The Interaction between Dietary Fiber and Fat and Risk of Colorectal Cancer in the Women’s Health Initiative

Combined intakes of specific dietary fiber and fat subtypes protect against colon cancer in animal models. We evaluated associations between self-reported individual and combinations of fiber (insoluble, soluble, and pectins, specifically) and fat (omega-6, omega-3, and docosahexaenoic acid (DHA) and eicosapentaenoic acid (EPA), specifically) and colorectal cancer (CRC) risk in the Women’s Health Initiative prospective cohort (n = 134,017). During a mean 11.7 years (1993–2010), 1952 incident CRC cases were identified. Cox regression models computed multivariate adjusted hazard ratios to estimate the association between dietary factors and CRC risk. Assessing fiber and fat individually, there was a modest trend for lower CRC risk with increasing intakes of total and insoluble fiber (p-trend 0.09 and 0.08). An interaction (p = 0.01) was observed between soluble fiber and DHA + EPA, with protective effects of DHA + EPA with lower intakes of soluble fiber and an attenuation at higher intakes, however this association was no longer significant after correction for multiple testing. These results suggest a modest protective effect of higher fiber intake on CRC risk, but not in combination with dietary fat subtypes. Given the robust results in preclinical models and mixed results in observational studies, controlled dietary interventions with standardized intakes are needed to better understand the interaction of specific fat and fiber subtypes on colon biology and ultimately CRC susceptibility in humans.

[1]  S. Serini,et al.  Long-chain n-3 PUFA against breast and prostate cancer: Which are the appropriate doses for intervention studies in animals and humans? , 2017, Critical reviews in food science and nutrition.

[2]  J. Meyerhardt,et al.  Marine ω-3 polyunsaturated fatty acid intake and survival after colorectal cancer diagnosis , 2016, Gut.

[3]  Ahmad Esmaillzadeh,et al.  Cereal fibre intake and risk of mortality from all causes, CVD, cancer and inflammatory diseases: a systematic review and meta-analysis of prospective cohort studies. , 2016, The British journal of nutrition.

[4]  L. Hou,et al.  Diet Quality and Colorectal Cancer Risk in the Women's Health Initiative Observational Study. , 2016, American journal of epidemiology.

[5]  N. Parekh,et al.  Consumption of whole grains and cereal fiber in relation to cancer risk: a systematic review of longitudinal studies. , 2016, Nutrition reviews.

[6]  E. Riboli,et al.  Pre-diagnostic meat and fibre intakes in relation to colorectal cancer survival in the European Prospective Investigation into Cancer and Nutrition. , 2016, The British journal of nutrition.

[7]  F. Ricceri,et al.  Dietary Total Antioxidant Capacity and Colorectal Cancer in the Italian EPIC Cohort , 2015, PloS one.

[8]  S. Berndt,et al.  Dietary fiber intake and risk of colorectal cancer and incident and recurrent adenoma in the Prostate, Lung, Colorectal, and Ovarian Cancer Screening Trial. , 2015, The American journal of clinical nutrition.

[9]  O. Franco,et al.  Dietary Fiber Intake Modifies the Positive Association between n-3 PUFA Intake and Colorectal Cancer Risk in a Caucasian Population. , 2015, The Journal of nutrition.

[10]  M. Orlich,et al.  Vegetarian dietary patterns and the risk of colorectal cancers. , 2015, JAMA internal medicine.

[11]  R. Chapkin,et al.  Chemoprotective Epigenetic Mechanisms in a Colorectal Cancer Model: Modulation by n-3 PUFA in Combination With Fermentable Fiber , 2015, Current Pharmacology Reports.

[12]  Leo Lahti,et al.  Fat, Fiber and Cancer Risk in African Americans and Rural Africans , 2015, Nature Communications.

[13]  Shan Wang,et al.  Fiber consumption and all-cause, cardiovascular, and cancer mortalities: a systematic review and meta-analysis of cohort studies. , 2015, Molecular nutrition & food research.

[14]  D. Mozaffarian,et al.  Dietary intake of fish, ω‐3 and ω‐6 fatty acids and risk of colorectal cancer: A prospective study in U.S. men and women , 2014, International journal of cancer.

[15]  Johanna W Lampe,et al.  Long-Chain Omega-3 Polyunsaturated Fatty Acid Intake and Risk of Colorectal Cancer , 2014, Nutrition and cancer.

[16]  A. Qian,et al.  Dietary fiber intake reduces risk for colorectal adenoma: a meta-analysis. , 2014, Gastroenterology.

[17]  H. Rasmussen,et al.  Position of the academy of nutrition and dietetics: dietary fatty acids for healthy adults. , 2014, Journal of the Academy of Nutrition and Dietetics.

