Inst. 2012;104(18):1363–72.  https://doi.org/10.1093/jnci/djs351.CrossRefGoogle Scholar
  22. 22.
    Obermair A, Youlden DR, Young JP, Lindor NM, Baron JA, Newcomb P, et al. Risk of endometrial cancer for women diagnosed with HNPCC-related colorectal carcinoma. Int J Cancer. 2010;127(11):2678–84.  https://doi.org/10.1002/ijc.25501.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Win AK, Lindor NM, Winship I, Tucker KM, Buchanan DD, Young JP, et al. Risks of colorectal and other cancers after endometrial cancer for women with Lynch syndrome. J Natl Cancer Inst. 2013;105(4):274–9.  https://doi.org/10.1093/jnci/djs525.CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Heath JA, Reece JC, Buchanan DD, Casey G, Durno CA, Gallinger S, et al. Childhood cancers in families with and without Lynch syndrome. Fam Cancer. 2015;14(4):545–51.  https://doi.org/10.1007/s10689-015-9810-3.CrossRefGoogle Scholar
  25. 25.
    Win AK, Dowty JG, Antill YC, English DR, Baron JA, Young JP, et al. Body mass index in early adulthood and endometrial cancer risk for mismatch repair gene mutation carriers. Obstet Gynecol. 2011;117(4):899–905.  https://doi.org/10.1097/AOG.0b013e3182110ea3.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Win AK, Dowty JG, English DR, Campbell PT, Young JP, Winship I, et al. Body mass index in early adulthood and colorectal cancer risk for carriers and non-carriers of germline mutations in DNA mismatch repair genes. Br J Cancer. 2011;105(1):162–9.  https://doi.org/10.1038/bjc.2011.172.CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Pande M, Lynch PM, Hopper JL, Jenkins MA, Gallinger S, Haile RW, et al. Smoking and colorectal cancer in Lynch syndrome: results from the Colon Cancer Family Registry and the University of Texas M.D. Anderson Cancer Center. Clin Cancer Res. 2010;16(4):1331–9.  https://doi.org/10.1158/1078-0432.ccr-09-1877.CrossRefGoogle Scholar
  28. 28.
    Dashti SG, Buchanan DD, Jayasekara H, Ait Ouakrim D, Clendenning M, Rosty C, et al. Alcohol consumption and the risk of colorectal cancer for mismatch repair gene mutation carriers. Cancer Epidemiol Biomark Prev. 2017;26(3):366–75.  https://doi.org/10.1158/1055-9965.epi-16-0496.CrossRefGoogle Scholar
  29. 29.
    Ait Ouakrim D, Dashti SG, Chau R, Buchanan DD, Clendenning M, Rosty C, et al. Aspirin, ibuprofen, and the risk of colorectal cancer in Lynch syndrome. J Natl Cancer Inst. 2015;107(9).  https://doi.org/10.1093/jnci/djv170.CrossRefGoogle Scholar
  30. 30.
    Chau R, Dashti SG, Ait Ouakrim D, Buchanan DD, Clendenning M, Rosty C, et al. Multivitamin, calcium and folic acid supplements and the risk of colorectal cancer in Lynch syndrome. Int J Epidemiol. 2016;45(3):940–53.  https://doi.org/10.1093/ije/dyw036.CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Dashti SG, Chau R, Ouakrim DA, Buchanan DD, Clendenning M, Young JP, et al. Female hormonal factors and the risk of endometrial cancer in Lynch syndrome. JAMA. 2015;314(1):61–71.  https://doi.org/10.1001/jama.2015.6789.CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Win AK, Clendenning M, Crawford W, Rosty C, Preston SG, Southey MC, et al. Genetic variants within the hTERT gene and the risk of colorectal cancer in Lynch syndrome. Genes Cancer. 2015;6(11–12):445–51.  https://doi.org/10.18632/genesandcancer.85.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Win AK, Reece JC, Buchanan DD, Clendenning M, Young JP, Cleary SP, et al. Risk of colorectal cancer for people with a mutation in both a MUTYH and a DNA mismatch repair gene. Fam Cancer. 2015;14(4):575–83.  https://doi.org/10.1007/s10689-015-9824-x.CrossRefGoogle Scholar
  34. 34.
    Win AK, Hopper JL, Buchanan DD, Young JP, Tenesa A, Dowty JG, et al. Are the common genetic variants associated with colorectal cancer risk for DNA mismatch repair gene mutation carriers? Eur J Cancer. 2013;49(7):1578–87.  https://doi.org/10.1016/j.ejca.2013.01.029.CrossRefGoogle Scholar
  35. 35.
    Stupart D, Win AK, Jenkins M, Winship IM, Goldberg P, Ramesar R. Fertility and apparent genetic anticipation in Lynch syndrome. Fam Cancer. 2014;13(3):369–74.  https://doi.org/10.1007/s10689-014-9714-7.CrossRefGoogle Scholar
  36. 36.
    Stupart D, Win AK, Winship IM, Jenkins M. Fertility after young-onset colorectal cancer: a study of subjects with Lynch syndrome. Colorectal Dis. 2015;17(9):787–93.  https://doi.org/10.1111/codi.12940.CrossRefGoogle Scholar
  37. 37.
    Shiovitz S, Copeland WK, Passarelli MN, Burnett-Hartman AN, Grady WM, Potter JD, et al. Characterisation of familial colorectal cancer Type X, Lynch syndrome, and non-familial colorectal cancer. Br J Cancer. 2014;111(3):598–602.  https://doi.org/10.1038/bjc.2014.309.CrossRefGoogle Scholar
  38. 38.
    Walsh MD, Cummings MC, Pearson SA, Clendenning M, Walters RJ, Nagler B, et al. Lynch syndrome-associated breast cancers do not overexpress chromosome 11-encoded mucins. Modern Pathol. 2013;26(7):944–54.  https://doi.org/10.1038/modpathol.2012.232.CrossRefGoogle Scholar
  39. 39.
    Antill YC, Dowty JG, Win AK, Thompson T, Walsh MD, Cummings MC, et al. Lynch syndrome and cervical cancer. Int J Cancer. 2015;137(11):2757–61.  https://doi.org/10.1002/ijc.29641.CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Rosty C, Walsh MD, Lindor NM, Thibodeau SN, Mundt E, Gallinger S, et al. High prevalence of mismatch repair deficiency in prostate cancers diagnosed in mismatch repair gene mutation carriers from the Colon Cancer Family Registry. Fam Cancer. 2014;13(4):573–82.  https://doi.org/10.1007/s10689-014-9744-1.CrossRefGoogle Scholar
  41. 41.
    Toon CW, Walsh MD, Chou A, Capper D, Clarkson A, Sioson L, et al. BRAFV600E immunohistochemistry facilitates universal screening of colorectal cancers for Lynch syndrome. Am J Surg Pathol. 2013;37(10):1592–602.  https://doi.org/10.1097/PAS.0b013e31828f233d.CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Newton K, Jorgensen NM, Wallace AJ, Buchanan DD, Lalloo F, RF MM, et al. Tumour MLH1 promoter region methylation testing is an effective prescreen for Lynch Syndrome (HNPCC). J Med Genet. 2014;51(12):789–96.  https://doi.org/10.1136/jmedgenet-2014-102552.CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Tomsic J, Senter L, Liyanarachchi S, Clendenning M, Vaughn CP, Jenkins MA, et al. Recurrent and founder mutations in the PMS2 gene. Clin Genet. 2013;83(3):238–43.  https://doi.org/10.1111/j.1399-0004.2012.01898.x.CrossRefPubMedGoogle Scholar
  44. 44.
