Nut Consumption and Survival in Patients With Stage III Colon Cancer: Results From CALGB 89803 (Alliance)
Temidayo Fadelu, Sui Zhang, Donna Niedzwiecki, Xing Ye, Leonard B Saltz, Robert J Mayer, Rex B Mowat, Renaud Whittom, Alexander Hantel, Al B Benson, Daniel M Atienza, Michael Messino, Hedy L Kindler, Alan Venook, Shuji Ogino, Kimmie Ng, Kana Wu, Walter Willett, Edward Giovannucci, Jeffrey Meyerhardt, Ying Bao, Charles S Fuchs, Temidayo Fadelu, Sui Zhang, Donna Niedzwiecki, Xing Ye, Leonard B Saltz, Robert J Mayer, Rex B Mowat, Renaud Whittom, Alexander Hantel, Al B Benson, Daniel M Atienza, Michael Messino, Hedy L Kindler, Alan Venook, Shuji Ogino, Kimmie Ng, Kana Wu, Walter Willett, Edward Giovannucci, Jeffrey Meyerhardt, Ying Bao, Charles S Fuchs
Abstract
Purpose Observational studies have reported increased colon cancer recurrence and mortality in patients with states of hyperinsulinemia, including type 2 diabetes, obesity, sedentary lifestyle, and high glycemic load diet. Nut intake has been associated with a lower risk of type 2 diabetes, metabolic syndrome, and insulin resistance. However, the effect of nut intake on colon cancer recurrence and survival is not known. Patients and Methods We conducted a prospective, observational study of 826 eligible patients with stage III colon cancer who reported dietary intake on food frequency questionnaires while enrolled onto a randomized adjuvant chemotherapy trial. Using Cox proportional hazards regression, we assessed associations of nut intake with cancer recurrence and mortality. Results After a median follow-up of 6.5 years, compared with patients who abstained from nuts, individuals who consumed two or more servings of nuts per week experienced an adjusted hazard ratio (HR) for disease-free survival of 0.58 (95% CI, 0.37 to 0.92; Ptrend = .03) and an HR for overall survival of 0.43 (95% CI, 0.25 to 0.74; Ptrend = .01). In subgroup analysis, the apparent benefit was confined to tree nut intake (HR for disease-free survival, 0.54; 95% CI, 0.34 to 0.85; Ptrend = .04; and HR for overall survival, 0.47; 95% CI, 0.27 to 0.82; Ptrend = .04). The association of total nut intake with improved outcomes was maintained across other known or suspected risk factors for cancer recurrence and mortality. Conclusion Diets with a higher consumption of nuts may be associated with a significantly reduced incidence of cancer recurrence and death in patients with stage III colon cancer.
Trial registration: ClinicalTrials.gov NCT00003835.
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References
- Meyerhardt JA, Sato K, Niedzwiecki D, et al. : Dietary glycemic load and cancer recurrence and survival in patients with stage III colon cancer: Findings from CALGB 89803. J Natl Cancer Inst 104:1702-1711, 2012
- Meyerhardt JA, Heseltine D, Niedzwiecki D, et al. : Impact of physical activity on cancer recurrence and survival in patients with stage III colon cancer: Findings from CALGB 89803. J Clin Oncol 24:3535-3541, 2006
- Meyerhardt JA, Niedzwiecki D, Hollis D, et al. : Association of dietary patterns with cancer recurrence and survival in patients with stage III colon cancer. JAMA 298:754-764, 2007
- Meyerhardt JA, Niedzwiecki D, Hollis D, et al. : Impact of body mass index and weight change after treatment on cancer recurrence and survival in patients with stage III colon cancer: Findings from Cancer and Leukemia Group B 89803. J Clin Oncol 26:4109-4115, 2008
- Meyerhardt JA, Giovannucci EL, Holmes MD, et al. : Physical activity and survival after colorectal cancer diagnosis. J Clin Oncol 24:3527-3534, 2006
- Dignam JJ, Polite BN, Yothers G, et al. : Body mass index and outcomes in patients who receive adjuvant chemotherapy for colon cancer. J Natl Cancer Inst 98:1647-1654, 2006
- Meyerhardt JA, Catalano PJ, Haller DG, et al. : Impact of diabetes mellitus on outcomes in patients with colon cancer. J Clin Oncol 21:433-440, 2003
- Fuchs MA, Sato K, Niedzwiecki D, et al. : Sugar-sweetened beverage intake and cancer recurrence and survival in CALGB 89803 (Alliance). PLoS One 9:e99816, 2014
- Wolpin BM, Meyerhardt JA, Chan AT, et al. : Insulin, the insulin-like growth factor axis, and mortality in patients with nonmetastatic colorectal cancer. J Clin Oncol 27:176-185, 2009