[18]  S. Bultman.  Molecular Pathways: Gene–Environment Interactions Regulating Dietary Fiber Induction of Proliferation and Apoptosis via Butyrate for Cancer Prevention , 2013, Clinical Cancer Research.

[19]  E. Negri,et al.  Dietary total antioxidant capacity and colorectal cancer: A large case–control study in Italy , 2013, International journal of cancer.

[20]  Amy M. Sheflin,et al.  Stool Microbiome and Metabolome Differences between Colorectal Cancer Patients and Healthy Adults , 2013, PloS one.

[21]  G. Gao,et al.  Dysbiosis Signature of Fecal Microbiota in Colorectal Cancer Patients , 2013, Microbial Ecology.

[22]  R. Chapkin,et al.  Inhibitory effects of omega-3 fatty acids on injury-induced epidermal growth factor receptor transactivation contribute to delayed wound healing. , 2013, American journal of physiology. Cell physiology.

[23]  T. van de Wiele,et al.  Gut metabotypes govern health effects of dietary polyphenols. , 2013, Current opinion in biotechnology.

[24]  S. Azer.  Overview of molecular pathways in inflammatory bowel disease associated with colorectal cancer development , 2013, European journal of gastroenterology & hepatology.

[25]  Wei Sun,et al.  The Warburg effect dictates the mechanism of butyrate-mediated histone acetylation and cell proliferation. , 2012, Molecular cell.

[26]  G. Jahreis,et al.  Survey of n-3 and n-6 polyunsaturated fatty acids in fish and fish products , 2012, Lipids in Health and Disease.

[27]  Jesse R. Zaneveld,et al.  Identifying genomic and metabolic features that can underlie early successional and opportunistic lifestyles of human gut symbionts , 2012, Genome research.

[28]  S. Bultman,et al.  Metaboloepigenetics: Interrelationships between energy metabolism and epigenetic control of gene expression , 2012, Journal of cellular physiology.

[29]  A. Vaculová,et al.  Docosahexaenoic fatty acid (DHA) in the regulation of colon cell growth and cell death: a review. , 2012, Biomedical papers of the Medical Faculty of the University Palacky, Olomouc, Czechoslovakia.

[30]  J. Raes,et al.  Microbial interactions: from networks to models , 2012, Nature Reviews Microbiology.

[31]  Jennifer M. Brulc,et al.  454 pyrosequencing reveals a shift in fecal microbiota of healthy adult men consuming polydextrose or soluble corn fiber. , 2012, The Journal of nutrition.

[32]  Curtis Huttenhower,et al.  Microbial Co-occurrence Relationships in the Human Microbiome , 2012, PLoS Comput. Biol..

[33]  F. Clavel-Chapelon,et al.  Dietary Fibre Intake and Risks of Cancers of the Colon and Rectum in the European Prospective Investigation into Cancer and Nutrition (EPIC) , 2012, PloS one.

[34]  Shuang-yin Han,et al.  Fish consumption and colorectal cancer risk in humans: a systematic review and meta-analysis. , 2012, The American journal of medicine.

[35]  M. Gerber.  Omega-3 fatty acids and cancers: a systematic update review of epidemiological studies , 2012, British Journal of Nutrition.

[36]  A. Bhatnagar,et al.  Ras Signaling Pathway in the Chemopreventive Action of Different Ratios of Fish Oil and Corn Oil in Experimentally Induced Colon Carcinogenesis , 2012, Nutrition and cancer.

[37]  W. Verbeke,et al.  Consumer implications of the WCRF's permanent update on colorectal cancer. , 2012, Meat science.

[38]  J. Lindon,et al.  Stability and robustness of human metabolic phenotypes in response to sequential food challenges. , 2012, Journal of proteome research.

[39]  Liping Zhao,et al.  Structural segregation of gut microbiota between colorectal cancer patients and healthy volunteers , 2011, The ISME Journal.

[40]  J. Lupton,et al.  Interactive effects of fatty acid and butyrate‐induced mitochondrial Ca2+ loading and apoptosis in colonocytes , 2011, Cancer.

[41]  R. Lau,et al.  Dietary fibre, whole grains, and risk of colorectal cancer: systematic review and dose-response meta-analysis of prospective studies , 2011, BMJ : British Medical Journal.

[42]  A. Simopoulos.  Importance of the omega-6/omega-3 balance in health and disease: evolutionary aspects of diet. , 2011, World review of nutrition and dietetics.

[43]  R. Lau,et al.  Nonlinear reduction in risk for colorectal cancer by fruit and vegetable intake based on meta-analysis of prospective studies. , 2011, Gastroenterology.

[44]  R. Carroll,et al.  A chemoprotective fish oil- and pectin-containing diet temporally alters gene expression profiles in exfoliated rat colonocytes throughout oncogenesis. , 2011, The Journal of nutrition.

