Co-consumption of Vegetables and Fruit, Whole Grains, and Fiber Reduces the Cancer Risk of Red and Processed Meat in a Large Prospective Cohort of Adults from Alberta's Tomorrow Project

Katerina Maximova, Elham Khodayari Moez, Julia Dabravolskaj, Alexa R Ferdinands, Irina Dinu, Geraldine Lo Siou, Ala Al Rajabi, Paul J Veugelers, Katerina Maximova, Elham Khodayari Moez, Julia Dabravolskaj, Alexa R Ferdinands, Irina Dinu, Geraldine Lo Siou, Ala Al Rajabi, Paul J Veugelers

Abstract

We examined whether co-consumption of red and processed meat with key foods items and food constituents recommended for cancer prevention (vegetables and fruit, whole grains, and fiber) mitigates cancer incidence. In a prospective cohort of 26,218 adults aged 35-69 years at baseline, dietary intake was collected through 124-item past-year food frequency questionnaire. Incidence of all-cause and 15 cancers previously linked to red and processed meat intake was obtained through data linkage with a cancer registry (average follow-up 13.5 years). Competing risk Cox Proportional Hazard models estimated cancer risk and Accelerated Failure Time models estimated time-to-cancer occurrence for different combinations of intake levels while considering mortality from vital statistics and established confounders. Co-consumption of low vegetables and fruit intake with high processed meat was associated with higher incidence of all-cause and 15 cancers (men: HR = 1.85, 1.91; women: HR = 1.44, 1.49) and accelerated time-to-cancer occurrence (men: 6.5 and 7.1 years and women: 5.6 and 6.3 years, respectively), compared to high vegetables and fruit with low processed meat intake. Less pronounced and less consistent associations were observed for whole grains and fiber and for red meat. The findings provide initial evidence toward refining existing cancer prevention recommendations to optimize the intake and combination of foods in the general adult population.

Keywords: cancer prevention; fiber; healthy eating; processed meat; red meat; vegetables and fruit; whole grains.

Conflict of interest statement

The authors have no conflicts of interest relevant to this article to disclose.

References

    1. Continuous Update Project Report: Diet, Nutrition, Physical Activity and Cancer: A Global Perspective (Third Expert Report Edition) [(accessed on 27 June 2020)]; Available online: .
    1. Bluher M. Obesity: Global epidemiology and pathogenesis. Nat. Rev. Endocrinol. 2019;15:288–298. doi: 10.1038/s41574-019-0176-8.
    1. Guthold R., Stevens G.A., Riley L.M., Bull F.C. Worldwide trends in insufficient physical activity from 2001 to 2016: A pooled analysis of 358 population-based surveys with 1.9 million participants. Lancet Glob. Health. 2018;6:e1077–e1086. doi: 10.1016/S2214-109X(18)30357-7.
    1. Micha R., Khatibzadeh S., Shi P., Andrews K.G., Engell R.E., Mozaffarian D. Global, regional and national consumption of major food groups in 1990 and 2010: A systematic analysis including 266 country-specific nutrition surveys worldwide. BMJ Open. 2015;5:e008705. doi: 10.1136/bmjopen-2015-008705.
    1. McAfee A.J., McSorley E.M., Cuskelly G.J., Moss B.W., Wallace J.M.W., Bonham M.P., Fearon A.M. Red meat consumption: An overview of the risks and benefits. Meat Sci. 2010;84:1–13. doi: 10.1016/j.meatsci.2009.08.029.
    1. Bouvard V., Loomis D., Guyton K.Z., Grosse Y., El Ghissassi F., Benbrahim-Tallaa L., Guha N., Mattock H., Straif K., International Agency for Research on Cancer Monograph Working Group Carcinogenicity of consumption of red and processed meat. Lancet Oncol. 2015;16:1599–1600. doi: 10.1016/S1470-2045(15)00444-1.
    1. Truswell A.S. Problems with red meat in the WCRF2. Am. J. Clin. Nutr. 2009;89:1274–1275. doi: 10.3945/ajcn.2008.27201.
