Abstract
Several case–control and prospective cohort studies have examined the association between the consumption of nuts and legumes and the risk of colorectal cancer. For the quantitative assessment of this association, we conducted a meta-analysis of observational studies. We searched PubMed and Web of Science databases along with hand searches for eligible studies published up to January 2022. A total of 13 studies (8 cohort studies and 5 case–control studies) on nuts consumption and 29 studies (16 cohort studies and 13 case–control studies) on legumes consumption were included in the meta-analysis. The pooled relative risks (RRs) of colorectal cancer for the highest versus lowest categories of nuts consumption and legumes consumption were 0.84 (95% CI: 0.71–0.99) and 0.90 (95% CI: 0.83–0.98), respectively. Based on the dose–response analysis, a 28 g/day (1 serving/day) increment of nut consumption was associated with a 33% lower risk of colorectal cancer, and 100 g/day (1 serving/day) increment of legumes consumption was associated with a 21% lower risk of colorectal cancer. By geographic region for nuts consumption, however, the inverse association for the highest versus lowest categories was only observed in Asia (RR = 0.44; 95% CI: 0.29–0.68) from 3 studies, and no association was found in America (RR = 1.01; 95% CI: 0.92–1.11) (Pdifference = 0.003) or Europe (RR = 1.02; 95% CI: 0.84–1.25) (Pdifference = 0.003). In addition, the associations tended to be weak when stratified by adjustment for confounders. Our findings suggest that the evidence for an association is currently weak, and thus further well-designed prospective studies are needed.
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References
Ferlay JEM, Lam F, Colombet M, Mery L, Piñeros M, Znaor A, Soerjomataram I, Bray F. Global cancer observatory: cancer today. Lyon, France: International Agency for Research on Cancer. 2020. https://gco.iarc.fr/today. Accessed 23 July 2021
Ferlay JLM, Ervik M, Lam F, Colombet M, Mery L, Piñeros M, Znaor A, Soerjomataram I, Bray F. Global cancer observatory: cancer tomorrow. Lyon, France: International Agency for Research on Cancer. 2020. https://gco.iarc.fr/tomorrow. Accessed 23 July 2021
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.
Martini D, Godos J, Marventano S, et al. Nut and legume consumption and human health: an umbrella review of observational studies. Int J Food Sci Nutr 2021;1–8. https://doi.org/10.1080/09637486.2021.1880554
González CA, Salas-Salvadó J. The potential of nuts in the prevention of cancer. Br J Nutr. 2006;96(Suppl 2):S87-94. https://doi.org/10.1017/bjn20061868.
Alasalvar C, Bolling BW. Review of nut phytochemicals, fat-soluble bioactives, antioxidant components and health effects. Br J Nutr. 2015;113(Suppl 2):S68-78. https://doi.org/10.1017/s0007114514003729.
Naghshi S, Sadeghian M, Nasiri M, Mobarak S, Asadi M, Sadeghi O. Association of total nut, tree nut, peanut, and peanut butter consumption with cancer incidence and mortality: a comprehensive systematic review and dose-response meta-analysis of observational studies. Adv Nutr (Bethesda, Md.). 2021;12(3):793–808. https://doi.org/10.1093/advances/nmaa152
Messina M. Soy and health update: evaluation of the clinical and epidemiologic literature. Nutrients. 2016;8(12). https://doi.org/10.3390/nu8120754
Hu JF, Liu YY, Yu YK, Zhao TZ, Liu SD, Wang QQ. Diet and cancer of the colon and rectum: a case-control study in China. Int J Epidemiol. 1991;20(2):362–7. https://doi.org/10.1093/ije/20.2.362.
Hoshiyama Y, Sekine T, Sasaba T. A case-control study of colorectal cancer and its relation to diet, cigarettes, and alcohol consumption in Saitama Prefecture, Japan. Tohoku J Exp Med. 1993;171(2):153–65. https://doi.org/10.1620/tjem.171.153.
