Top

Current Colorectal Cancer Reports

Published in:

Open Access 01-12-2017 | NUTRITION AND NUTRITIONAL INTERVENTIONS IN COLORECTAL CANCER (K WU, SECTION EDITOR)

Lifestyle, Diet, and Colorectal Cancer Risk According to (Epi)genetic Instability: Current Evidence and Future Directions of Molecular Pathological Epidemiology

Authors: Laura A. E. Hughes, Colinda C. J. M. Simons, Piet A. van den Brandt, Manon van Engeland, Matty P. Weijenberg

Published in: Current Colorectal Cancer Reports | Issue 6/2017

Abstract

Purpose of Review

In this review, we describe molecular pathological epidemiology (MPE) studies from around the world that have studied diet and/or lifestyle factors in relation to molecular markers of (epi)genetic pathways in colorectal cancer (CRC), and explore future perspectives in this realm of research. The main focus of this review is diet and lifestyle factors for which there is evidence for an association with CRC as identified by the World Cancer Research Fund reports. In addition, we review promising hypotheses, that warrant consideration in future studies.

Recent Findings

Associations between molecular characteristics of CRC have been published in relation to smoking, alcohol consumption; body mass index (BMI); waist:hip ratio; adult attained height; physical activity; early life energy restriction; dietary acrylamide, fiber, fat, methyl donors, omega 3 fatty acids; meat, including total protein, processed meat, and heme iron; and fruit and vegetable intake.

Summary

MPE studies help identify where associations between diet, lifestyle, and CRC risk may otherwise be masked and also shed light on how timing of exposure can influence etiology. Sample size is often an issue, but this may be addressed in the future by pooling data.

Arnold M, Sierra MS, Laversanne M, Soerjomataram I, Jemal A, Bray F. Global patterns and trends in colorectal cancer incidence and mortality. Gut. 2017;66(4):683–91. https://doi.org/10.1136/gutjnl-2015-310912.PubMedCrossRef

Muller MF, Ibrahim AE, Arends MJ. Molecular pathological classification of colorectal cancer. Virchows Arch. 2016;469(2):125–34. https://doi.org/10.1007/s00428-016-1956-3.PubMedPubMedCentralCrossRef

World Cancer Research Fund/American Institute for Cancer Research. Continuous Update Project Report: Diet, Nutrition, Physical Activity and Colorectal Cancer. 2017. Available at: wcrf.

• Ogino S, Chan AT, Fuchs CS, Giovannucci E. Molecular pathological epidemiology of colorectal neoplasia: an emerging transdisciplinary and interdisciplinary field. Gut. 2011;60(3):397–411. https://doi.org/10.1136/gut.2010.217182. This article coined the field of molecular pathological epidemiology PubMedCrossRef

• Song N, Pogue-Geile KL, Gavin PG, Yothers G, Kim SR, Johnson NL, et al. Clinical Outcome From Oxaliplatin Treatment in Stage II/III Colon Cancer According to Intrinsic Subtypes: Secondary Analysis of NSABP C-07/NRG Oncology Randomized Clinical Trial. JAMA Oncol. 2016;2(9):1162–9. https://doi.org/10.1001/jamaoncol.2016.2314. This article identifies recent advancements in CRC subtyping, which could influence future MPE study designs, leading to even more accurate prediction of risk. PubMedPubMedCentralCrossRef

Sadanandam A, Lyssiotis CA, Homicsko K, Collisson EA, Gibb WJ, Wullschleger S, et al. A colorectal cancer classification system that associates cellular phenotype and responses to therapy. Nat Med. 2013;19(5):619–25. https://doi.org/10.1038/nm.3175.PubMedPubMedCentralCrossRef

de Sousa E, Walter LT, Higa GS, Casado OA, Kihara AH. Developmental and functional expression of miRNA-stability related genes in the nervous system. PLoS One. 2013;8(5):e56908. https://doi.org/10.1371/journal.pone.0056908.PubMedPubMedCentralCrossRef

• Guinney J, Dienstmann R, Wang X, de Reynies A, Schlicker A, Soneson C, et al. The consensus molecular subtypes of colorectal cancer. Nat Med. 2015;21(11):1350–6. https://doi.org/10.1038/nm.3967. This summarizes recent advancements in CRC subtyping, which could influence future MPE study designs, leading to even more accurate prediction of risk. PubMedPubMedCentralCrossRef

Sadanandam A, Wang X, de Sousa EMF, Gray JW, Vermeulen L, Hanahan D, et al. Reconciliation of classification systems defining molecular subtypes of colorectal cancer: interrelationships and clinical implications. Cell Cycle. 2014;13(3):353–7. https://doi.org/10.4161/cc.27769.PubMedPubMedCentralCrossRef

10.