[45]  P. Bork,et al.  Enterotypes of the human gut microbiome , 2011, Nature.

[46]  Wei Sun,et al.  The microbiome and butyrate regulate energy metabolism and autophagy in the mammalian colon. , 2011, Cell metabolism.

[47]  J. Lupton,et al.  Dietary Fish Oil Promotes Colonic Apoptosis and Mitochondrial Proton Leak in Oxidatively Stressed Mice , 2011, Cancer Prevention Research.

[48]  M. Hull,et al.  Omega-3 polyunsaturated fatty acids for the treatment and prevention of colorectal cancer , 2011, Gut.

[49]  Stephen J. Bruce,et al.  A whole-grain cereal-rich diet increases plasma betaine, and tends to decrease total and LDL-cholesterol compared with a refined-grain diet in healthy subjects , 2011, British Journal of Nutrition.

[50]  Y. Kakeji,et al.  Dietary fiber, source foods and colorectal cancer risk: the Fukuoka Colorectal Cancer Study , 2010, Scandinavian journal of gastroenterology.

[51]  J. Barnholtz-Sloan,et al.  Dietary fatty acids, luminal modifiers, and risk of colorectal cancer , 2010, International journal of cancer.

[52]  A. Jemal,et al.  Annual report to the nation on the status of cancer, 1975‐2006, featuring colorectal cancer trends and impact of interventions (risk factors, screening, and treatment) to reduce future rates , 2010, Cancer.

[53]  Robin P Boushey,et al.  Colorectal cancer epidemiology: incidence, mortality, survival, and risk factors. , 2009, Clinics in colon and rectal surgery.

[54]  M. Thun,et al.  Dietary Intake of ω-6 and ω-3 Fatty Acids and Risk of Colorectal Cancer in a Prospective Cohort of U.S. Men and Women , 2009, Cancer Epidemiology Biomarkers & Prevention.

[55]  J. Lupton,et al.  Upregulation of p21Waf1/Cip1 expression in vivo by butyrate administration can be chemoprotective or chemopromotive depending on the lipid component of the diet. , 2008, Carcinogenesis.

[56]  J. Lupton,et al.  Mechanisms by which docosahexaenoic acid and related fatty acids reduce colon cancer risk and inflammatory disorders of the intestine. , 2008, Chemistry and physics of lipids.

[57]  R J Carroll,et al.  Dietary fish oil and pectin enhance colonocyte apoptosis in part through suppression of PPARdelta/PGE2 and elevation of PGE3. , 2008, Carcinogenesis.

[58]  P. van’t Veer,et al.  Fish consumption, n-3 fatty acids, and colorectal cancer: a meta-analysis of prospective cohort studies. , 2007, American journal of epidemiology.

[59]  P. G. Reeves,et al.  Pinto bean consumption changes SCFA profiles in fecal fermentations, bacterial populations of the lower bowel, and lipid profiles in blood of humans. , 2007, The Journal of nutrition.

[60]  V. Fogliano,et al.  Whole-grain wheat breakfast cereal has a prebiotic effect on the human gut microbiota: a double-blind, placebo-controlled, crossover study , 2007, British Journal of Nutrition.

[61]  J. Lupton,et al.  Synergy between docosahexaenoic acid and butyrate elicits p53-independent apoptosis via mitochondrial Ca(2+) accumulation in colonocytes. , 2007, American journal of physiology. Gastrointestinal and liver physiology.

[62]  A. Schatzkin,et al.  Dietary fiber and whole-grain consumption in relation to colorectal cancer in the NIH-AARP Diet and Health Study. , 2007, The American journal of clinical nutrition.

[63]  A. Tamakoshi,et al.  Dietary Fiber and Risk of Colorectal Cancer in the Japan Collaborative Cohort Study , 2007, Cancer Epidemiology Biomarkers & Prevention.

[64]  J. Lupton,et al.  Docosahexaenoic acid and butyrate synergistically induce colonocyte apoptosis by enhancing mitochondrial calcium accumulation , 2007, Cancer research.

[65]  Wcr Fund.  Food, Nutrition, Physical Activity, and the Prevention of Cancer: a Global Perspective , 2007 .

[66]  Stuart K Johnson,et al.  Lupin kernel fiber consumption modifies fecal microbiota in healthy men as determined by rRNA gene fluorescent in situ hybridization , 2006, European journal of nutrition.

[67]  J. Manson,et al.  Low-fat dietary pattern and risk of colorectal cancer: the Women's Health Initiative Randomized Controlled Dietary Modification Trial. , 2006, JAMA.

[68]  Stuart K Johnson,et al.  Lupin kernel fibre foods improve bowel function and beneficially modify some putative faecal risk factors for colon cancer in men , 2006, British Journal of Nutrition.