    1. Lauber S.N., Gooderharn N.J. The cooked meat-derived genotoxic carcinogen 2-Amino-3-Methylimidazo 4,5-b Pyridine has potent hormone-like activity: Mechanistic support for a role in breast cancer. Cancer Res. 2007;67:9597–9602. doi: 10.1158/0008-5472.CAN-07-1661.
    1. Sanz Alaejos M., Afonso A.M. Factors That Affect the Content of Heterocyclic Aromatic Amines in Foods. Compr. Rev. Food Sci. Food Saf. 2011;10:52–108. doi: 10.1111/j.1541-4337.2010.00141.x.
    1. Alomirah H., Al-Zenki S., Al-Hooti S., Zaghloul S., Sawaya W., Ahmed N., Kannan K. Concentrations and dietary exposure to polycyclic aromatic hydrocarbons (PAHs) from grilled and smoked foods. Food Control. 2011;22:2028–2035. doi: 10.1016/j.foodcont.2011.05.024.
    1. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans. [(accessed on 27 June 2020)]; Available online: .
    1. Norat T., Scoccianti C., Boutron-Ruault M.C., Anderson A., Berrino F., Cecchini M., Espina C., Key T., Leitzmann M., Powers H., et al. European Code against Cancer 4th Edition: Diet and cancer. Cancer Epidemiol. 2015;39:S56–S66. doi: 10.1016/j.canep.2014.12.016.
    1. Robson P.J., Solbak N.M., Haig T.R., Whelan H.K., Vena J.E., AK A., Rosner W.K., Darren R., Brenner D.R., Cook L.S., et al. Cohort profile: Design, methods, and demographics from phase I of Alberta’s Tomorrow Project cohort. CMAJ Open. 2016;4:E515–E527. doi: 10.9778/cmajo.20160005.
    1. Bryant H., Robson P., Ullman R., Friedenreich C.M., Dawe U. Population-based cohort development in Alberta, Canada: A feasibility study. Chronic Dis. Can. 2006;27:55–63.
    1. North American Association of Central Cancer Registries—Certification Levels. [(accessed on 20 September 2016)]; Available online: .
    1. National Institutes of Health . Diet History Questionnaire. National Institutes of Health; Washington, DC, USA: 2007. [(accessed on 30 August 2016)]. Available online:
    1. Csizmadi I., Boucher B., Lo Siou G., Massarrelli I., Rondeau I., Garriguet D., Koushik A., Elenko J., Subar A.F. Using national dietary intake data to evaluate and adapt the US Diet History Questionnaire: The stepwise tailoring of an FFQ for Canadian use. Public Health Nutr. 2016;28:1–9. doi: 10.1017/S1368980016001506.
    1. Csizmadi I., Kahle L., Ullman R., Dawe U., Zimmerman T.P., Friedenreich C.M., Bryant H., Subar A.F. Adaptation and evaluation of the National Cancer Institute’s Diet History Questionnaire and nutrient database for Canadian populations. Public Health Nutr. 2007;10:88–96. doi: 10.1017/S1368980007184287.
    1. Health Canada Eating Well with Canada’s Food Guide. [(accessed on 27 June 2020)]; Available online: .
    1. Canadian Cancer Society Eat well. [(accessed on 27 June 2020)]; Available online: .
    1. U.S. Department of Health and Human Services. U.S. Department of Agriculture [(accessed on 27 June 2020)];2015–2020 Dietary Guidelines for Americans. (8th ed.). 2015 Available online:
    1. Oladimeji O. Global, regional, and national comparative risk assessment of 79 behavioural, environmental and occupational, and metabolic risks or clusters of risks, 1990–2015: A systematic analysis for the Global Burden of Disease Study. 2015. Lancet. 2016;388:1659–1724.
    1. Aune D., Chan D.S.M., Vieira A.R., Rosenblatt D.A.N., Vieira R., Greenwood D.C., Kampman E., Norat T. Red and processed meat intake and risk of colorectal adenomas: A systematic review and meta-analysis of epidemiological studies. Cancer Causes Control. 2013;24:611–627. doi: 10.1007/s10552-012-0139-z.