    Win AK, Jenkins MA, Buchanan DD, Clendenning M, Young JP, Giles GG, et al. Determining the frequency of de novo germline mutations in DNA mismatch repair genes. J Med Genet. 2011;48(8):530–4.  https://doi.org/10.1136/jmedgenet-2011-100082.CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Thompson BA, Spurdle AB, Plazzer JP, Greenblatt MS, Akagi K, Al-Mulla F, et al. Application of a 5-tiered scheme for standardized classification of 2,360 unique mismatch repair gene variants in the InSiGHT locus-specific database. Nat Genet. 2014;46(2):107–15.  https://doi.org/10.1038/ng.2854.CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Thompson BA, Greenblatt MS, Vallee MP, Herkert JC, Tessereau C, Young EL, et al. Calibration of multiple in silico tools for predicting pathogenicity of mismatch repair gene missense substitutions. Hum Mutat. 2013;34(1):255–65.  https://doi.org/10.1002/humu.22214.CrossRefPubMedGoogle Scholar
  47. 47.
    Thompson BA, Goldgar DE, Paterson C, Clendenning M, Walters R, Arnold S, et al. A multifactorial likelihood model for MMR gene variant classification incorporating probabilities based on sequence bioinformatics and tumor characteristics: a report from the Colon Cancer Family Registry. Hum Mutat. 2013;34(1):200–9.  https://doi.org/10.1002/humu.22213.CrossRefGoogle Scholar
  48. 48.
    Win AK, Jenkins MA, Dowty JG, Antoniou AC, Lee A, Giles GG, et al. Prevalence and penetrance of major genes and polygenes for colorectal cancer. Cancer Epidemiol Biomarkers Prev. 2017;26(3):404–12.  https://doi.org/10.1158/1055-9965.epi-16-0693.CrossRefPubMedGoogle Scholar
  49. 49.
    Win AK, Dowty JG, Cleary SP, Kim H, Buchanan DD, Young JP, et al. Risk of colorectal cancer for carriers of mutations in MUTYH, with and without a family history of cancer. Gastroenterology. 2014;146(5):1208–11. e1-5.  https://doi.org/10.1053/j.gastro.2014.01.022.CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Jenkins MA, Croitoru ME, Monga N, Cleary SP, Cotterchio M, Hopper JL, 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(2):312–4.  https://doi.org/10.1158/1055-9965.epi-05-0793.CrossRefGoogle Scholar
  51. 51.
    Win AK, Reece JC, Dowty JG, Buchanan DD, Clendenning M, Rosty C, et al. Risk of extracolonic cancers for people with biallelic and monoallelic mutations in MUTYH. Int J Cancer. 2016;139(7):1557–63.  https://doi.org/10.1002/ijc.30197.CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Win AK, Cleary SP, Dowty JG, Baron JA, Young JP, Buchanan DD, et al. Cancer risks for monoallelic MUTYH mutation carriers with a family history of colorectal cancer. Int J Cancer. 2011;129(9):2256–62.  https://doi.org/10.1002/ijc.25870.CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Phipps AI, Lindor NM, Jenkins MA, Baron JA, Win AK, Gallinger S, et al. Colon and rectal cancer survival by tumor location and microsatellite instability: the Colon Cancer Family Registry. Dis Colon Rectum. 2013;56(8):937–44.  https://doi.org/10.1097/DCR.0b013e31828f9a57.CrossRefGoogle Scholar
  54. 54.
    Lynch PM. Colorectal cancer survival by location and microsatellite status: data from the Colon Cancer Family Registries and their implications. Dis Colon Rectum. 2013;56(8):935–6.  https://doi.org/10.1097/DCR.0b013e31828f9954.CrossRefGoogle Scholar
  55. 55.
    Phipps AI, Buchanan DD, Makar KW, Burnett-Hartman AN, Coghill AE, Passarelli MN, et al. BRAF mutation status and survival after colorectal cancer diagnosis according to patient and tumor characteristics. Cancer Epidemiol Biomark Prev. 2012;21(10):1792–8.  https://doi.org/10.1158/1055-9965.epi-12-0674.CrossRefGoogle Scholar
  56. 56.
    Levine AJ, Phipps AI, Baron JA, Buchanan DD, Ahnen DJ, Cohen SA, et al. Clinicopathologic risk factor distributions for MLH1 promoter region methylation in CIMP-positive tumors. Cancer Epidemiol Biomark Prev. 2016;25(1):68–75.  https://doi.org/10.1158/1055-9965.epi-15-0935.CrossRefGoogle Scholar
  57. 57.
    Phipps AI, Limburg PJ, Baron JA, Burnett-Hartman AN, Weisenberger DJ, Laird PW, et al. Association between molecular subtypes of colorectal cancer and patient survival. Gastroenterology. 2015;148(1):77–87. e2.  https://doi.org/10.1053/j.gastro.2014.09.038.CrossRefPubMedGoogle Scholar
  58. 58.
    Phipps AI, Buchanan DD, Makar KW, Win AK, Baron JA, Lindor NM, et al. KRAS-mutation status in relation to colorectal cancer survival: the joint impact of correlated tumour markers. Br J Cancer. 2013;108(8):1757–64.  https://doi.org/10.1038/bjc.2013.118.CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Phipps AI, Ahnen DJ, Cheng I, Newcomb PA, Win AK, Burnett T. PIK3CA somatic mutation status in relation to patient and tumor factors in racial/ethnic minorities with colorectal cancer. Cancer Epidemiol Biomark Prev. 2015;24(7):1046–51.  https://doi.org/10.1158/1055-9965.epi-15-0204.CrossRefGoogle Scholar
  60. 60.
    Loo LW, Tiirikainen M, Cheng I, Lum-Jones A, Seifried A, Church JM, et al. Integrated analysis of genome-wide copy number alterations and gene expression in microsatellite stable, CpG island methylator phenotype-negative colon cancer. Genes Chromosomes Cancer. 2013;52(5):450–66.  https://doi.org/10.1002/gcc.22043.CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Passarelli MN, Coghill AE, Hutter CM, Zheng Y, Makar KW, Potter JD, et al. Common colorectal cancer risk variants in SMAD7 are associated with survival among prediagnostic nonsteroidal anti-inflammatory drug users: a population-based study of postmenopausal women. Genes Chromosomes Cancer. 2011;50(11):875–86.  https://doi.org/10.1002/gcc.20913.CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Slattery ML, Curtin K, Poole EM, Duggan DJ, Samowitz WS, Peters U, et al. Genetic variation in C-reactive protein in relation to colon and rectal cancer risk and survival. Int J Cancer. 2011;128(11):2726–34.  https://doi.org/10.1002/ijc.25721.CrossRefPubMedGoogle Scholar
  63. 63.
    Coghill AE, Newcomb PA, Poole EM, Hutter CM, Makar KW, Duggan D, et al. Genetic variation in inflammatory pathways is related to colorectal cancer survival. Clin Cancer Res. 2011;17(22):7139–47.  https://doi.org/10.1158/1078-0432.ccr-11-1134.CrossRefGoogle Scholar
  64. 64.