Steinmetz KA, Potter JD. Food-group consumption and colon cancer in the Adelaide Case-Control Study. I. Vegetables and fruit. Int J Cancer. 1993;53(5):711–9. https://doi.org/10.1002/ijc.2910530502
Singh PN, Fraser GE. Dietary risk factors for colon cancer in a low-risk population. Am J Epidemiol. 1998;148(8):761–74. https://doi.org/10.1093/oxfordjournals.aje.a009697.
Deneo-Pellegrini H, Boffetta P, De Stefani E, Ronco A, Brennan P, Mendilaharsu M. Plant foods and differences between colon and rectal cancers. Eur J Cancer Prev Off J Eur Cancer Prev Org (ECP). 2002;11(4):369–75. https://doi.org/10.1097/00008469-200208000-00009.
Yeh CC, You SL, Chen CJ, Sung FC. Peanut consumption and reduced risk of colorectal cancer in women: a prospective study in Taiwan. World J Gastroenterol. 2006;12(2):222–7. https://doi.org/10.3748/wjg.v12.i2.222.
Yang G, Shu XO, Li H, et al. Prospective cohort study of soy food intake and colorectal cancer risk in women. Am J Clin Nutr. 2009;89(2):577–83. https://doi.org/10.3945/ajcn.2008.26742.
Shin A, Lee J, Lee J, et al. Isoflavone and soyfood intake and colorectal cancer risk: a case-control study in Korea. PLoS ONE. 2015;10(11): e0143228. https://doi.org/10.1371/journal.pone.0143228.
Lee J, Shin A, Oh JH, Kim J. The relationship between nut intake and risk of colorectal cancer: a case control study. Nutr J. 2018;17(1):37. https://doi.org/10.1186/s12937-018-0345-y.
Zhang D, Dai C, Zhou L, et al. Meta-analysis of the association between nut consumption and the risks of cancer incidence and cancer-specific mortality. Aging. 2020;12(11):10772–94. https://doi.org/10.18632/aging.103292
Long J, Ji Z, Yuan P, et al. Nut consumption and risk of cancer: a meta-analysis of prospective studies. Cancer Epidemiol Biom Prev. 2020;29(3):565–73. https://doi.org/10.1158/1055-9965.epi-19-1167.
Zhu B, Sun Y, Qi L, Zhong R, Miao X. Dietary legume consumption reduces risk of colorectal cancer: evidence from a meta-analysis of cohort studies. Sci Rep. 2015;5:8797. https://doi.org/10.1038/srep08797.
Vieira AR, Abar L, Chan DSM, et al. 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(8):1788–802. https://doi.org/10.1093/annonc/mdx171.
Stroup DF, Berlin JA, Morton SC, et al. Meta-analysis of observational studies in epidemiology. A proposal for reporting. JAMA. 2000;283(15):2008–12. https://doi.org/10.1001/jama.283.15.2008.
DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986;7(3):177–88. https://doi.org/10.1016/0197-2456(86)90046-2.
Inoue M, Tajima K, Hirose K, et al. Subsite-specific risk factors for colorectal cancer: a hospital-based case-control study in Japan. Cancer Causes Control CCC. 1995;6(1):14–22. https://doi.org/10.1007/bf00051676.
Nishi M, Yoshida K, Hirata K, Miyake H. Eating habits and colorectal cancer. Oncol Rep. 1997;4(5):995–8. https://doi.org/10.3892/or.4.5.995.
Voorrips LE, Goldbohm RA, van Poppel G, Sturmans F, Hermus RJ, van den Brandt PA. Vegetable and fruit consumption and risks of colon and rectal cancer in a prospective cohort study: the Netherlands cohort study on diet and cancer. Am J Epidemiol. 2000;152(11):1081–92. https://doi.org/10.1093/aje/152.11.1081.