Ogino S, Stampfer M. Lifestyle factors and microsatellite instability in colorectal cancer: the evolving field of molecular pathological epidemiology. J Natl Cancer Inst. 2010;102(6):365–7. https://doi.org/10.1093/jnci/djq031.PubMedPubMedCentralCrossRef

11.

• Bae JM, Kim JH, Kang GH. Molecular subtypes of colorectal cancer and their clinicopathologic features, with an emphasis on the serrated neoplasia pathway. Arch Pathol Lab Med. 2016;140(5):406–12. https://doi.org/10.5858/arpa.2015-0310-RA. This article summarizes recent advancements in CRC subtyping, which could influence future MPE study designs, leading to even more accurate prediction of risk. PubMedCrossRef

12.

•• Campbell PT, Rebbeck TR, Nishihara R, Beck AH, Begg CB, Bogdanov AA, et al. Proceedings of the third international molecular pathological epidemiology (MPE) meeting. Cancer Causes Control. 2017;28(2):167–76. https://doi.org/10.1007/s10552-016-0845-z. This article highlighted a new wave of MPE research that is focused on increasing the understanding of the role that lifestyle/behavioural factors on modifying prognosis. PubMedCrossRef

13.

Ogino S, Nishihara R, VanderWeele TJ, Wang M, Nishi A, Lochhead P, et al. Review article: the role of molecular pathological epidemiology in the study of neoplastic and non-neoplastic diseases in the era of precision medicine. Epidemiology. 2016;27(4):602–11. https://doi.org/10.1097/EDE.0000000000000471.PubMedPubMedCentralCrossRef

14.

Rajagopalan H, Nowak MA, Vogelstein B, Lengauer C. The significance of unstable chromosomes in colorectal cancer. Nat Rev Cancer. 2003;3(9):695–701. https://doi.org/10.1038/nrc1165.PubMedCrossRef

15.

Sieber OM, Heinimann K, Tomlinson IP. Genomic instability—the engine of tumorigenesis? Nat Rev Cancer. 2003;3(9):701–8. https://doi.org/10.1038/nrc1170.PubMedCrossRef

16.

Derks S, Postma C, Carvalho B, van den Bosch SM, Moerkerk PT, Herman JG, et al. Integrated analysis of chromosomal, microsatellite and epigenetic instability in colorectal cancer identifies specific associations between promoter methylation of pivotal tumour suppressor and DNA repair genes and specific chromosomal alterations. Carcinogenesis. 2008;29(2):434–9. https://doi.org/10.1093/carcin/bgm270.PubMedCrossRef

17.

Hermsen M, Postma C, Baak J, Weiss M, Rapallo A, Sciutto A, et al. Colorectal adenoma to carcinoma progression follows multiple pathways of chromosomal instability. Gastroenterology. 2002;123(4):1109–19. https://doi.org/10.1053/gast.2002.36051.PubMedCrossRef

18.

Imai K, Yamamoto H. Carcinogenesis and microsatellite instability: the interrelationship between genetics and epigenetics. Carcinogenesis. 2008;29(4):673–80. https://doi.org/10.1093/carcin/bgm228.PubMedCrossRef

19.

Snover DC. Update on the serrated pathway to colorectal carcinoma. Hum Pathol. 2011;42(1):1–10. https://doi.org/10.1016/j.humpath.2010.06.002.PubMedCrossRef

20.

Cancer Genome Atlas N. Comprehensive molecular characterization of human colon and rectal cancer. Nature. 2012;487(7407):330–7. https://doi.org/10.1038/nature11252.CrossRef

21.