    Passarelli MN, Newcomb PA, Makar KW, Burnett-Hartman AN, Phipps AI, David SP, et al. No association between germline variation in catechol-O-methyltransferase and colorectal cancer survival in postmenopausal women. Menopause. 2014;21(4):415–20.  https://doi.org/10.1097/GME.0b013e31829e498d.
  65. 65.
    Passarelli MN, Phipps AI, Potter JD, Makar KW, Coghill AE, Wernli KJ, et al. Common single-nucleotide polymorphisms in the estrogen receptor beta promoter are associated with colorectal cancer survival in postmenopausal women. Cancer Res. 2013;73(2):767–75.  https://doi.org/10.1158/0008-5472.can-12-2484.CrossRefPubMedGoogle Scholar
  66. 66.
    Phipps AI, Ahnen DJ, Campbell PT, Win AK, Jenkins MA, Lindor NM, et al. Family history of colorectal cancer is not associated with colorectal cancer survival regardless of microsatellite instability status. Cancer Epidemiol Biomark Prev. 2014;23(8):1700–4.  https://doi.org/10.1158/1055-9965.epi-14-0533.CrossRefGoogle Scholar
  67. 67.
    Adams SV, Ahnen DJ, Baron JA, Campbell PT, Gallinger S, Grady WM, et al. Survival after inflammatory bowel disease-associated colorectal cancer in the Colon Cancer Family Registry. World J Gastroenterol. 2013;19(21):3241–8.  https://doi.org/10.3748/wjg.v19.i21.3241.CrossRefGoogle Scholar
  68. 68.
    Campbell PT, Newton CC, Newcomb PA, Phipps AI, Ahnen DJ, Baron JA, et al. Association between body mass index and mortality for colorectal cancer survivors: overall and by tumor molecular phenotype. Cancer Epidemiol Biomark Prev. 2015;24(8):1229–38.  https://doi.org/10.1158/1055-9965.epi-15-0094.CrossRefGoogle Scholar
  69. 69.
    Phipps AI, Baron J, Newcomb PA. Prediagnostic smoking history, alcohol consumption, and colorectal cancer survival: the Seattle Colon Cancer Family Registry. Cancer. 2011;117(21):4948–57.  https://doi.org/10.1002/cncr.26114.CrossRefGoogle Scholar
  70. 70.
    Phipps AI, Robinson JR, Campbell PT, Win AK, Figueiredo JC, Lindor NM, et al. Prediagnostic alcohol consumption and colorectal cancer survival: the Colon Cancer Family Registry. Cancer. 2016.  https://doi.org/10.1002/cncr.30446.
  71. 71.
    Coghill AE, Newcomb PA, Campbell PT, Burnett-Hartman AN, Adams SV, Poole EM, et al. Prediagnostic non-steroidal anti-inflammatory drug use and survival after diagnosis of colorectal cancer. Gut. 2011;60(4):491–8.  https://doi.org/10.1136/gut.2010.221143.CrossRefPubMedGoogle Scholar
  72. 72.
    Coghill AE, Newcomb PA, Chia VM, Zheng Y, Wernli KJ, Passarelli MN, et al. Pre-diagnostic NSAID use but not hormone therapy is associated with improved colorectal cancer survival in women. Br J Cancer. 2011;104(5):763–8.  https://doi.org/10.1038/sj.bjc.6606041.CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Hardikar S, Newcomb PA, Campbell PT, Win AK, Lindor NM, Buchanan DD, et al. Prediagnostic physical activity and colorectal cancer survival: overall and stratified by tumor characteristics. Cancer Epidemiol Biomark Prev. 2015;24(7):1130–7.  https://doi.org/10.1158/1055-9965.epi-15-0039.CrossRefGoogle Scholar
  74. 74.
    Jayasekara H, Reece JC, Buchanan DD, Rosty C, Dashti SG, Ait Ouakrim D, et al. Risk factors for metachronous colorectal cancer following a primary colorectal cancer: a prospective cohort study. Int J Cancer. 2016;139(5):1081–90.  https://doi.org/10.1002/ijc.30153.CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Cleary SP, Cotterchio M, Shi E, Gallinger S, Harper P. Cigarette smoking, genetic variants in carcinogen-metabolizing enzymes, and colorectal cancer risk. Am J Epidemiol. 2010;172(9):1000–14.  https://doi.org/10.1093/aje/kwq245.CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Campbell PT, Jacobs ET, Ulrich CM, Figueiredo JC, Poynter JN, JR ML, et al. Case–control study of overweight, obesity, and colorectal cancer risk, overall and by tumor microsatellite instability status. J Natl Cancer Inst. 2010;102(6):391–400.  https://doi.org/10.1093/jnci/djq011.CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Wernli KJ, Wang Y, Zheng Y, Potter JD, Newcomb PA. The relationship between gravidity and parity and colorectal cancer risk. J Women's Health. 2009;18(7):995–1001.  https://doi.org/10.1089/jwh.2008.1068.CrossRefGoogle Scholar
  78. 78.
    Boardman LA, Morlan BW, Rabe KG, Petersen GM, Lindor NM, Nigon SK, et al. Colorectal cancer risks in relatives of young-onset cases: is risk the same across all first-degree relatives? Clin Gastroenterol Hepatol. 2007;5(10):1195–8.  https://doi.org/10.1016/j.cgh.2007.06.001.CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Lindor NM, Rabe KG, Petersen GM, Chen H, Bapat B, Hopper J, et al. Parent of origin effects on age at colorectal cancer diagnosis. Int J Cancer. 2010;127(2):361–6.  https://doi.org/10.1002/ijc.25037.CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Gong J, Hutter CM, Newcomb PA, Ulrich CM, Bien SA, Campbell PT, et al. Genome-wide interaction analyses between genetic variants and alcohol consumption and smoking for risk of colorectal cancer. PLoS Genet. 2016;12(10):e1006296.  https://doi.org/10.1371/journal.pgen.1006296.CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Makar KW, Poole EM, Resler AJ, Seufert B, Curtin K, Kleinstein SE, et al. COX-1 (PTGS1) and COX-2 (PTGS2) polymorphisms, NSAID interactions, and risk of colon and rectal cancers in two independent populations. Cancer Causes Control. 2013;24(12):2059–75.  https://doi.org/10.1007/s10552-013-0282-1.CrossRefGoogle Scholar
  82. 82.
    Nan H, Hutter CM, Lin Y, Jacobs EJ, Ulrich CM, White E, et al. Association of aspirin and NSAID use with risk of colorectal cancer according to genetic variants. JAMA. 2015;313(11):1133–42.  https://doi.org/10.1001/jama.2015.1815.CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Resler AJ, Makar KW, Heath L, Whitton J, Potter JD, Poole EM, et al. Genetic variation in prostaglandin synthesis and related pathways, NSAID use and colorectal cancer risk in the Colon Cancer Family Registry. Carcinogenesis. 2014;35(9):2121–6.  https://doi.org/10.1093/carcin/bgu119.CrossRefGoogle Scholar
  84. 84.