    1. Chan D.S.M., Lau R., Aune D., Vieira R., Greenwood D.C., Kampman E., Norat T. Red and Processed Meat and Colorectal Cancer Incidence: Meta-Analysis of Prospective Studies. PLoS ONE. 2011;66:e20456. doi: 10.1371/journal.pone.0020456.
    1. Friedenreich C.M., Courneya K.S., Neilson H.K., Matthews C.E., Willis G., Irwin M., Troiano R., Ballard-Barbash R. Reliability and validity of the Past Year Total Physical Activity Questionnaire. Am. J. Epidemiol. 2006;163:959–970. doi: 10.1093/aje/kwj112.
    1. Willett W. Nutritional Epidemiology. 3rd ed. Oxford University Press; Oxford, UK: 2012.
    1. Zhou B., Latouche A., Rocha V., Fine J. Competing risks regression for stratified data. Biometrics. 2011;67:661–670. doi: 10.1111/j.1541-0420.2010.01493.x.
    1. Fine J.P., Gray R.J. A Proportional Hazards Model for the Subdistribution of a Competing Risk. J. Am. Stat. Assoc. 1999;94:496–509. doi: 10.1080/01621459.1999.10474144.
    1. Zhou B., Fine J., Laird G. Goodness-of-fit test for proportional subdistribution hazards model. Stat. Med. 2013;32:3804–3811. doi: 10.1002/sim.5815.
    1. Austin P.C., Lee D.S., Fine J.P. Introduction to the Analysis of Survival Data in the Presence of Competing Risks. Circulation. 2016;133:601–609. doi: 10.1161/CIRCULATIONAHA.115.017719.
    1. Hutton J.L., Monaghan P.F. Choice of parametric accelerated life and proportional hazards models for survival data: Asymptotic results. Lifetime Data Anal. 2002;8:375–393. doi: 10.1023/A:1020570922072.
    1. Bagdonavicius V., Nikulin M. Accelerated Life Models. Modeling and Statistical Analysis. Chapman & Hall/CRC; Boca Raton, FL, USA: 2002.
    1. Orbe J., Ferreira E., Nunez-Anton V. Comparing proportional hazards and accelerated failure time models for survival analysis. Stat. Med. 2002;21:3493–3510. doi: 10.1002/sim.1251.
    1. Swindell W.R. Accelerated failure time models provide a useful statistical framework for aging research. Exp. Gerontol. 2009;44:190–200. doi: 10.1016/j.exger.2008.10.005.
    1. Shen Y., Ning J., Qin J. Analyzing Length-biased Data with Semiparametric Transformation and Accelerated Failure Time Models. J. Am. Stat. Assoc. 2009;104:1192–1202. doi: 10.1198/jasa.2009.tm08614.
    1. Liu X. Survival Analysis: Models and Applications. John Wiley & Sons Ltd; Chichester, UK: Higher Education Press; Beijing, China: 2012.
    1. Diallo A., Deschasaux M., Latino-Martel P., Hercberg S., Galan P., Fassier P., Alles B., Gueraud F., Pierre F.H., Touvier M. Red and processed meat intake and cancer risk: Results from the prospective NutriNet-Sante cohort study. Int. J. Cancer. 2018;142:230–237. doi: 10.1002/ijc.31046.
    1. Arthur R., Kirsh V.A., Kreiger N., Rohan T. A healthy lifestyle index and its association with risk of breast, endometrial, and ovarian cancer among Canadian women. Cancer Causes Control. 2018;29:485–493. doi: 10.1007/s10552-018-1032-1.
    1. Romaguera D., Vergnaud A.C., Peeters P.H., van Gils C.H., Chan D.S., Ferrari P., Romieu I., Jenab M., Slimani N., Clavel-Chapelon F., et al. Is concordance with World Cancer Research Fund/American Institute for Cancer Research guidelines for cancer prevention related to subsequent risk of cancer? Results from the EPIC study. Am. J. Clin. Nutr. 2012;96:150–163. doi: 10.3945/ajcn.111.031674.