Gay LJ, Mitrou PN, Keen J, Bowman R, Naguib A, Cooke J, et al. Dietary, lifestyle and clinicopathological factors associated with APC mutations and promoter methylation in colorectal cancers from the EPIC-Norfolk study. J Pathol. 2012;228(3):405–15. https://doi.org/10.1002/path.4085.PubMedCrossRef

22.

Gay LJ, Arends MJ, Mitrou PN, Bowman R, Ibrahim AE, Happerfield L, et al. MLH1 promoter methylation, diet, and lifestyle factors in mismatch repair deficient colorectal cancer patients from EPIC-Norfolk. Nutr Cancer. 2011;63(7):1000–10. https://doi.org/10.1080/01635581.2011.596987.PubMedCrossRef

23.

Naguib A, Mitrou PN, Gay LJ, Cooke JC, Luben RN, Ball RY, et al. Dietary, lifestyle and clinicopathological factors associated with BRAF and K-ras mutations arising in distinct subsets of colorectal cancers in the EPIC Norfolk study. BMC Cancer. 2010;10(1):99. https://doi.org/10.1186/1471-2407-10-99.PubMedPubMedCentralCrossRef

24.

Park JY, Mitrou PN, Keen J, Dahm CC, Gay LJ, Luben RN, et al. Lifestyle factors and p53 mutation patterns in colorectal cancer patients in the EPIC-Norfolk study. Mutagenesis. 2010;25(4):351–8. https://doi.org/10.1093/mutage/geq012.PubMedCrossRef

25.

Samadder NJ, Vierkant RA, Tillmans LS, Wang AH, Lynch CF, Anderson KE, et al. Cigarette smoking and colorectal cancer risk by KRAS mutation status among older women. Am J Gastroenterol. 2012;107(5):782–9. https://doi.org/10.1038/ajg.2012.21.PubMedPubMedCentralCrossRef

26.

Brandstedt J, Wangefjord S, Borgquist S, Nodin B, Eberhard J, Manjer J, et al. Influence of anthropometric factors on tumour biological characteristics of colorectal cancer in men and women: a cohort study. J Transl Med. 2013;11(1):293. https://doi.org/10.1186/1479-5876-11-293.PubMedPubMedCentralCrossRef

27.

Brandstedt J, Wangefjord S, Nodin B, Eberhard J, Jirstrom K, Manjer J. Associations of hormone replacement therapy and oral contraceptives with risk of colorectal cancer defined by clinicopathological factors, beta-catenin alterations, expression of cyclin D1, p53, and microsatellite-instability. BMC Cancer. 2014;14(1):371. https://doi.org/10.1186/1471-2407-14-371.PubMedPubMedCentralCrossRef

28.

Razzak AA, Oxentenko AS, Vierkant RA, Tillmans LS, Wang AH, Weisenberger DJ, et al. Alcohol intake and colorectal cancer risk by molecularly defined subtypes in a prospective study of older women. Cancer Prev Res. 2011;4(12):2035–43. https://doi.org/10.1158/1940-6207.CAPR-11-0276.CrossRef

29.

Limburg PJ, Limsui D, Vierkant RA, Tillmans LS, Wang AH, Lynch CF, et al. Postmenopausal hormone therapy and colorectal cancer risk in relation to somatic KRAS mutation status among older women. Cancer Epidemiol Biomark Prev. 2012;21(4):681–4. https://doi.org/10.1158/1055-9965.EPI-11-1168.CrossRef

30.

Nishihara R, Morikawa T, Kuchiba A, Lochhead P, Yamauchi M, Liao X, et al. A prospective study of duration of smoking cessation and colorectal cancer risk by epigenetics-related tumor classification. Am J Epidemiol. 2013;178(1):84–100. https://doi.org/10.1093/aje/kws431.PubMedPubMedCentralCrossRef

31.

Song M, Nishihara R, Wu K, Qian ZR, Kim SA, Sukawa Y, et al. Marine omega-3 polyunsaturated fatty acids and risk of colorectal cancer according to microsatellite instability. J Natl Cancer Inst. 2015;107(4) https://doi.org/10.1093/jnci/djv007.

32.

Lee JE, Baba Y, Ng K, Giovannucci E, Fuchs CS, Ogino S, et al. Statin use and colorectal cancer risk according to molecular subtypes in two large prospective cohort studies. Cancer Prev Res. 2011;4(11):1808–15. https://doi.org/10.1158/1940-6207.CAPR-11-0113.CrossRef

33.