- Bhupathiraju SN, Pan A, Manson JE, et al. : Changes in coffee intake and subsequent risk of type 2 diabetes: Three large cohorts of US men and women. Diabetologia 57:1346-1354, 2014
- Ding M, Bhupathiraju SN, Chen M, et al. : Caffeinated and decaffeinated coffee consumption and risk of type 2 diabetes: A systematic review and a dose-response meta-analysis. Diabetes Care 37:569-586, 2014
- Bhupathiraju SN, Pan A, Malik VS, et al. : Caffeinated and caffeine-free beverages and risk of type 2 diabetes. Am J Clin Nutr 97:155-166, 2013
- van Dam RM, Hu FB: Coffee consumption and risk of type 2 diabetes: A systematic review. JAMA 294:97-104, 2005
- Salazar-Martinez E, Willett WC, Ascherio A, et al. : Coffee consumption and risk for type 2 diabetes mellitus. Ann Intern Med 140:1-8, 2004
- Wu T, Willett WC, Hankinson SE, et al. : Caffeinated coffee, decaffeinated coffee, and caffeine in relation to plasma C-peptide levels, a marker of insulin secretion, in U.S. women. Diabetes Care 28:1390-1396, 2005
- Fung TT, Hu FB, Schulze M, et al. : A dietary pattern that is associated with C-peptide and risk of colorectal cancer in women. Cancer Causes Control 23:959-965, 2012
- Wedick NM, Brennan AM, Sun Q, et al. : Effects of caffeinated and decaffeinated coffee on biological risk factors for type 2 diabetes: A randomized controlled trial. Nutr J 10:93, 2011
- Williams CJ, Fargnoli JL, Hwang JJ, et al. : Coffee consumption is associated with higher plasma adiponectin concentrations in women with or without type 2 diabetes: A prospective cohort study. Diabetes Care 31:504-507, 2008
- Guercio BJ, Sato K, Niedzwiecki D, et al. : Coffee intake, recurrence, and mortality in stage III colon cancer: Results from CALGB 89803 (Alliance). J Clin Oncol 33:3598-3607, 2015
- Casas-Agustench P, López-Uriarte P, Bulló M, et al. : Effects of one serving of mixed nuts on serum lipids, insulin resistance and inflammatory markers in patients with the metabolic syndrome. Nutr Metab Cardiovasc Dis 21:126-135, 2011
- Holligan SD, West SG, Gebauer SK, et al. : A moderate-fat diet containing pistachios improves emerging markers of cardiometabolic syndrome in healthy adults with elevated LDL levels. Br J Nutr 112:744-752, 2014
- O’Neil CE, Fulgoni VL, III, Nicklas TA: Tree nut consumption is associated with better adiposity measures and cardiovascular and metabolic syndrome health risk factors in U.S. adults: NHANES 2005-2010. Nutr J 14:64, 2015
- Ros E: Health benefits of nut consumption. Nutrients 2:652-682, 2010
- Hernández-Alonso P, Salas-Salvadó J, Baldrich-Mora M, et al. : Beneficial effect of pistachio consumption on glucose metabolism, insulin resistance, inflammation, and related metabolic risk markers: A randomized clinical trial. Diabetes Care 37:3098-3105, 2014
- Jenkins DJ, Kendall CW, Josse AR, et al. : Almonds decrease postprandial glycemia, insulinemia, and oxidative damage in healthy individuals. J Nutr 136:2987-2992, 2006
- Jiang R, Jacobs DR, Jr, Mayer-Davis E, et al. : Nut and seed consumption and inflammatory markers in the multi-ethnic study of atherosclerosis. Am J Epidemiol 163:222-231, 2006
- Sweazea KL, Johnston CS, Ricklefs KD, et al. : Almond supplementation in the absence of dietary advice significantly reduces C-reactive protein in subjects with type 2 diabetes. J Funct Foods 10:252-259, 2014
- Kris-Etherton PM, Hu FB, Ros E, et al. : The role of tree nuts and peanuts in the prevention of coronary heart disease: Multiple potential mechanisms. J Nutr 138:1746S-1751S, 2008
- González CA, Salas-Salvadó J: The potential of nuts in the prevention of cancer. Br J Nutr 96:S87-S94, 2006. (suppl 2)
- Pfundstein B, Haubner R, Würtele G, et al. : Pilot walnut intervention study of urolithin bioavailability in human volunteers. J Agric Food Chem 62:10264-10273, 2014
- Saltz LB, Niedzwiecki D, Hollis D, et al. : Irinotecan fluorouracil plus leucovorin is not superior to fluorouracil plus leucovorin alone as adjuvant treatment for stage III colon cancer: Results of CALGB 89803. J Clin Oncol 25:3456-3461, 2007
- Zubrod CG, Schneiderman M, Frei E, et al. : Appraisal of methods for the study of chemotherapy of cancer in man: Comparative therapeutic trial of nitrogen mustard and triethylene thiophosphoramide. J Chronic Dis 11:7-33, 1960
- Sturrock PR, Maykel JA: Postoperative management, in colorectal surgery. .
