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Open Access 01-12-2022 | Colorectal Cancer | Research article

Plant-based dietary patterns defined by a priori indices and colorectal cancer risk by sex and race/ethnicity: the Multiethnic Cohort Study

Authors: Jihye Kim, Carol J. Boushey, Lynne R. Wilkens, Christopher A. Haiman, Loïc Le Marchand, Song-Yi Park

Published in: BMC Medicine | Issue 1/2022

Abstract

Background

Plant-based diets assessed by a priori indices are associated with health outcomes. This study investigated the associations between pre-defined indices of plant-based diets and risk of colorectal cancer (CRC) and evaluated whether the association varies by sex, race and ethnicity, and anatomic subsite of tumors.

Methods

A total of 79,952 men and 93,475 women who participated in the Multiethnic Cohort Study were included. Primary outcome was incidence of invasive CRC. Cox models were used to estimate the risk of CRC across quintiles of three plant-based diet scores: overall plant-based diet index (PDI), healthful plant-based diet index (hPDI), and unhealthful plant-based diet index (uPDI).

Results

During a mean follow-up of 19.2 years, 4976 incident CRC were identified. Among men, multivariable-adjusted HR (95% CI) for the highest vs. lowest quintiles was 0.77 (0.67–0.88) for PDI, and 0.80 (0.70–0.91) for hPDI, while no significant association was found for uPDI among men and for all indices among women. In men, the inverse association for PDI was stronger in Japanese American, Native Hawaiian, and White groups than African American or Latino group (P for heterogeneity = 0.01) and for left colon and rectal tumors than right tumors (P for heterogeneity = 0.005), whereas the decreased risk with hPDI was found consistently across racial and ethnic groups and subsites.

Conclusions

Greater adherence to plant-based diets rich in healthy plant foods and low in less healthy plant foods is associated with a reduced risk of CRC in men, but not in women. The strength of the association among men may vary by race and ethnicity and anatomic subsite of tumors.

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Araghi M, Soerjomataram I, Jenkins M, et al. Global trends in colorectal cancer mortality: projections to the year 2035. Int J Cancer. 2019;144(12):2992–3000. https://doi.org/10.1002/ijc.32055.CrossRefPubMed

Farvid MS, Sidahmed E, Spence ND, Mante Angua K, Rosner BA, Barnett JB. Consumption of red meat and processed meat and cancer incidence: a systematic review and meta-analysis of prospective studies. Eur J Epidemiol. 2021:1–15. https://doi.org/10.1007/s10654-021-00741-9

Veettil SK, Wong TY, Loo YS, et al. Role of diet in colorectal cancer incidence: umbrella review of meta-analyses of prospective observational studies. JAMA Netw Open. 2021;4(2):e2037341. https://doi.org/10.1001/jamanetworkopen.2020.37341.CrossRefPubMedPubMedCentral

World Cancer Research Fund & American Institute for Cacner Research. Diet, Nutrition, Physical Activity and Cancer: a Global Perspective. 2017. https://www.wcrf.org/wp-content/uploads/2021/02/Summary-of-Third-Expert-Report-2018.pdf. Accessed 15 Oct 2021.

Nucci D, Fatigoni C, Salvatori T, Nardi M, Realdon S, Gianfredi V. Association between dietary fibre intake and colorectal adenoma: a systematic review and meta-analysis. Int J Environ Res Public Health. 2021;18(8):4168. https://doi.org/10.3390/ijerph18084168.CrossRefPubMedPubMedCentral

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(10170):434–45. https://doi.org/10.1016/S0140-6736(18)31809-9.CrossRefPubMed

Satija A, Hu FB. Plant-based diets and cardiovascular health. Trends Cardiovasc Med. 2018;28(7):437–41. https://doi.org/10.1016/j.tcm.2018.02.004.CrossRefPubMedPubMedCentral

Hur J, Otegbeye E, Joh H-K, et al. Sugar-sweetened beverage intake in adulthood and adolescence and risk of early-onset colorectal cancer among women. Gut. 2021. https://doi.org/10.1136/gutjnl-2020-323450.CrossRefPubMed

Gaesser GA. Whole grains, refined grains, and cancer risk: a systematic review of meta-analyses of observational studies. Nutrients. 2020;12(12):3756. https://doi.org/10.3390/nu12123756.CrossRefPubMedCentral

10.

Kim H, Caulfield LE, Garcia-Larsen V, et al. Plant-based diets and incident CKD and kidney function. Clin J Am Soc Nephrol. 2019;14(5):682–91. https://doi.org/10.2215/CJN.12391018.CrossRefPubMedPubMedCentral

11.

Kim J, Kim H, Giovannucci EL. Quality of plant-based diets and risk of hypertension: a Korean genome and examination study. Eur J Nutr. 2021;60(7):3841–51. https://doi.org/10.1007/s00394-021-02559-3.CrossRefPubMed

12.