Liao X, Lochhead P, Nishihara R, Morikawa T, Kuchiba A, Yamauchi M, et al. Aspirin use, tumor PIK3CA mutation, and colorectal-cancer survival. N Engl J Med. 2012;367(17):1596–606. https://doi.org/10.1056/NEJMoa1207756.PubMedPubMedCentralCrossRef

34.

Morikawa T, Kuchiba A, Lochhead P, Nishihara R, Yamauchi M, Imamura Y, et al. Prospective analysis of body mass index, physical activity, and colorectal cancer risk associated with beta-catenin (CTNNB1) status. Cancer Res. 2013;73(5):1600–10. https://doi.org/10.1158/0008-5472.CAN-12-2276.PubMedPubMedCentralCrossRef

35.

Nishihara R, Lochhead P, Kuchiba A, Jung S, Yamauchi M, Liao X, et al. Aspirin use and risk of colorectal cancer according to BRAF mutation status. JAMA. 2013;309(24):2563–71. https://doi.org/10.1001/jama.2013.6599.PubMedPubMedCentralCrossRef

36.

Nishihara R, Wang M, Qian ZR, Baba Y, Yamauchi M, Mima K, et al. Alcohol, one-carbon nutrient intake, and risk of colorectal cancer according to tumor methylation level of IGF2 differentially methylated region. Am J Clin Nutr. 2014;100(6):1479–88. https://doi.org/10.3945/ajcn.114.095539.PubMedPubMedCentralCrossRef

37.

Ogino S, Liao X, Chan AT. Aspirin, PIK3CA mutation, and colorectal-cancer survival. N Engl J Med. 2013;368(3):289–90. https://doi.org/10.1056/NEJMc1214189.PubMedCrossRef

38.

Jayasekara H, MacInnis RJ, Williamson EJ, Hodge AM, Clendenning M, Rosty C, et al. Lifetime alcohol intake is associated with an increased risk of KRAS+ and BRAF-/KRAS- but not BRAF+ colorectal cancer. Int J Cancer. 2016;140(7):1485–93. https://doi.org/10.1002/ijc.30568.PubMedCrossRef

39.

• Hughes LA, Williamson EJ, van Engeland M, Jenkins MA, Giles GG, Hopper JL, et al. Body size and risk for colorectal cancers showing BRAF mutations or microsatellite instability: a pooled analysis. Int J Epidemiol. 2012;41(4):1060–72. https://doi.org/10.1093/ije/dys055. This study was the first to successfully pool MPE data when considering risk of molecular endpoints of CRC in relation to lifestyle factors, to improve precision estimates. PubMedCrossRef

40.

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.CrossRef

41.

Luchtenborg M, Weijenberg MP, Kampman E, van Muijen GN, Roemen GM, Zeegers MP, et al. Cigarette smoking and colorectal cancer: APC mutations, hMLH1 expression, and GSTM1 and GSTT1 polymorphisms. Am J Epidemiol. 2005;161(9):806–15. https://doi.org/10.1093/aje/kwi114.PubMedCrossRef

42.

Weijenberg MP, Aardening PW, de Kok TM, de Goeij AF, van den Brandt PA. Cigarette smoking and KRAS oncogene mutations in sporadic colorectal cancer: results from the Netherlands cohort study. Mutat Res. 2008;652(1):54–64. https://doi.org/10.1016/j.mrgentox.2007.12.008.PubMedCrossRef

43.

Bongaerts BW, de Goeij AF, van den Brandt PA, Weijenberg MP. Alcohol and the risk of colon and rectal cancer with mutations in the K-ras gene. Alcohol. 2006;38(3):147–54. https://doi.org/10.1016/j.alcohol.2006.06.003.PubMedCrossRef

44.

Bongaerts BW, de Goeij AF, de Vogel S, van den Brandt PA, Goldbohm RA, Weijenberg MP. Alcohol consumption and distinct molecular pathways to colorectal cancer. Br J Nutr. 2007;97(3):430–4. https://doi.org/10.1017/S0007114507381336.PubMedCrossRef

45.