Budhathoki S, Joshi AM, Ohnaka K, et al. Soy food and isoflavone intake and colorectal cancer risk: the Fukuoka colorectal cancer study. Scand J Gastroenterol. 2011;46(2):165–72. https://doi.org/10.3109/00365521.2010.522720.
Michels KB, Edward G, Joshipura KJ, et al. Prospective study of fruit and vegetable consumption and incidence of colon and rectal cancers. J Natl Cancer Inst. 2000;92(21):1740–52. https://doi.org/10.1093/jnci/92.21.1740.
Nieuwenhuis L, Simons C, Weijenberg MP, van den Brandt PA. Nut and peanut butter intake and the risk of colorectal cancer and its anatomical and molecular subtypes: the Netherlands Cohort Study. Carcinogenesis. 2020;41(10):1368–84. https://doi.org/10.1093/carcin/bgaa080.
Oba S, Nagata C, Shimizu N, et al. Soy product consumption and the risk of colon cancer: a prospective study in Takayama. Japan Nutr Cancer. 2007;57(2):151–7. https://doi.org/10.1080/01635580701274475.
Park Y, Subar AF, Kipnis V, et al. Fruit and vegetable intakes and risk of colorectal cancer in the NIH-AARP diet and health study. Am J Epidemiol. 2007;166(2):170–80. https://doi.org/10.1093/aje/kwm067.
Akhter M, Inoue M, Kurahashi N, Iwasaki M, Sasazuki S, Tsugane S. Dietary soy and isoflavone intake and risk of colorectal cancer in the Japan public health center-based prospective study. Cancer Epidemiol Biom Prev. 2008;17(8):2128–35. https://doi.org/10.1158/1055-9965.epi-08-0182.
Le Marchand L, Hankin JH, Wilkens LR, Kolonel LN, Englyst HN, Lyu LC. Dietary fiber and colorectal cancer risk. Epidemiology. 1997;8(6):658–65. https://doi.org/10.1097/00001648-199710000-00008
Young TB, Wolf DA. Case-control study of proximal and distal colon cancer and diet in Wisconsin. Int J Cancer. 1988;42(2):167–75. https://doi.org/10.1002/ijc.2910420205.
Williams CD, Satia JA, Adair LS, et al. Dietary patterns, food groups, and rectal cancer risk in Whites and African-Americans. Cancer Epidemiol Biom Prev. 2009;18(5):1552–61. https://doi.org/10.1158/1055-9965.epi-08-1146.
Sellers TA, Bazyk AE, Bostick RM, et al. Diet and risk of colon cancer in a large prospective study of older women: an analysis stratified on family history (Iowa, United States). Cancer Causes Control CCC. 1998;9(4):357–67. https://doi.org/10.1023/a:1008886715597.
Huang XE, Hirose K, Wakai K, et al. Comparison of lifestyle risk factors by family history for gastric, breast, lung and colorectal cancer. Asian Pacific J Cancer Prev APJCP. 2004;5(4):419–27.
Greenland S, Longnecker MP. Methods for trend estimation from summarized dose-response data, with applications to meta-analysis. Am J Epidemiol. 1992;135(11):1301–9. https://doi.org/10.1093/oxfordjournals.aje.a116237.
Berlin JA, Longnecker MP, Greenland S. Meta-analysis of epidemiologic dose-response data. Epidemiology. 1993;4(3):218–28. https://doi.org/10.1097/00001648-199305000-00005
Orsini N, Bellocco R, Greenland S. Generalized least squares for trend estimation of summarized dose–response data. Stand Genomic Sci. 2006;6(1):40–57. https://doi.org/10.1177/1536867X0600600103.
Bechthold A, Boeing H, Schwedhelm C, et al. Food groups and risk of coronary heart disease, stroke and heart failure: a systematic review and dose-response meta-analysis of prospective studies. Crit Rev Food Sci Nutr. 2019;59(7):1071–90. https://doi.org/10.1080/10408398.2017.1392288.