    Scherer D, Koepl LM, Poole EM, Balavarca Y, Xiao L, Baron JA, et al. Genetic variation in UGT genes modify the associations of NSAIDs with risk of colorectal cancer: Colon Cancer Family Registry. Genes Chromosomes Cancer. 2014;53(7):568–78.  https://doi.org/10.1002/gcc.22167.CrossRefGoogle Scholar
  85. 85.
    Seufert BL, Poole EM, Whitton J, Xiao L, Makar KW, Campbell PT, et al. IkappaBKbeta and NFkappaB1, NSAID use and risk of colorectal cancer in the Colon Cancer Family Registry. Carcinogenesis. 2013;34(1):79–85.  https://doi.org/10.1093/carcin/bgs296.
  86. 86.
    Campbell PT, Newcomb P, Gallinger S, Cotterchio M, McLaughlin JR. Exogenous hormones and colorectal cancer risk in Canada: associations stratified by clinically defined familial risk of cancer. Cancer Causes Control. 2007;18(7):723–33.  https://doi.org/10.1007/s10552-007-9015-7.CrossRefGoogle Scholar
  87. 87.
    Campbell PT, Cotterchio M, Klar N, JR ML, Gallinger S. Colorectal cancer risk among post-menopausal hormone users in a population-based familial case-control study. Ann Epidemiol. 2003;13(8):562. https://doi.org/10.1016/S1047-2797(03)00144-3.CrossRefGoogle Scholar
  88. 88.
    Garcia-Albeniz X, Rudolph A, Hutter C, White E, Lin Y, Rosse SA, et al. CYP24A1 variant modifies the association between use of oestrogen plus progestogen therapy and colorectal cancer risk. Br J Cancer. 2016;114(2):221–9.  https://doi.org/10.1038/bjc.2015.443.CrossRefPubMedPubMedCentralGoogle Scholar
  89. 89.
    Figueiredo J, Levine A, Lee W, Conti D, Poynter J, Campbell P, et al. Genes involved with folate uptake and distribution and their association with colorectal cancer risk. Cancer Causes Control. 2010;21(4):597–608.  https://doi.org/10.1007/s10552-009-9489-6.CrossRefPubMedGoogle Scholar
  90. 90.
    Levine AJ, Figueiredo JC, Lee W, Poynter JN, Conti D, Duggan DJ, et al. Genetic variability in the MTHFR gene and Colorectal cancer risk using the Colorectal Cancer Family Registry. Cancer Epidemiol Biomark Prev. 2010;19(1):89–100.  https://doi.org/10.1158/1055-9965.epi-09-0727.CrossRefGoogle Scholar
  91. 91.
    Levine AJ, Figueiredo JC, Lee W, Conti DV, Kennedy K, Duggan DJ, et al. A candidate gene study of folate-associated one carbon metabolism genes and colorectal cancer risk. Cancer Epidemiol Biomark Prev. 2010;19(7):1812–21.  https://doi.org/10.1158/1055-9965.EPI-10-0151.CrossRefGoogle Scholar
  92. 92.
    Kim HS, Newcomb PA, Ulrich CM, Keener CL, Bigler J, Farin FM, et al. Vitamin D receptor polymorphism and the risk of colorectal adenomas. Cancer Epidemiol Biomark Prev. 2001;10(8):869–74.Google Scholar
  93. 93.
    Poynter JN, Jacobs ET, Figueiredo JC, Lee WH, Conti DV, Campbell PT, et al. Genetic variation in the vitamin D receptor (VDR) and the vitamin D-binding protein (GC) and risk for colorectal cancer: results from the Colon Cancer Family Registry. Cancer Epidemiol Biomark Prev. 2010;19(2):525–36.  https://doi.org/10.1158/1055-9965.EPI-09-0662.CrossRefGoogle Scholar
  94. 94.
    Sun Z, Wang PP, Roebothan B, Cotterchio M, Green R, Buehler S et al. Calcium and vitamin D and risk of colorectal cancer: results from a large population-based case-control study in Newfoundland and Labrador and Ontario. Can J Public Health. 2011;102(5):382-9.Google Scholar
  95. 95.
    Hiraki LT, Qu C, Hutter CM, Baron JA, Berndt SI, Bezieau S, et al. Genetic predictors of circulating 25-hydroxyvitamin d and risk of colorectal cancer. Cancer Epidemiol Biomark Prev. 2013;22(11):2037–46.  https://doi.org/10.1158/1055-9965.epi-13-0209.
  96. 96.
    Du M, Zhang X, Hoffmeister M, Schoen RE, Baron JA, Berndt SI, et al. No evidence of gene-calcium interactions from genome-wide analysis of colorectal cancer risk. Cancer Epidemiol Biomark Prev. 2014;23(12):2971–6.  https://doi.org/10.1158/1055-9965.epi-14-0893.
  97. 97.
    Joshi AD, Corral R, Siegmund KD, Haile RW, Le Marchand L, Martinez ME, et al. Red meat and poultry intake, polymorphisms in the nucleotide excision repair and mismatch repair pathways and colorectal cancer risk. Carcinogenesis. 2009;30(3):472–9.  https://doi.org/10.1093/carcin/bgn260.CrossRefPubMedGoogle Scholar
  98. 98.
    Cotterchio M, Boucher BA, Manno M, Gallinger S, Okey AB, Harper PA. Red meat intake, doneness, polymorphisms in genes that encode carcinogen-metabolizing enzymes, and colorectal cancer risk. Cancer Epidemiol Biomark Prev. 2008;17(11):3098–107.  https://doi.org/10.1158/1055-9965.epi-08-0341.CrossRefGoogle Scholar
  99. 99.
    Chia VM, Newcomb PA, Lampe JW, White E, Mandelson MT, McTiernan A, et al. Leptin concentrations, leptin receptor polymorphisms, and colorectal adenoma risk. Cancer Epidemiol Biomark Prev. 2007;16(12):2697–703.  https://doi.org/10.1158/1055-9965.EPI-07-0467.CrossRefGoogle Scholar
  100. 100.
    Cotterchio M, Boucher BA, Manno M, Gallinger S, Okey A, Harper P. Dietary phytoestrogen intake is associated with reduced colorectal cancer risk. J Nutr. 2006;136(12):3046–53.CrossRefGoogle Scholar
  101. 101.
    Sun Z, Zhu Y, Wang PP, Roebothan B, Zhao J, Dicks E, et al. Reported intake of selected micronutrients and risk of colorectal cancer: results from a large population-based case-control study in Newfoundland, Labrador and Ontario, Canada. Anticancer Res. 2012;32(2):687–96.PubMedGoogle Scholar
  102. 102.
    Thrift AP, Gong J, Peters U, Chang-Claude J, Rudolph A, Slattery ML, et al. Mendelian randomization study of height and risk of colorectal cancer. Int J Epidemiol. 2015;44(2):662–72.  https://doi.org/10.1093/ije/dyv082.CrossRefPubMedPubMedCentralGoogle Scholar
  103. 103.
    Thrift AP, Gong J, Peters U, Chang-Claude J, Rudolph A, Slattery ML, et al. Mendelian randomization study of body mass index and colorectal cancer risk. Cancer Epidemiol Biomark Prev. 2015;24(7):1024–31.  https://doi.org/10.1158/1055-9965.epi-14-1309.
  104. 104.