    1. Leroy F., Cofnas N. Should dietary guidelines recommend low red meat intake? Crit. Rev. Food Sci. Nutr. 2019 doi: 10.1080/10408398.2019.1657063.
    1. Fraser G.E. Associations between diet and cancer, ischemic heart disease, and all-cause mortality in non-Hispanic white California Seventh-day Adventists. Am. J. Clin. Nutr. 1999;70:532S–538S. doi: 10.1093/ajcn/70.3.532s.
    1. Key T.J., Appleby P.N., Spencer E.A., Travis R.C., Roddam A.W., Allen N.E. Cancer incidence in vegetarians: Results from the European Prospective Investigation into Cancer and Nutrition (EPIC-Oxford) Am. J. Clin. Nutr. 2009;89:S1620–S1626. doi: 10.3945/ajcn.2009.26736M.
    1. Oostindjer M., Alexander J., Amdam G.V., Andersen G., Bryan N.S., Chen D., Corpet D.E., De Smet S., Dragsted L.O., Haug A., et al. The role of red and processed meat in colorectal cancer development: A perspective. Meat Sci. 2014;97:583–596. doi: 10.1016/j.meatsci.2014.02.011.
    1. Ritchie H., Roser M. Meat and Dairy Production. [(accessed on 27 June 2020)]; Available online: .
    1. Zhang F.F., Cudhea F., Shan Z., Michaud D.S., Imamura F., Eom H., Ruan M., Rehm C.D., Liu J., Du M., et al. Preventable Cancer Burden Associated With Poor Diet in the United States. JNCI Cancer Spectr. 2019;3:pkz034. doi: 10.1093/jncics/pkz034.
    1. Position of the American Dietetic Association and Dietitians of Canada: Vegetarian Diets. Can. J. Diet. Pract. Res. 2003;64:62–81. doi: 10.3148/64.2.2003.62.
    1. Godfray H.C.J., Aveyard P., Garnett T., Hall J.W., Key T.J., Lorimer J., Pierrehumbert R.T., Scarborough P., Springmann M., Jebb S.A. Meat consumption, health, and the environment. Science. 2018 doi: 10.1126/science.aam5324.
    1. Hawkes N. Cutting Europe’s meat and dairy consumption would benefit health and environment, says report. Br. Med. J. 2014;348:g2949. doi: 10.1136/bmj.g2949.
    1. Zeng L., Ruan M., Liu J., Wilde P., Naumova E.N., Mozaffarian D., Zhang F.F. Trends in Processed Meat, Unprocessed Red Meat, Poultry, and Fish Consumption in the United States, 1999–2016. J. Acad. Nutr. Diet. 2019;119:1085–1098. doi: 10.1016/j.jand.2019.04.004.
    1. Tugault-Lafleur C.N., Black J.L. Differences in the Quantity and Types of Foods and Beverages Consumed by Canadians between 2004 and 2015. Nutrients. 2019;11:526. doi: 10.3390/nu11030526.
    1. Sung H., Siegel R.L., Rosenberg P.S., Jemal A. Emerging cancer trends among young adults in the USA: Analysis of a population-based cancer registry. Lancet Public Health. 2019;4:e137–e147. doi: 10.1016/S2468-2667(18)30267-6.
    1. Brenner D.R., Ruan Y., Shaw E., O’Sullivan D., Poirier A.E., Heer E., Villeneuve P.J., Walter S.D., Friedenreich C.M., Smith L., et al. Age-standardized cancer-incidence trends in Canada, 1971–2015. Can. Med. Assoc. 2019;191:E1262–E1273. doi: 10.1503/cmaj.190355.
    1. Patel P., De P. Trends in colorectal cancer incidence and related lifestyle risk factors in 15–49-year-olds in Canada, 1969-2010. Cancer Epidemiol. 2016;42:90–100. doi: 10.1016/j.canep.2016.03.009.