Cochran WG. The combination of estimates from different experiments. Biometrics. 1954;10(1):101–29. https://doi.org/10.2307/3001666.
Higgins JPT, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ. 2003;327(7414):557. https://doi.org/10.1136/bmj.327.7414.557.
Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics. 1994;50(4):1088–101. https://doi.org/10.2307/2533446.
Egger M, Smith GD, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997;315(7109):629. https://doi.org/10.1136/bmj.315.7109.629.
Duval S, Tweedie R. Trim and fill: a simple funnel-plot-based method of testing and adjusting for publication bias in meta-analysis. Biometrics. 2000;56(2):455–63. https://doi.org/10.1111/j.0006-341x.2000.00455.x.
Jenab M, Ferrari P, Slimani N, et al. Association of nut and seed intake with colorectal cancer risk in the European Prospective Investigation into Cancer and Nutrition. Cancer Epidemiol Biom Prev. 2004;13(10):1595–603.
Lin J, Zhang SM, Cook NR, Lee IM, Buring JE. Dietary fat and fatty acids and risk of colorectal cancer in women. Am J Epidemiol. 2004;160(10):1011–22. https://doi.org/10.1093/aje/kwh319.
Yang M, Hu FB, Giovannucci EL, et al. Nut consumption and risk of colorectal cancer in women. Eur J Clin Nutr. 2016;70(3):333–7. https://doi.org/10.1038/ejcn.2015.66.
Fang Z, Wu Y, Li Y, et al. Association of nut consumption with risk of total cancer and 5 specific cancers: evidence from 3 large prospective cohort studies. Am J Clin Nutr. 2021;114(6):1925–35. https://doi.org/10.1093/ajcn/nqab295.
Evans RC, Fear S, Ashby D, et al. Diet and colorectal cancer: an investigation of the lectin/galactose hypothesis. Gastroenterology. 2002;122(7):1784–92. https://doi.org/10.1053/gast.2002.33659.
Flood A, Velie EM, Chaterjee N, et al. Fruit and vegetable intakes and the risk of colorectal cancer in the Breast Cancer Detection Demonstration Project follow-up cohort. Am J Clin Nutr. 2002;75(5):936–43. https://doi.org/10.1093/ajcn/75.5.936.
Lin J, Zhang SM, Cook NR, et al. Dietary intakes of fruit, vegetables, and fiber, and risk of colorectal cancer in a prospective cohort of women (United States). Cancer Causes Control CCC. 2005;16(3):225–33. https://doi.org/10.1007/s10552-004-4025-1.
Butler LM, Wang R, Koh WP, Yu MC. Prospective study of dietary patterns and colorectal cancer among Singapore Chinese. Br J Cancer. 2008;99(9):1511–6. https://doi.org/10.1038/sj.bjc.6604678.
Bamia C, Lagiou P, Buckland G, et al. Mediterranean diet and colorectal cancer risk: results from a European cohort. Eur J Epidemiol. 2013;28(4):317–28. https://doi.org/10.1007/s10654-013-9795-x.
Vogtmann E, Xiang YB, Li HL, et al. Fruit and vegetable intake and the risk of colorectal cancer: results from the Shanghai Men’s Health Study. Cancer Causes Control CCC. 2013;24(11):1935–45. https://doi.org/10.1007/s10552-013-0268-z.
Jones P, Cade JE, Evans CEL, Hancock N, Greenwood DC. The Mediterranean diet and risk of colorectal cancer in the UK Women’s Cohort Study. Int J Epidemiol. 2017;46(6):1786–96. https://doi.org/10.1093/ije/dyx155.
Seow A, Quah SR, Nyam D, Straughan PT, Chua T, Aw TC. Food groups and the risk of colorectal carcinoma in an Asian population. Cancer. 2002;95(11):2390–6. https://doi.org/10.1002/cncr.10971.