Satija A, Bhupathiraju SN, Rimm EB, et al. Plant-based dietary patterns and incidence of type 2 diabetes in US men and women: results from three prospective cohort studies. PLoS Med. 2016;13(6):e1002039. https://doi.org/10.1371/journal.pmed.1002039.CrossRefPubMedPubMedCentral

13.

Satija A, Bhupathiraju SN, Spiegelman D, et al. Healthful and unhealthful plant-based diets and the risk of coronary heart disease in US adults. J Am Coll Cardiol. 2017;70(4):411–22. https://doi.org/10.1016/j.jacc.2017.05.047.CrossRefPubMedPubMedCentral

14.

Kim H, Lee K, Rebholz CM, Kim J. Plant-based diets and incident metabolic syndrome: Results from a South Korean prospective cohort study. PLoS Med. 2020;17(11):e1003371. https://doi.org/10.1371/journal.pmed.1003371.CrossRefPubMedPubMedCentral

15.

Kolonel LN, Henderson BE, Hankin JH, et al. A multiethnic cohort in Hawaii and Los Angeles: baseline characteristics. Am J Epidemiol. 2000;151(4):346–57. https://doi.org/10.1093/oxfordjournals.aje.a010213.CrossRefPubMed

16.

Park SY, Boushey CJ, Wilkens LR, Haiman CA, Le Marchand L. High-quality diets associate with reduced risk of colorectal cancer: analyses of diet quality indexes in the multiethnic cohort. Gastroenterology. 2017;153(2):386-94. e2. https://doi.org/10.1053/j.gastro.2017.04.004.CrossRefPubMed

17.

Stram DO, Hankin JH, Wilkens LR, et al. Calibration of the dietary questionnaire for a multiethnic cohort in Hawaii and Los Angeles. Am J Epidemiol. 2000;151(4):358–70. https://doi.org/10.1093/oxfordjournals.aje.a010214.CrossRefPubMed

18.

Martinez-Gonzalez MA, Sanchez-Tainta A, Corella D, et al. A provegetarian food pattern and reduction in total mortality in the Prevencion con Dieta Mediterranea (PREDIMED) study. Am J Clin Nutr. 2014;100(Suppl 1):320S–8S. https://doi.org/10.3945/ajcn.113.071431.CrossRefPubMed

19.

Bowman SA FJ, Moshfegh A. MyPyramid Equivalents Database, 2.0 for USDA Survey Foods, 2003–2004. Food Surveys Research Group; 2008. https://www.ars.usda.gov/ARSUserFiles/80400530/pdf/mped/mped2_doc.pdf. Accessed 20 Sept 2021.

20.

Liese AD, Krebs-Smith SM, Subar AF, et al. The Dietary Patterns Methods Project: synthesis of findings across cohorts and relevance to dietary guidance. J Nutr. 2015;145(3):393–402. https://doi.org/10.3945/jn.114.205336.CrossRefPubMedPubMedCentral

21.

Schoenfeld D. Partial residuals for the proportional hazards regression model. Biometrika. 1982;69(1):239–41.CrossRef

22.

Bernstein AM, Sun Q, Hu FB, Stampfer MJ, Manson JE, Willett WC. Major dietary protein sources and risk of coronary heart disease in women. Circulation. 2010;122(9):876–83. https://doi.org/10.1161/CIRCULATIONAHA.109.915165.CrossRefPubMedPubMedCentral

23.

Lunn M, McNeil D. Applying Cox regression to competing risks. Biometrics. 1995;51(2):524–32.CrossRefPubMed

24.

Therneau T, Grambsh P. Modeling survival data: extending the Cox model. New York: Springer; 2000.CrossRef

25.

Desquilbet L, Mariotti F. Dose-response analyses using restricted cubic spline functions in public health research. Stat Med. 2010;29(9):1037–57. https://doi.org/10.1002/sim.3841.CrossRefPubMed

26.

Wirfalt E, Midthune D, Reedy J, et al. Associations between food patterns defined by cluster analysis and colorectal cancer incidence in the NIH-AARP diet and health study. Eur J Clin Nutr. 2009;63(6):707–17. https://doi.org/10.1038/ejcn.2008.40.CrossRefPubMed

27.

Watling CZ, Schmidt JA, Dunneram Y, et al. Risk of cancer in regular and low meat-eaters, fish-eaters, and vegetarians: a prospective analysis of UK Biobank participants. BMC Med. 2022;20(1):73. https://doi.org/10.1186/s12916-022-02256-w.CrossRefPubMedPubMedCentral

28.

Gilsing AM, Schouten LJ, Goldbohm RA, Dagnelie PC, van den Brandt PA, Weijenberg MP. Vegetarianism, low meat consumption and the risk of colorectal cancer in a population based cohort study. Sci Rep. 2015;5(1):1–12. https://doi.org/10.1038/srep13484.CrossRef

29.

Cassidy A, Rogers G, Peterson JJ, Dwyer JT, Lin H, Jacques PF. Higher dietary anthocyanin and flavonol intakes are associated with anti-inflammatory effects in a population of US adults. Am J Clin Nutr. 2015;102(1):172–81. https://doi.org/10.3945/ajcn.115.108555.CrossRefPubMedPubMedCentral

30.