    Jarvis D, Mitchell JS, Law PJ, Palin K, Tuupanen S, Gylfe A, et al. Mendelian randomisation analysis strongly implicates adiposity with risk of developing colorectal cancer. Br J Cancer. 2016;115(2):266–72.  https://doi.org/10.1038/bjc.2016.188.CrossRefPubMedPubMedCentralGoogle Scholar
  105. 105.
    Houlston RS, Webb E, Broderick P, Pittman AM, Di Bernardo MC, Lubbe S, et al. Meta-analysis of genome-wide association data identifies four new susceptibility loci for colorectal cancer. Nat Genet. 2008;40(12):1426–35.  https://doi.org/10.1038/ng.262.CrossRefPubMedGoogle Scholar
  106. 106.
    Tenesa A, Farrington SM, Prendergast JG, Porteous ME, Walker M, Haq N, et al. Genome-wide association scan identifies a colorectal cancer susceptibility locus on 11q23 and replicates risk loci at 8q24 and 18q21. Nat Genet. 2008;40(5):631–7.  https://doi.org/10.1038/ng.133.CrossRefPubMedPubMedCentralGoogle Scholar
  107. 107.
    Poynter JN, Figueiredo JC, Conti DV, Kennedy K, Gallinger S, Siegmund KD, et al. Variants on 9p24 and 8q24 are associated with risk of colorectal cancer: results from the Colon Cancer Family Registry. Cancer Res. 2007;67(23):11128–32.  https://doi.org/10.1158/0008-5472.can-07-3239.CrossRefGoogle Scholar
  108. 108.
    Schumacher FR, Schmit SL, Jiao S, Edlund CK, Wang H, Zhang B, et al. Genome-wide association study of colorectal cancer identifies six new susceptibility loci. Nat Commun. 2015;6:7138.  https://doi.org/10.1038/ncomms8138.CrossRefPubMedPubMedCentralGoogle Scholar
  109. 109.
    Al-Tassan NA, Whiffin N, Hosking FJ, Palles C, Farrington SM, Dobbins SE, et al. A new GWAS and meta-analysis with 1000Genomes imputation identifies novel risk variants for colorectal cancer. Sci Rep. 2015;5:10442.  https://doi.org/10.1038/srep10442.CrossRefPubMedPubMedCentralGoogle Scholar
  110. 110.
    Cheng I, Kocarnik JM, Dumitrescu L, Lindor NM, Chang-Claude J, Avery CL, et al. Pleiotropic effects of genetic risk variants for other cancers on colorectal cancer risk: PAGE, GECCO and CCFR consortia. Gut. 2014;63(5):800–7.  https://doi.org/10.1136/gutjnl-2013-305189.CrossRefPubMedGoogle Scholar
  111. 111.
    Cheng TH, Thompson D, Painter J, O’Mara T, Gorman M, Martin L, et al. Meta-analysis of genome-wide association studies identifies common susceptibility polymorphisms for colorectal and endometrial cancer near SH2B3 and TSHZ1. Sci Rep. 2015;5:17369.  https://doi.org/10.1038/srep17369.CrossRefPubMedPubMedCentralGoogle Scholar
  112. 112.
    Lemire M, Qu C, Loo LW, Zaidi SH, Wang H, Berndt SI, et al. A genome-wide association study for colorectal cancer identifies a risk locus in 14q23.1. Hum Genet. 2015;134(11–12):1249–62.  https://doi.org/10.1007/s00439-015-1598-6.CrossRefPubMedPubMedCentralGoogle Scholar
  113. 113.
    Whiffin N, Hosking FJ, Farrington SM, Palles C, Dobbins SE, Zgaga L, et al. Identification of susceptibility loci for colorectal cancer in a genome-wide meta-analysis. Hum Mol Genet. 2014;23(17):4729–37.  https://doi.org/10.1093/hmg/ddu177.CrossRefPubMedPubMedCentralGoogle Scholar
  114. 114.
    Zeng C, Matsuda K, Jia WH, Chang J, Kweon SS, Xiang YB, et al. Identification of susceptibility loci and genes for colorectal cancer risk. Gastroenterology. 2016;150(7):1633–45.  https://doi.org/10.1053/j.gastro.2016.02.076.CrossRefPubMedPubMedCentralGoogle Scholar
  115. 115.
    Jia WH, Zhang B, Matsuo K, Shin A, Xiang YB, Jee SH, et al. Genome-wide association analyses in east Asians identify new susceptibility loci for colorectal cancer. Nat Genet. 2013;45(2):191–6.  https://doi.org/10.1038/ng.2505.CrossRefGoogle Scholar
  116. 116.
    Wang H, Haiman CA, Burnett T, Fortini BK, Kolonel LN, Henderson BE, et al. Fine-mapping of genome-wide association study-identified risk loci for colorectal cancer in African Americans. Hum Mol Genet. 2013;22(24):5048–55.  https://doi.org/10.1093/hmg/ddt337.CrossRefPubMedPubMedCentralGoogle Scholar
  117. 117.
    Wang H, Burnett T, Kono S, Haiman CA, Iwasaki M, Wilkens LR, et al. Trans-ethnic genome-wide association study of colorectal cancer identifies a new susceptibility locus in VTI1A. Nat Commun. 2014;5:4613.  https://doi.org/10.1038/ncomms5613.CrossRefPubMedPubMedCentralGoogle Scholar
  118. 118.
    Dunlop MG, Tenesa A, Farrington SM, Ballereau S, Brewster DH, Koessler T, et al. Cumulative impact of common genetic variants and other risk factors on colorectal cancer risk in 42,103 individuals. Gut. 2013;62(6):871–81.  https://doi.org/10.1136/gutjnl-2011-300537.CrossRefPubMedGoogle Scholar
  119. 119.
    Roberts A, Nancarrow D, Clendenning M, Buchanan DD, Jenkins MA, Duggan D, et al. Linkage to chromosome 2q32.2-q33.3 in familial serrated neoplasia (Jass syndrome). Fam Cancer. 2011;10(2):245–54.  https://doi.org/10.1007/s10689-010-9408-8.CrossRefGoogle Scholar
  120. 120.
    Zogopoulos G, Jorgensen C, Bacani J, Montpetit A, Lepage P, Ferretti V, et al. Germline EPHB2 receptor variants in familial colorectal cancer. PLoS One. 2008;3(8):e2885.  https://doi.org/10.1371/journal.pone.0002885.CrossRefPubMedPubMedCentralGoogle Scholar
  121. 121.
    Young J, Jass JR. The case for a genetic predisposition to serrated neoplasia in the colorectum: hypothesis and review of the literature. Cancer Epidemiol Biomark Prev. 2006;15(10):1778–84.  https://doi.org/10.1158/1055-9965.epi-06-0164.CrossRefGoogle Scholar
  122. 122.
    Young J, Jenkins M, Parry S, Young B, Nancarrow D, English D, et al. Serrated pathway colorectal cancer in the population: genetic consideration. Gut. 2007;56(10):1453–9.  https://doi.org/10.1136/gut.2007.126870.CrossRefPubMedPubMedCentralGoogle Scholar
  123. 123.
    Yeoman A, Young J, Arnold J, Jass J, Parry S. Hyperplastic polyposis in the New Zealand population: a condition associated with increased colorectal cancer risk and European ancestry. N Z Med J. 2007;120(1266):U2827.PubMedGoogle Scholar
  124. 124.