[69]  R. Burger,et al.  Use of a dummy (pacifier) during sleep and risk of sudden infant death syndrome (SIDS): population based case-control study , 2005, BMJ : British Medical Journal.

[70]  W. Willett,et al.  Dietary fiber intake and risk of colorectal cancer: a pooled analysis of prospective cohort studies. , 2005, JAMA.

[71]  J. Lupton,et al.  The role of docosahexaenoic acid in mediating mitochondrial membrane lipid oxidation and apoptosis in colonocytes. , 2005, Carcinogenesis.

[72]  G. Young,et al.  Dietary fibre and colorectal cancer: a model for environment--gene interactions. , 2005, Molecular nutrition & food research.

[73]  W. Willett,et al.  Fiber Intake and Incidence of Colorectal Cancer among 76,947 Women and 47,279 Men , 2005, Cancer Epidemiology Biomarkers & Prevention.

[74]  Joanne L Slavin,et al.  Dietary fiber and body weight. , 2005, Nutrition.

[75]  R. Carroll,et al.  Biochemical and Molecular Actions of Nutrients An Increase in Reactive Oxygen Species by Dietary Fish Oil Coupled with the Attenuation of Antioxidant Defenses by Dietary Pectin Enhances Rat Colonocyte Apoptosis , 2004 .

[76]  C. Gluud,et al.  Antioxidant supplements for prevention of gastrointestinal cancers: a systematic review and meta-analysis , 2004, The Lancet.

[77]  Magnus Ingelman-Sundberg,et al.  Dietary long-chain n-3 fatty acids for the prevention of cancer: a review of potential mechanisms. , 2004, The American journal of clinical nutrition.

[78]  Garnet L Anderson,et al.  The Women's Health Initiative recruitment methods and results. , 2003, Annals of epidemiology.

[79]  R. Langer,et al.  The Women's Health Initiative Observational Study: baseline characteristics of participants and reliability of baseline measures. , 2003, Annals of epidemiology.

[80]  Scott Davis,et al.  Implementation of the Women's Health Initiative study design. , 2003, Annals of epidemiology.

[81]  C. Kooperberg,et al.  Outcomes ascertainment and adjudication methods in the Women's Health Initiative. , 2003, Annals of epidemiology.

[82]  A. Kristal,et al.  Dietary supplement use and medical conditions: the VITAL study. , 2003, American journal of preventive medicine.

[83]  P. Trumbo,et al.  Dietary reference intakes for energy, carbohydrate, fiber, fat, fatty acids, cholesterol, protein and amino acids. , 2002, Journal of the American Dietetic Association.

[84]  C. la Vecchia,et al.  Dietary fibre and the risk of colorectal cancer. , 2001, European journal of cancer.

[85]  G. Gibson,et al.  The prebiotic effects of biscuits containing partially hydrolysed guar gum and fructo-oligosaccharides – a human volunteer study , 2001, British Journal of Nutrition.

[86]  R. Butrum.  American Institute for Cancer Research , 2000 .

[87]  A. Kristal,et al.  Measurement characteristics of the Women's Health Initiative food frequency questionnaire. , 1999, Annals of epidemiology.

[88]  W. Willett,et al.  Dietary fiber and the risk of colorectal cancer and adenoma in women. , 1999, The New England journal of medicine.

[89]  C. la Vecchia,et al.  Fiber intake and risk of colorectal cancer. , 1998, Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology.

[90]  A. Gostner,et al.  Effects of resistant starch on the colon in healthy volunteers: possible implications for cancer prevention. , 1998, The American journal of clinical nutrition.

[91]  JoAnn E. Manson,et al.  Design of the Women's Health Initiative clinical trial and observational study. The Women's Health Initiative Study Group. , 1998, Controlled clinical trials.

[92]  J. Lupton,et al.  Dietary Fat and Fiber Modulate the Effect of Carcinogen on Colonic Protein Kinase C λ Expression in Rats , 1997 .

[93]  L. Kolonel,et al.  Dietary Fiber and Colorectal Cancer Risk , 1997, Epidemiology.

[94]  J. Lupton,et al.  Predictive Value of Proliferation, Differentiation and Apoptosis as Intermediate Markers for Colon Tumorigenesis , 2022 .

[95]  G A Colditz,et al.  Relation of meat, fat, and fiber intake to the risk of colon cancer in a prospective study among women. , 1990, The New England journal of medicine.

[96]  Sheila A Bingham.  Diet and Large Bowel Cancer , 1990, Journal of the Royal Society of Medicine.

[97]  J. Freudenheim,et al.  Risks associated with source of fiber and fiber components in cancer of the colon and rectum. , 1990, Cancer research.

[98]  B. Trock,et al.  Dietary fiber, vegetables, and colon cancer: critical review and meta-analyses of the epidemiologic evidence. , 1990, Journal of the National Cancer Institute.