Hughes LA, Simons CC, van den Brandt PA, Goldbohm RA, de Goeij AF, de Bruine AP, et al. Body size, physical activity and risk of colorectal cancer with or without the CpG island methylator phenotype (CIMP). PLoS One. 2011;6(4):e18571. https://doi.org/10.1371/journal.pone.0018571.PubMedPubMedCentralCrossRef

46.

Hughes LA, van den Brandt PA, de Bruine AP, Wouters KA, Hulsmans S, Spiertz A, et al. Early life exposure to famine and colorectal cancer risk: a role for epigenetic mechanisms. PLoS One. 2009;4(11):e7951. https://doi.org/10.1371/journal.pone.0007951.PubMedPubMedCentralCrossRef

47.

Hogervorst JG, de Bruijn-Geraets D, Schouten LJ, van Engeland M, de Kok TM, Goldbohm RA, et al. Dietary acrylamide intake and the risk of colorectal cancer with specific mutations in KRAS and APC. Carcinogenesis. 2014;35(5):1032–8. https://doi.org/10.1093/carcin/bgu002.PubMedCrossRef

48.

Brink M, Weijenberg MP, De Goeij AF, Schouten LJ, Koedijk FD, Roemen GM, et al. Fat and K-ras mutations in sporadic colorectal cancer in The Netherlands cohort study. Carcinogenesis. 2004;25(9):1619–28. https://doi.org/10.1093/carcin/bgh177.PubMedCrossRef

49.

Weijenberg MP, Luchtenborg M, de Goeij AF, Brink M, van Muijen GN, de Bruine AP, et al. Dietary fat and risk of colon and rectal cancer with aberrant MLH1 expression, APC or KRAS genes. Cancer Causes Control. 2007;18(8):865–79. https://doi.org/10.1007/s10552-007-9032-6.PubMedPubMedCentralCrossRef

50.

de Vogel S, van Engeland M, Luchtenborg M, de Bruine AP, Roemen GM, Lentjes MH, et al. Dietary folate and APC mutations in sporadic colorectal cancer. J Nutr. 2006;136(12):3015–21.PubMed

51.

• Gilsing AM, Fransen F, de Kok TM, Goldbohm AR, Schouten LJ, de Bruine AP, et al. Dietary heme iron and the risk of colorectal cancer with specific mutations in KRAS and APC. Carcinogenesis. 2013;34(12):2757–66. https://doi.org/10.1093/carcin/bgt290. This article presents data from one of the first MPE studies used to test hypotheses with regards to mutagenic effects and CRC. PubMedCrossRef

52.

de Vogel S, Bongaerts BW, Wouters KA, Kester AD, Schouten LJ, de Goeij AF, et al. Associations of dietary methyl donor intake with MLH1 promoter hypermethylation and related molecular phenotypes in sporadic colorectal cancer. Carcinogenesis. 2008;29(9):1765–73. https://doi.org/10.1093/carcin/bgn074.PubMedCrossRef

53.

de Vogel S, Wouters KA, Gottschalk RW, van Schooten FJ, de Goeij AF, de Bruine AP, et al. Dietary methyl donors, methyl metabolizing enzymes, and epigenetic regulators: diet-gene interactions and promoter CpG island hypermethylation in colorectal cancer. Cancer Causes Control. 2011;22(1):1–12. https://doi.org/10.1007/s10552-010-9659-6.PubMedCrossRef

54.

Simons CC, van den Brandt PA, Stehouwer CD, van Engeland M, Weijenberg MP. Body size, physical activity, early-life energy restriction, and associations with methylated insulin-like growth factor-binding protein genes in colorectal cancer. Cancer Epidemiol Biomark Prev. 2014;23(9):1852–62. https://doi.org/10.1158/1055-9965.EPI-13-1285.CrossRef

55.

van Engeland M, Weijenberg MP, Roemen GM, Brink M, de Bruine AP, Goldbohm RA, et al. Effects of dietary folate and alcohol intake on promoter methylation in sporadic colorectal cancer: the Netherlands cohort study on diet and cancer. Cancer Res. 2003;63(12):3133–7.PubMed

56.