    Jiang X, Castelao JE, Vandenberg D, Carracedo A, Redondo CM, Conti DV, et al. Genetic variations in SMAD7 are associated with colorectal cancer risk in the Colon Cancer Family Registry. PLoS One. 2013;8(4):e60464.  https://doi.org/10.1371/journal.pone.0060464.CrossRefGoogle Scholar
  125. 125.
    Chang CM, Chia VM, Gunter MJ, Zanetti KA, Ryan BM, Goodman JE, et al. Innate immunity gene polymorphisms and the risk of colorectal neoplasia. Carcinogenesis. 2013;34(11):2512–20.  https://doi.org/10.1093/carcin/bgt228.CrossRefPubMedPubMedCentralGoogle Scholar
  126. 126.
    Wang H, Taverna D, Stram DO, Fortini BK, Cheng I, Wilkens LR, et al. Genetic variation in the inflammation and innate immunity pathways and colorectal cancer risk. Cancer Epidemiol Biomark Prev. 2013;22(11):2094–101.  https://doi.org/10.1158/1055-9965.epi-13-0694.CrossRefGoogle Scholar
  127. 127.
    Abbenhardt C, Poole EM, Kulmacz RJ, Xiao L, Curtin K, Galbraith RL, et al. Phospholipase A2G1B polymorphisms and risk of colorectal neoplasia. Int J Mol Epidemiol Genet. 2013;4(3):140–9.PubMedPubMedCentralGoogle Scholar
  128. 128.
    Akbari MR, Anderson LN, Buchanan DD, Clendenning M, Jenkins MA, Win AK, et al. Germline HOXB13 p.Gly84Glu mutation and risk of colorectal cancer. Cancer Epidemiol. 2013;37(4):424–7.  https://doi.org/10.1016/j.canep.2013.03.003.CrossRefPubMedPubMedCentralGoogle Scholar
  129. 129.
    Yurgelun MB, Masciari S, Joshi VA, Mercado RC, Lindor NM, Gallinger S, et al. Germline TP53mutations in patients with early-onset colorectal cancer in the Colon Cancer Family Registry. JAMA Oncol. 2015;1(2):214–21.  https://doi.org/10.1001/jamaoncol.2015.0197.CrossRefGoogle Scholar
  130. 130.
    Bapat B, Lindor NM, Baron J, Siegmund K, Li L, Zheng Y, et al. The association of tumor microsatellite instability phenotype with family history of colorectal cancer. Cancer Epidemiol Biomark Prev. 2009;18(3):967–75.  https://doi.org/10.1158/1055-9965.EPI-08-0878.CrossRefGoogle Scholar
  131. 131.
    English DR, Young JP, Simpson JA, Jenkins MA, Southey MC, Walsh MD, et al. Ethnicity and risk for colorectal cancers showing somatic BRAF V600E mutation or CpG island methylator phenotype. Cancer Epidemiol Biomark Prev. 2008;17(7):1774–80.  https://doi.org/10.1158/1055-9965.EPI-08-0091.CrossRefGoogle Scholar
  132. 132.
    Weisenberger DJ, Siegmund KD, Campan M, Young J, Long TI, Faasse MA, et al. CpG island methylator phenotype underlies sporadic microsatellite instability and is tightly associated with BRAF mutation in colorectal cancer. Nat Genet. 2006;38(7):787–93. https://doi.org/10.1038/ng1834.CrossRefGoogle Scholar
  133. 133.
    Kambara T, Simms LA, VLJ W, Spring KJ, CVA W, Walsh MD, et al. BRAF mutation is associated with DNA methylation in serrated polyps and cancers of the colorectum. Gut. 2004;53(8):1137–44.  https://doi.org/10.1136/gut.2003.037671.CrossRefPubMedPubMedCentralGoogle Scholar
  134. 134.
    Hitchins M, Williams R, Cheong K, Halani N, Lin VAP, Packham D, et al. MLH1 Germline Epimutations as a factor in hereditary nonpolyposis colorectal cancer. Gastroenterology. 2005;129(5):1392–9.  https://doi.org/10.1053/j.gastro.2005.09.003.CrossRefPubMedGoogle Scholar
  135. 135.
    Coolbaugh-Murphy MI, Xu J, Ramagli LS, Brown BW, Siciliano MJ. Microsatellite instability (MSI) increases with age in normal somatic cells. Mech Ageing Dev. 2005;126(10):1051–9.  https://doi.org/10.1016/j.mad.2005.06.005.CrossRefPubMedGoogle Scholar
  136. 136.
    Kakar S, Burgart LJ, Thibodeau SN, Rabe KG, Petersen GM, Goldberg RM, et al. Frequency of loss of hMLH1 expression in colorectal carcinoma increases with advancing age. Cancer. 2003;97(6):1421–7.  https://doi.org/10.1002/cncr.11206.CrossRefPubMedGoogle Scholar
  137. 137.
    Savio AJ, Daftary D, Dicks E, Buchanan DD, Parfrey PS, Young JP, et al. Promoter methylation of ITF2, but not APC, is associated with microsatellite instability in two populations of colorectal cancer patients. BMC Cancer. 2016;16:113.  https://doi.org/10.1186/s12885-016-2149-9.CrossRefPubMedPubMedCentralGoogle Scholar
  138. 138.
    Walters RJ, Williamson EJ, English DR, Young JP, Rosty C, Clendenning M, et al. Association between hypermethylation of DNA repetitive elements in white blood cell DNA and early-onset colorectal cancer. Epigenetics. 2013;8(7):748–55.  https://doi.org/10.4161/epi.25178.CrossRefPubMedPubMedCentralGoogle Scholar
  139. 139.
    Win AK, Jenkins MA, Dowty JG, Antoniou AC, Lee A, Giles GG, et al. Prevalence and penetrance of major genes and polygenes for colorectal cancer. Cancer Epidemiol Biomarkers Prev. 2016.  https://doi.org/10.1158/1055-9965.EPI-16-0693.
  140. 140.
    Kastrinos F, Ojha RP, Leenen C, Alvero C, Mercado RC, Balmana J, et al. Comparison of prediction models for Lynch syndrome among individuals with colorectal cancer. J Natl Cancer Inst. 2016;108(2).  https://doi.org/10.1093/jnci/djv308.
  141. 141.
    Kastrinos F, Steyerberg EW, Balmana J, Mercado R, Gallinger S, Haile R, et al. Comparison of the clinical prediction model PREMM(1,2,6) and molecular testing for the systematic identification of Lynch syndrome in colorectal cancer. Gut. 2013;62(2):272–9.  https://doi.org/10.1136/gutjnl-2011-301265.CrossRefPubMedGoogle Scholar
  142. 142.
    Kastrinos F, Steyerberg EW, Mercado R, Balmana J, Holter S, Gallinger S, et al. The PREMM(1,2,6) model predicts risk of MLH1, MSH2, and MSH6 germline mutations based on cancer history. Gastroenterology. 2011;140(1):73–81.  https://doi.org/10.1053/j.gastro.2010.08.021.CrossRefPubMedPubMedCentralGoogle Scholar
  143. 143.
    Casey G, Lindor NM, Papadopoulos N, Thibodeau SN, Moskow J, Steelman S, et al. Conversion analysis for mutation detection in MLH1 and MSH2 in patients with colorectal cancer. JAMA. 2005;293(7):799–809.  https://doi.org/10.1001/jama.293.7.799.CrossRefPubMedPubMedCentralGoogle Scholar
  144. 144.