    1. Alexander D.D., Cushing C.A. Red meat and colorectal cancer: A critical summary of prospective epidemiologic studies. Obes. Rev. 2011;12:e472–e493. doi: 10.1111/j.1467-789X.2010.00785.x.
    1. Alexander D.D., Weed D.L., Cushing C.A., Lowe K.A. Meta-analysis of prospective studies of red meat consumption and colorectal cancer. Eur. J. Cancer Prev. 2011;20:293–307. doi: 10.1097/CEJ.0b013e328345f985.
    1. Arab L., Su J., Steck S.E., Ang A., Fontham E.T.H., Bensen J.T., Mohler J.L. Adherence to World Cancer Research Fund/American Institute for Cancer Research Lifestyle Recommendations Reduces Prostate Cancer Aggressiveness among African and Caucasian Americans. Nutr. Cancer Int. J. 2013;65:633–643. doi: 10.1080/01635581.2013.789540.
    1. Larsson S.C., Wolk A. Red and processed meat consumption and risk of pancreatic cancer: Meta-analysis of prospective studies. Br. J. Cancer. 2012;106:603–607. doi: 10.1038/bjc.2011.585.
    1. Kim E., Coelho D., Blachier F. Review of the association between meat consumption and risk of colorectal cancer. Nutr. Res. 2013;33:983–994. doi: 10.1016/j.nutres.2013.07.018.
    1. Zhao Z., Feng Q., Yin Z., Shuang J., Bai B., Yu P., Guo M., Zhao Q. Red and processed meat consumption and colorectal cancer risk: A systematic review and meta-analysis. Oncotarget. 2017;8:83306–83314. doi: 10.18632/oncotarget.20667.
    1. Schwingshackl L., Schwedhelm C., Hoffmann G., Knuppel S., Laure Preterre A., Iqbal K., Bechthold A., De Henauw S., Michels N., Devleesschauwer B., et al. Food groups and risk of colorectal cancer. Int. J. Cancer. 2018;142:1748–1758. doi: 10.1002/ijc.31198.
    1. Zeraatkar D., Johnston B.C., Bartoszko J., Cheung K., Bala M.M., Valli C., Rabassa M., Sit D., Milio K., Sadeghirad B., et al. Effect of Lower versus Higher Red Meat Intake on Cardiometabolic and Cancer Outcomes: A Systematic Review of Randomized Trials. Ann. Intern. Med. 2019;171:721–731. doi: 10.7326/M19-0622.
    1. Vernooij R.W.M., Zeraatkar D., Han M.A., El Dib R., Zworth M., Milio K., Sit D., Lee Y., Gomaa H., Valli C., et al. Patterns of Red and Processed Meat Consumption and Risk for Cardiometabolic and Cancer Outcomes: A Systematic Review and Meta-analysis of Cohort Studies. Ann. Intern. Med. 2019;171:732–741. doi: 10.7326/M19-1583.
    1. Han M.A., Zeraatkar D., Guyatt G.H., Vernooij R.W.M., El Dib R., Zhang Y., Algarni A., Leung G., Storman D., Valli C., et al. Reduction of Red and Processed Meat Intake and Cancer Mortality and Incidence: A Systematic Review and Meta-analysis of Cohort Studies. Ann. Intern. Med. 2019;171:711–720. doi: 10.7326/M19-0699.
    1. Catsburg C., Kim R.S., Kirsh V.A., Soskolne C.L., Kreiger N., Rohan T.E. Dietary patterns and breast cancer risk: A study in 2 cohorts. Am. J. Clin. Nutr. 2015;101:817–823. doi: 10.3945/ajcn.114.097659.
    1. Chen Z., Wang P.P., Woodrow J., Zhu Y., Roebothan B., McLaughlin J.R., Parfrey P.S. Dietary patterns and colorectal cancer: Results from a Canadian population-based study. Nutr. J. 2015;14:8. doi: 10.1186/1475-2891-14-8.
    1. Zhu Y., Wu H., Wang P.P., Savas S., Woodrow J., Wish T., Jin R., Green R., Woods M., Roebothan B., et al. Dietary patterns and colorectal cancer recurrence and survival: A cohort study. BMJ Open. 2013;3:e002270. doi: 10.1136/bmjopen-2012-002270.