Schernhammer ES, Giovannucci E, Baba Y, Fuchs CS, Ogino S. B vitamins, methionine and alcohol intake and risk of colon cancer in relation to BRAF mutation and CpG island methylator phenotype (CIMP). PLoS One. 2011;6(6):e21102. https://doi.org/10.1371/journal.pone.0021102.PubMedPubMedCentralCrossRef

57.

Schernhammer ES, Giovannucci E, Kawasaki T, Rosner B, Fuchs CS, Ogino S. Dietary folate, alcohol and B vitamins in relation to LINE-1 hypomethylation in colon cancer. Gut. 2010;59(6):794–9. https://doi.org/10.1136/gut.2009.183707.PubMedCrossRef

58.

Limsui D, Vierkant RA, Tillmans LS, Wang AH, Weisenberger DJ, Laird PW, et al. Cigarette smoking and colorectal cancer risk by molecularly defined subtypes. J Natl Cancer Inst. 2010;102(14):1012–22. https://doi.org/10.1093/jnci/djq201.PubMedPubMedCentralCrossRef

59.

Hoffmeister M, Blaker H, Kloor M, Roth W, Toth C, Herpel E, et al. Body mass index and microsatellite instability in colorectal cancer: a population-based study. Cancer Epidemiol Biomark Prev. 2013;22(12):2303–11. https://doi.org/10.1158/1055-9965.EPI-13-0239.CrossRef

60.

Curtin K, Samowitz WS, Wolff RK, Herrick J, Caan BJ, Slattery ML. Somatic alterations, metabolizing genes and smoking in rectal cancer. Int J Cancer. 2009;125(1):158–64. https://doi.org/10.1002/ijc.24338.PubMedPubMedCentralCrossRef

61.

Samowitz WS, Albertsen H, Sweeney C, Herrick J, Caan BJ, Anderson KE, et al. Association of smoking, CpG island methylator phenotype, and V600E BRAF mutations in colon cancer. J Natl Cancer Inst. 2006;98(23):1731–8. https://doi.org/10.1093/jnci/djj468.PubMedCrossRef

62.

Slattery ML, Curtin K, Anderson K, Ma KN, Ballard L, Edwards S, et al. Associations between cigarette smoking, lifestyle factors, and microsatellite instability in colon tumors. J Natl Cancer Inst. 2000;92(22):1831–6. https://doi.org/10.1093/jnci/92.22.1831.PubMedCrossRef

63.

Slattery ML, Anderson K, Curtin K, Ma KN, Schaffer D, Samowitz W. Dietary intake and microsatellite instability in colon tumors. Int J Cancer. 2001;93(4):601–7. https://doi.org/10.1002/ijc.1370.PubMedCrossRef

64.

Slattery ML, Curtin K, Sweeney C, Levin TR, Potter J, Wolff RK, et al. Diet and lifestyle factor associations with CpG island methylator phenotype and BRAF mutations in colon cancer. Int J Cancer. 2007;120(3):656–63. https://doi.org/10.1002/ijc.22342.PubMedCrossRef

65.

Poynter JN, Haile RW, Siegmund KD, Campbell PT, Figueiredo JC, Limburg P, et al. Associations between smoking, alcohol consumption, and colorectal cancer, overall and by tumor microsatellite instability status. Cancer Epidemiol Biomark Prev. 2009;18(10):2745–50. https://doi.org/10.1158/1055-9965.EPI-09-0517.CrossRef

66.

Diergaarde B, van Geloof WL, van Muijen GN, Kok FJ, Kampman E. Diet and truncating APC mutations in sporadic colon tumours. IARC Sci Publ. 2002;156:505–6.PubMed

67.

Diergaarde B, Braam H, van Muijen GN, Ligtenberg MJ, Kok FJ, Kampman E. Dietary factors and microsatellite instability in sporadic colon carcinomas. Cancer Epidemiol Biomark Prev. 2003;12(11 Pt 1):1130–6.

68.

Diergaarde B, van Geloof WL, van Muijen GN, Kok FJ, Kampman E. Dietary factors and the occurrence of truncating APC mutations in sporadic colon carcinomas: a Dutch population-based study. Carcinogenesis. 2003;24(2):283–90. https://doi.org/10.1093/carcin/24.2.283.PubMedCrossRef

69.