    Cleary SP, Kim H, Croitoru ME, Redston M, Knight JA, Gallinger S, et al. Missense polymorphisms in the adenomatous polyposis coli gene and colorectal cancer risk. Dis Colon Rectum. 2008;51(10):1467–73; discussion 1473-74.  https://doi.org/10.1007/s10350-008-9356-7.CrossRefGoogle Scholar
  145. 145.
    Hahnloser D, Petersen GM, Rabe K, Snow K, Lindor NM, Boardman L, et al. The APC E1317Q variant in adenomatous polyps and colorectal cancers. Cancer Epidemiol Biomark Prev. 2003;12(10):1023–8.Google Scholar
  146. 146.
    Jaskowski L, Young J, Jackson L, Arnold S, Barker MA, Walsh MD, et al. Stability of BAT26 in Lynch syndrome colorectal tumours. Eur J Hum Genet. 2007;15(2):139–41; author reply 41-2.  https://doi.org/10.1038/sj.ejhg.5201740.CrossRefGoogle Scholar
  147. 147.
    Jenkins MA, Hayashi S, O'Shea AM, Burgart LJ, Smyrk TC, Shimizu D, et al. Pathology features in Bethesda guidelines predict colorectal cancer microsatellite instability: a population-based study. Gastroenterology. 2007;133(1):48–56.  https://doi.org/10.1053/j.gastro.2007.04.044.CrossRefPubMedPubMedCentralGoogle Scholar
  148. 148.
    Zogopoulos G, Ha KC, Naqib F, Moore S, Kim H, Montpetit A, et al. Germ-line DNA copy number variation frequencies in a large North American population. Hum Genet. 2007;122(3–4):345–53.  https://doi.org/10.1007/s00439-007-0404-5.CrossRefPubMedGoogle Scholar
  149. 149.
    Clendenning M, Macrae FA, Walsh MD, Walters RJ, Thibodeau SN, Gunawardena SR, et al. Absence of PMS2 mutations in Colon-CFR participants whose colorectal cancers demonstrate unexplained loss of MLH1 expression. Clin Genet. 2013;83(6):591–3.  https://doi.org/10.1111/cge.12011.CrossRefGoogle Scholar
  150. 150.
    Clendenning M, Walsh MD, Gelpi JB, Thibodeau SN, Lindor N, Potter JD, et al. Detection of large scale 3′ deletions in the PMS2 gene amongst Colon-CFR participants: have we been missing anything? Fam Cancer. 2013;12(3):563–6.  https://doi.org/10.1007/s10689-012-9597-4.CrossRefGoogle Scholar
  151. 151.
    Cunningham JM, Johnson RA, Litzelman K, Skinner HG, Seo S, Engelman CD, et al. Telomere length varies by DNA extraction method: implications for epidemiologic research. Cancer Epidemiol Biomark Prev. 2013;22(11):2047–54.  https://doi.org/10.1158/1055-9965.epi-13-0409.
  152. 152.
    Boardman LA, Litzelman K, Seo S, Johnson RA, Vanderboom RJ, Kimmel GW, et al. The association of telomere length with colorectal cancer differs by the age of cancer onset. Clinical and Translat Gastroenterol. 2014;5:e52.  https://doi.org/10.1038/ctg.2014.3.CrossRefGoogle Scholar
  153. 153.
    Kuroiwa-Trzmielina J, Wang F, Rapkins RW, Ward RL, Buchanan DD, Win AK, et al. SNP rs16906252C>T is an expression and methylation quantitative trait locus associated with an increased risk of developing MGMT-methylated colorectal cancer. Clin Cancer Res. 2016;22(24):6266–77.  https://doi.org/10.1158/1078-0432.ccr-15-2765.CrossRefGoogle Scholar
  154. 154.
    Uddin M, Thiruvahindrapuram B, Walker S, Wang Z, Hu P, Lamoureux S, et al. A high-resolution copy-number variation resource for clinical and population genetics. Genet Med. 2015;17(9):747–52.  https://doi.org/10.1038/gim.2014.178.CrossRefGoogle Scholar
  155. 155.
    Win AK, Buchanan DD, Rosty C, RJ MI, Dowty JG, Dite GS, et al. Role of tumour molecular and pathology features to estimate colorectal cancer risk for first-degree relatives. Gut. 2015;64(1):101–10.  https://doi.org/10.1136/gutjnl-2013-306567.CrossRefGoogle Scholar
  156. 156.
    Kim JS, Coyte PC, Cotterchio M, Keogh LA, Flander LB, Gaff C, et al. The impact of receiving predictive genetic information about Lynch syndrome on individual colonoscopy and smoking behaviors. Cancer Epidemiol Biomark Prev. 2016;25(11):1524–33.  https://doi.org/10.1158/1055-9965.epi-16-0346.CrossRefGoogle Scholar
  157. 157.
    Esplen MJ, Wong J, Aronson M, Butler K, Rothenmund H, Semotiuk K, et al. Long-term psychosocial and behavioral adjustment in individuals receiving genetic test results in Lynch syndrome. Clin Genet. 2015;87(6):525–32.  https://doi.org/10.1111/cge.12509.CrossRefPubMedGoogle Scholar
  158. 158.
    Graves KD, Sinicrope PS, Esplen MJ, Peterson SK, Patten CA, Lowery J, et al. Communication of genetic test results to family and health-care providers following disclosure of research results. Genet Med. 2014;16(4):294–301.  https://doi.org/10.1038/gim.2013.137.CrossRefPubMedGoogle Scholar
  159. 159.
    Patel SG, Ahnen DJ, Kinney AY, Horick N, Finkelstein DM, Hill DA, et al. Knowledge and uptake of genetic counseling and colonoscopic screening among individuals at increased risk for Lynch syndrome and their endoscopists from the Family Health Promotion Project. Am J Gastroenterol. 2016;111(2):285–93.  https://doi.org/10.1038/ajg.2015.397.CrossRefGoogle Scholar
  160. 160.
    Flander L, Speirs-Bridge A, Rutstein A, Niven H, Win AK, Ait Ouakrim D, et al. Perceived versus predicted risks of colorectal cancer and self-reported colonoscopies by members of mismatch repair gene mutation-carrying families who have declined genetic testing. J Genet Couns. 2014;23(1):79–88.  https://doi.org/10.1007/s10897-013-9614-2.CrossRefPubMedGoogle Scholar
  161. 161.
    Steel EJ, Trainer AH, Heriot AG, Lynch C, Parry S, Win AK, et al. The experience of extended bowel resection in individuals with a high metachronous colorectal cancer risk: a qualitative study. Oncol Nurs Forum. 2016;43(4):444–52.  https://doi.org/10.1188/16.onf.444-452.CrossRefGoogle Scholar
  162. 162.
    Adams SV, Ceballos R, Newcomb PA. Quality of life and mortality of long-term colorectal cancer survivors in the Seattle Colorectal Cancer Family Registry. PLoS One. 2016;11(6):e0156534.  https://doi.org/10.1371/journal.pone.0156534.CrossRefGoogle Scholar
  163. 163.