    1. Vieira A.R., Abar L., Chan D.S.M., Vingeliene S., Polemiti E., Stevens C., Greenwood D., Norat T. Foods and beverages and colorectal cancer risk: A systematic review and meta-analysis of cohort studies, an update of the evidence of the WCRF-AICR Continuous Update Project. Ann. Oncol. 2017;28:1788–1802. doi: 10.1093/annonc/mdx171.
    1. Reynolds A., Mann J., Cummings J., Winter N., Mete E., Te Morenga L. Carbohydrate quality and human health: A series of systematic reviews and meta-analyses. Lancet. 2019;393:434–445. doi: 10.1016/S0140-6736(18)31809-9.
    1. Makarem N., Nicholson J.M., Bandera E.V., McKeown N.M., Parekh N. Consumption of whole grains and cereal fiber in relation to cancer risk: A systematic review of longitudinal studies. Nutr. Rev. 2016;74:353–373. doi: 10.1093/nutrit/nuw003.
    1. Statistics Canada Canadian Community Health Survey: Overview of Canadians’ Eating Habits. [(accessed on 9 September 2016)];2006 Available online: .
    1. Cancer Care Ontario Cancer Risk Factors in Ontario: Healthy Weights, Healthy Eating and Active Living. [(accessed on 8 September 2016)]; Available online: .
    1. Liese A.D., Krebs-Smith S.M., Subar A.F., George S.M., Harmon B.E., Neuhouser M.L., Boushey C.J., Schap T.E., Reedy J. The Dietary Patterns Methods Project: Synthesis of findings across cohorts and relevance to dietary guidance. J. Nutr. 2015;145:393–402. doi: 10.3945/jn.114.205336.
    1. Carroll R.J., Midthune D., Subar A.F., Shumakovich M., Freedman L.S., Thompson F.E., Kipnis V. Taking advantage of the strengths of 2 different dietary assessment instruments to improve intake estimates for nutritional epidemiology. Am. J. Epidemiol. 2012;175:340–347. doi: 10.1093/aje/kwr317.
    1. Nanri A., Shimazu T., Ishihara J., Takachi R., Mizoue T., Inoue M., Tsugane S. Reproducibility and validity of dietary patterns assessed by a food frequency questionnaire used in the 5-year follow-up survey of the Japan Public Health Center-Based Prospective Study. J. Epidemiol. 2012;22:205–215. doi: 10.2188/jea.JE20110087.
    1. Kimokoti R.W., Newby P.K., Gona P., Zhu L., Campbell W.R., D’Agostino R.B., Millen B.E. Stability of the Framingham Nutritional Risk Score and its component nutrients over 8 years: The Framingham Nutrition Studies. Eur. J. Clin. Nutr. 2012;66:336–344. doi: 10.1038/ejcn.2011.167.
    1. Rebagliato M. Validation of self reported smoking. J. Epidemiol. Commun. Health. 2002;56:163–164. doi: 10.1136/jech.56.3.163.
    1. Dobson C.M., Russell A.J., Rubin G.P. Patient delay in cancer diagnosis: What do we really mean and can we be more specific? BMC Health Serv. Res. 2014;14:387. doi: 10.1186/1472-6963-14-387.
    1. Kabat G., Matthews C., Kamensky V., Hollenbeck A., Rohan T. Adherence to cancer prevention guidelines and cancer incidence, cancer mortality, and total mortality: A prospective cohort study. Am. J. Clin. Nutr. 2015;101:558–569. doi: 10.3945/ajcn.114.094854.
    1. Ruan Y., Poirier A.E., Hebert L.A., Grevers X., Walter S.D., Villeneuve P.J., Brenner D.R., Friedenreich C.M., ComPARe Study Team Estimates of the current and future burden of cancer attributable to red and processed meat consumption in Canada. Prev. Med. 2019;122:31–39. doi: 10.1016/j.ypmed.2019.03.011.

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