Bautista D, Obrador A, Moreno V, Cabeza E, Canet R, Benito E, et al. Ki-ras mutation modifies the protective effect of dietary monounsaturated fat and calcium on sporadic colorectal cancer. Cancer Epidemiol Biomark Prev. 1997;6(1):57–61.

70.

Martinez F, Fernandez-Martos C, Quintana MJ, Castells A, Llombart A, Iniguez F, et al. APC and KRAS mutations in distal colorectal polyps are related to smoking habits in men: results of a cross-sectional study. Clin Transl Oncol. 2011;13(9):664–71. https://doi.org/10.1007/s12094-011-0712-z.PubMedCrossRef

71.

Dahlin AM, Palmqvist R, Henriksson ML, Jacobsson M, Eklof V, Rutegard J, et al. The role of the CpG island methylator phenotype in colorectal cancer prognosis depends on microsatellite instability screening status. Clin Cancer Res. 2010;16(6):1845–55. https://doi.org/10.1158/1078-0432.CCR-09-2594.PubMedCrossRef

72.

Diergaarde B, Vrieling A, van Kraats AA, van Muijen GN, Kok FJ, Kampman E. Cigarette smoking and genetic alterations in sporadic colon carcinomas. Carcinogenesis. 2003;24(3):565–71. https://doi.org/10.1093/carcin/24.3.565.PubMedCrossRef

73.

Botteri E, Iodice S, Bagnardi V, Raimondi S, Lowenfels AB, Maisonneuve P. Smoking and colorectal cancer: a meta-analysis. JAMA. 2008;300(23):2765–78. https://doi.org/10.1001/jama.2008.839.PubMedCrossRef

74.

De Sousa EMF, Wang X, Jansen M, Fessler E, Trinh A, de Rooij LP, et al. Poor-prognosis colon cancer is defined by a molecularly distinct subtype and develops from serrated precursor lesions. Nat Med. 2013;19(5):614–8. https://doi.org/10.1038/nm.3174.CrossRef

75.

Hughes LA, Khalid-de Bakker CA, Smits KM, van den Brandt PA, Jonkers D, Ahuja N, et al. The CpG island methylator phenotype in colorectal cancer: progress and problems. Biochim Biophys Acta. 2012;1825(1):77–85. https://doi.org/10.1016/j.bbcan.2011.10.005.PubMed

76.

Hughes LA, Melotte V, de Schrijver J, de Maat M, Smit VT, Bovee JV, et al. The CpG island methylator phenotype: what's in a name? Cancer Res. 2013;73(19):5858–68. https://doi.org/10.1158/0008-5472.CAN-12-4306.PubMedCrossRef

Title: Lifestyle, Diet, and Colorectal Cancer Risk According to (Epi)genetic Instability: Current Evidence and Future Directions of Molecular Pathological Epidemiology
Authors: Laura A. E. Hughes
Colinda C. J. M. Simons
Piet A. van den Brandt
Manon van Engeland
Matty P. Weijenberg
Publication date: 01-12-2017
Publisher: Springer US
Published in: Current Colorectal Cancer Reports / Issue 6/2017
Print ISSN: 1556-3790
Electronic ISSN: 1556-3804
DOI: https://doi.org/10.1007/s11888-017-0395-0

Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Watch now

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras

Prof. Fabrice Barlesi

Developed by: Springer Medicine

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Purpose of Review

Recent Findings

Summary

Please log in to get access to this content

Other articles of this Issue 6/2017

Liver Imaging for Colorectal Cancer Metastases

Dietary Patterns and Colorectal Cancer Risk: a Review of 17 Years of Evidence (2000–2016)

Author Correction: Chemoprevention of Colorectal Cancer in High-Risk Patients: from Molecular Targets to Clinical Trials

Second-Line Therapy for Advanced Colorectal Cancer: EGFR vs. Continuation of VEGF Inhibition

Conversion Therapy for Initially Borderline/Unresectable Metastases in Colon Cancer: What Is the Best Neoadjuvant Chemotherapy?

Diet, Gut Microbiota, and Colorectal Cancer Prevention: a Review of Potential Mechanisms and Promising Targets for Future Research

Keynote webinar | Spotlight on antibody–drug conjugates in cancer