    Howell LA, Brockman TA, Sinicrope PS, Patten CA, Decker PA, Ehlers SL, et al. Receptivity and preferences in cancer risk reduction lifestyle programs: a survey of colorectal cancer family members. J Behav Health. 2013;2(4):279–90.  https://doi.org/10.5455/jbh.20130921013627.CrossRefPubMedPubMedCentralGoogle Scholar
  164. 164.
    Lowery JT, Horick N, Kinney AY, Finkelstein DM, Garrett K, Haile RW, et al. A randomized trial to increase colonoscopy screening in members of high-risk families in the Colorectal Cancer Family Registry and Cancer Genetics Network. Cancer Epidemiol Biomark Prev. 2014;23(4):601–10.  https://doi.org/10.1158/1055-9965.epi-13-1085.CrossRefGoogle Scholar
  165. 165.
    Bharati R, Jenkins MA, Lindor NM, Le Marchand L, Gallinger S, Haile RW, et al. Does risk of endometrial cancer for women without a germline mutation in a DNA mismatch repair gene depend on family history of endometrial cancer or colorectal cancer? Gynecol Oncol. 2014;133(2):287–92.  https://doi.org/10.1016/j.ygyno.2014.03.011.CrossRefPubMedPubMedCentralGoogle Scholar
  166. 166.
    Ahsan H, Halpern J, Kibriya MG, Pierce BL, Tong L, Gamazon E, et al. A genome-wide association study of early-onset breast cancer identifies PFKM as a novel breast cancer gene and supports a common genetic spectrum for breast cancer at any age. Cancer Epidemiol Biomark Prev. 2014;23(4):658–69.  https://doi.org/10.1158/1055-9965.epi-13-0340.
  167. 167.
    Anderson LN, Cotterchio M, Knight JA, Borgida A, Gallinger S, Cleary SP. Genetic variants in vitamin D pathway genes and risk of pancreas cancer; results from a population-based case-control study in Ontario, Canada. PLoS One. 2013;8(6):e66768.  https://doi.org/10.1371/journal.pone.0066768.CrossRefGoogle Scholar
  168. 168.
    Bosetti C, Lucenteforte E, Bracci PM, Negri E, Neale RE, Risch HA, et al. Ulcer, gastric surgery and pancreatic cancer risk: an analysis from the international pancreatic cancer case-control consortium (PanC4). Ann Oncol. 2013;24(11):2903–10.  https://doi.org/10.1093/annonc/mdt336.CrossRefGoogle Scholar
  169. 169.
    Jang JH, Cotterchio M, Borgida A, Liu G, Gallinger S, Cleary SP. Interaction of polymorphisms in mitotic regulator genes with cigarette smoking and pancreatic cancer risk. Mol Carcinog. 2013;52(Suppl 1):E103–9.  https://doi.org/10.1002/mc.22037.CrossRefPubMedPubMedCentralGoogle Scholar
  170. 170.
    Olson SH, Hsu M, Satagopan JM, Maisonneuve P, Silverman DT, Lucenteforte E, et al. Allergies and risk of pancreatic cancer: a pooled analysis from the pancreatic cancer case-control consortium. Am J Epidemiol. 2013;178(5):691–700.  https://doi.org/10.1093/aje/kwt052.CrossRefPubMedPubMedCentralGoogle Scholar
  171. 171.
    Bosetti C, Rosato V, Li D, Silverman D, Petersen GM, Bracci PM, et al. Diabetes, antidiabetic medications, and pancreatic cancer risk: an analysis from the international pancreatic cancer case-control consortium. Ann Oncol. 2014;25(10):2065–72.  https://doi.org/10.1093/annonc/mdu276.
  172. 172.
    Vasen HF, Mecklin JP, Khan PM, Lynch HT. The International Collaborative Group on Hereditary Non-Polyposis Colorectal Cancer (ICG-HNPCC). Dis Colon Rectum. 1991;34(5):424–5.CrossRefGoogle Scholar
  173. 173.
    Vasen HF, Watson P, Mecklin JP, Lynch HT. New clinical criteria for hereditary nonpolyposis colorectal cancer (HNPCC, Lynch syndrome) proposed by the International Collaborative Group on HNPCC. Gastroenterology. 1999;116(6):1453–6.CrossRefGoogle Scholar
  174. 174.
    Jarvinen HJ, Aarnio M, Mustonen H, Aktan-Collan K, Aaltonen LA, Peltomaki P et al. Controlled 15-year trial on screening for colorectal cancer in families with hereditary nonpolyposis colorectal cancer. Gastroenterology 2000;118(5):829–834.CrossRefGoogle Scholar
  175. 175.
    Burn J, Gerdes AM, Macrae F, Mecklin JP, Moeslein G, Olschwang S, et al. Long-term effect of aspirin on cancer risk in carriers of hereditary colorectal cancer: an analysis from the CAPP2 randomised controlled trial. Lancet. 2011;378(9809):2081–7.  https://doi.org/10.1016/S0140-6736(11)61049-0.CrossRefPubMedPubMedCentralGoogle Scholar
  176. 176.
    Hopper JL. Disease-specific prospective family study cohorts enriched for familial risk. Epidemiol Perspect Innov. 2011;8(1):2. https://doi.org/10.1186/1742-5573-8-2.CrossRefGoogle Scholar
  177. 177.
    Cicek MS, Cunningham JM, Fridley BL, Serie DJ, Bamlet WR, Diergaarde B et al. Colorectal cancer linkage on chromosomes 4q21, 8q13, 12q24, and 15q22. PLoS One. 2012;7(5):e38175. https://doi.org/10.1371/journal.pone.0038175.CrossRefGoogle Scholar
  178. 178.
    Neklason DW, Kerber RA, Nilson DB, Anton-Culver H, Schwartz AG, Griffin CA et al. Common familial colorectal cancer linked to chromosome 7q31: a genome-wide analysis. Cancer Res. 2008;68(21):8993–7. https://doi.org/10.1158/0008-5472.can-08-1376.CrossRefGoogle Scholar
  179. 179.
    Gray-McGuire C, Guda K, Adrianto I, Lin CP, Natale L, Potter JD et al. Confirmation of linkage to and localization of familial colon cancer risk haplotype on chromosome 9q22. Cancer Res. 2010;70(13):5409–18. https://doi.org/10.1158/0008-5472.can-10-0188.CrossRefGoogle Scholar
  180. 180.
    DeRycke MS, Gunawardena SR, Middha S, Asmann YW, Schaid DJ, McDonnell SK et al. Identification of novel variants in colorectal cancer families by high-throughput exome sequencing. Cancer Epidemiol Biomarkers Prev. 2013;22(7):1239-51. https://doi.org/10.1158/1055-9965.epi-12-1226.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Mark A. Jenkins
    • 1
    • 2
  • Aung K. Win
    • 1
    • 2
    • 3
  • Noralane M. Lindor
    • 4
  1. 1.Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, Faculty of Medicine, Dentistry and Health Sciences, The University of MelbourneParkvilleAustralia
  2. 2.University of Melbourne Centre for Cancer Research, Victorian Comprehensive Cancer CentreParkvilleAustralia
  3. 3.Genetic Medicine and Familial Cancer Centre, The Royal Melbourne HospitalParkvilleAustralia
  4. 4.Department of Health Science ResearchMayo Clinic ArizonaScottsdaleUSA

Personalised recommendations