Abu Mweis SS, Tayyem RF, Shehadah I, et al. Food groups and the risk of colorectal cancer: results from a Jordanian case-control study. Eur J Cancer Prev. 2015;24(4):313–20. https://doi.org/10.1097/cej.0000000000000089.
Azzeh FS, Alshammari EM, Alazzeh AY, et al. Healthy dietary patterns decrease the risk of colorectal cancer in the Mecca Region, Saudi Arabia: a case-control study. BMC Public Health. 2017;17(1):607. https://doi.org/10.1186/s12889-017-4520-4.
International Nut and Dried Fruit Council Foundation. Nuts & dried fruits statistical yearbook 2020/2021. Reus, Spain; 2021.
Herforth A, Arimond M, Álvarez-Sánchez C, Coates J, Christianson K, Muehlhoff E. A global review of food-based dietary guidelines. Adv Nutr 2019;10(4):590–605. https://doi.org/10.1093/advances/nmy130
Shek LP, Cabrera-Morales EA, Soh SE, et al. A population-based questionnaire survey on the prevalence of peanut, tree nut, and shellfish allergy in 2 Asian populations. J Allergy Clin Immunol. 2010;126(2):324–31, 31.e1–7. https://doi.org/10.1016/j.jaci.2010.06.003
World Cancer Research Fund/American Institute for Cancer Research. Continuous Update Project Export Report 2018. Wholegrains, vegetables and fruit and the risk of cancer.London; Arlington (VA): World Cancer Research Fund International; American Institute for Cancer Research; 2018. https://www.wcrf.org/dietandcancer/wholegrains-vegetables-and-fruit/. Accessed 1 September 2021
Yu J, Bi X, Yu B, Chen D. Isoflavones: anti-inflammatory benefit and possible caveats. Nutrients. 2016;8(6). https://doi.org/10.3390/nu8060361
Khankari NK, Yang JJ, Sawada N, et al. Soy intake and colorectal cancer risk: results from a pooled analysis of prospective cohort studies conducted in China and Japan. J Nutr. 2020;150(9):2442–50. https://doi.org/10.1093/jn/nxaa194.
Zeng H, Lazarova DL, Bordonaro M. Mechanisms linking dietary fiber, gut microbiota and colon cancer prevention. World J Gastrointest Oncol. 2014;6(2):41–51. https://doi.org/10.4251/wjgo.v6.i2.41.
Falasca M, Casari I. Cancer chemoprevention by nuts: evidence and promises. Front Biosci. 2012;4:109–20. https://doi.org/10.2741/254.
Kuiper GG, Lemmen JG, Carlsson B, et al. Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology. 1998;139(10):4252–63. https://doi.org/10.1210/endo.139.10.6216.
Niv Y. Estrogen receptor β expression and colorectal cancer: a systematic review and meta-analysis. Eur J Gastroenterol Hepatol. 2015;27(12):1438–42. https://doi.org/10.1097/meg.0000000000000471.
Sterne JA, Gavaghan D, Egger M. Publication and related bias in meta-analysis: power of statistical tests and prevalence in the literature. J Clin Epidemiol. 2000;53(11):1119–29. https://doi.org/10.1016/s0895-4356(00)00242-0.
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This work was supported by the National Research Foundation of Korea, funded by Ministry of Science, ICT and Future Planning (Grant number: NRF-2021R1F1A1050847).
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Study concept and design: SJ and YJ, data collection and statistical analysis: SJ, writing—original draft: SJ, writing—review and editing: YJ, study supervision: YJ, Interpretation of the data, critical revision of the paper for important intellectual content and approval of the final paper for submission: SJ and YJ.
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Jin, S., Je, Y. Nuts and legumes consumption and risk of colorectal cancer: a systematic review and meta-analysis. Eur J Epidemiol 37, 569–585 (2022). https://doi.org/10.1007/s10654-022-00881-6
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DOI: https://doi.org/10.1007/s10654-022-00881-6