Zhao Y, Jiang Q. Roles of the polyphenol-gut microbiota interaction in alleviating colitis and preventing colitis-associated colorectal cancer. Adv Nutr. 2021;12(2):546–65. https://doi.org/10.1093/advances/nmaa104.CrossRefPubMed

31.

Park SY, Nomura AM, Murphy SP, Wilkens LR, Henderson BE, Kolonel LN. Carotenoid intake and colorectal cancer risk: the multiethnic cohort study. J Epidemiol. 2009:0903030074. https://doi.org/10.2188/jea.JE20080078.

32.

Mehta RS, Nishihara R, Cao Y, et al. Association of dietary patterns with risk of colorectal cancer subtypes classified by Fusobacterium nucleatum in tumor tissue. JAMA Oncol. 2017;3(7):921–7. https://doi.org/10.1001/jamaoncol.2016.6374.CrossRefPubMedPubMedCentral

33.

Smith PM, Howitt MR, Panikov N, et al. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science. 2013;341(6145):569–73. https://doi.org/10.1126/science.1241165.CrossRefPubMed

34.

Sonnenburg ED, Smits SA, Tikhonov M, Higginbottom SK, Wingreen NS, Sonnenburg JL. Diet-induced extinctions in the gut microbiota compound over generations. Nature. 2016;529(7585):212–5. https://doi.org/10.1038/nature16504.CrossRefPubMedPubMedCentral

35.

Debras C, Chazelas E, Srour B, et al. Glycaemic index, glycaemic load and cancer risk: results from the prospective NutriNet-Santé cohort. Int J Epidemiol. 2021. https://doi.org/10.1093/ije/dyab169.CrossRef

36.

Turati F, Galeone C, Augustin LS, La Vecchia C. Glycemic index, glycemic load and cancer risk: an updated meta-analysis. Nutrients. 2019;11(10):2342. https://doi.org/10.3390/nu11102342.CrossRefPubMedCentral

37.

Siegel RL, Miller KD, Goding Sauer A, et al. Colorectal cancer statistics, 2020. CA Cancer J Clin. 2020;70(3):145–64. https://doi.org/10.3322/caac.21601.CrossRefPubMed

38.

Park SY, Wilkens LR, Kolonel LN, Monroe KR, Haiman CA, Le Marchand L. Exploring Differences in the aspirin–colorectal cancer association by sex and race/ethnicity: the multiethnic cohort study. Cancer Epidemiol Biomarkers Prev. 2017;26(2):162–9. https://doi.org/10.1158/1055-9965.EPI-16-0560.CrossRefPubMed

39.

Park SY, Wilkens LR, Kolonel LN, Henderson BE, Le Marchand L. Inverse associations of dietary fiber and menopausal hormone therapy with colorectal cancer risk in the Multiethnic Cohort Study. Int J Cancer. 2016;139(6):1241–50. https://doi.org/10.1002/ijc.30172.CrossRefPubMedPubMedCentral

40.

Slattery ML, Curtin K, Wolff RK, Herrick JS, Caan BJ, Samowitz W. Diet, physical activity, and body size associations with rectal tumor mutations and epigenetic changes. Cancer Causes Control. 2010;21(8):1237–45. https://doi.org/10.1007/s10552-010-9551-4.CrossRefPubMedPubMedCentral

41.

Wang L, Lo CH, He X, et al. Risk factor profiles differ for cancers of different regions of the colorectum. Gastroenterology. 2020;159(1):241-56 e13. https://doi.org/10.1053/j.gastro.2020.03.054.CrossRefPubMed

42.

Gianfredi V, Nucci D, Salvatori T, et al. Rectal Cancer: 20% risk reduction thanks to dietary fibre intake. Systematic review and meta-analysis. Nutrients. 2019;11(7):1579. https://doi.org/10.3390/nu11071579.CrossRefPubMedCentral

43.

Orlich MJ, Singh PN, Sabaté J, et al. Vegetarian dietary patterns and the risk of colorectal cancers. JAMA Intern Med. 2015;175(5):767–76. https://doi.org/10.1001/jamainternmed.2015.59.CrossRefPubMedPubMedCentral

Title: Plant-based dietary patterns defined by a priori indices and colorectal cancer risk by sex and race/ethnicity: the Multiethnic Cohort Study
Authors: Jihye Kim
Carol J. Boushey
Lynne R. Wilkens
Christopher A. Haiman
Loïc Le Marchand
Song-Yi Park
Publication date: 01-12-2022
Publisher: BioMed Central
Keywords: Colorectal Cancer
Colorectal Cancer
Published in: BMC Medicine / Issue 1/2022
Electronic ISSN: 1741-7015
DOI: https://doi.org/10.1186/s12916-022-02623-7

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Plant-based dietary patterns defined by a priori indices and colorectal cancer risk by sex and race/ethnicity: the Multiethnic Cohort Study

Abstract

Background

Methods

Results

Conclusions

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Abstract

Background

Methods

Results

Conclusions

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