- Willett WC, Reynolds RD, Cottrell-Hoehner S, et al. : Validation of a semi-quantitative food frequency questionnaire: Comparison with a 1-year diet record. J Am Diet Assoc 87:43-47, 1987
- Willett WC, Sampson L, Stampfer MJ, et al. : Reproducibility and validity of a semiquantitative food frequency questionnaire. Am J Epidemiol 122:51-65, 1985
- US Department of Agriculture : Composition of Foods: Raw, Processed, and Prepared, 1963-1988. Washington, DC, Department of Agriculture, US Government Printing Office, 1989
- Willett W, Stampfer MJ: Total energy intake: Implications for epidemiologic analyses. Am J Epidemiol 124:17-27, 1986
- Salvini S, Hunter DJ, Sampson L, et al. : Food-based validation of a dietary questionnaire: The effects of week-to-week variation in food consumption. Int J Epidemiol 18:858-867, 1989
- Ogino S, Liao X, Imamura Y, et al. : Predictive and prognostic analysis of PIK3CA mutation in stage III colon cancer intergroup trial. J Natl Cancer Inst 105:1789-1798, 2013
- Ogino S, Shima K, Meyerhardt JA, et al. : Predictive and prognostic roles of BRAF mutation in stage III colon cancer: Results from intergroup trial CALGB 89803. Clin Cancer Res 18:890-900, 2012
- Ogino S, Kawasaki T, Brahmandam M, et al. : Sensitive sequencing method for KRAS mutation detection by pyrosequencing. J Mol Diagn 7:413-421, 2005
- Ogino S, Meyerhardt JA, Irahara N, et al. : KRAS mutation in stage III colon cancer and clinical outcome following intergroup trial CALGB 89803. Clin Cancer Res 15:7322-7329, 2009
- Warren RS, Atreya CE, Niedzwiecki D, et al. : Association of TP53 mutational status and gender with survival after adjuvant treatment for stage III colon cancer: Results of CALGB 89803. Clin Cancer Res 19:5777-5787, 2013
- Bertagnolli MM, Niedzwiecki D, Compton CC, et al: Microsatellite instability predicts improved response to adjuvant therapy with irinotecan, fluorouracil, and leucovorin in stage III colon cancer: Cancer and Leukemia Group B protocol 89803. J Clin Oncol 27:1814-1821, 2009.
- Chan AT, Ogino S, Fuchs CS: Aspirin and the risk of colorectal cancer in relation to the expression of COX-2. N Engl J Med 356:2131-2142, 2007
- Bao Y, Hu FB, Giovannucci EL, et al. : Nut consumption and risk of pancreatic cancer in women. Br J Cancer 109:2911-2916, 2013
- Wang W, Yang M, Kenfield SA, et al. : Nut consumption and prostate cancer risk and mortality. Br J Cancer 115:371-374, 2016
- Yang M, Hu FB, Giovannucci EL, et al. : Nut consumption and risk of colorectal cancer in women. Eur J Clin Nutr 70:333-337, 2016
- Bao Y, Han J, Hu FB, et al. : Association of nut consumption with total and cause-specific mortality. N Engl J Med 369:2001-2011, 2013
- Cox DR: Regression models and life-tables. J R Stat Soc B 34:187-220, 1972
- Yeh C-C, You S-L, Chen C-J, et al. : Peanut consumption and reduced risk of colorectal cancer in women: A prospective study in Taiwan. World J Gastroenterol 12:222-227, 2006
- 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 Biomarkers Prev 13:1595-1603, 2004
- Guasch-Ferré M, Bulló M, Martínez-González MÁ, et al. : Frequency of nut consumption and mortality risk in the PREDIMED nutrition intervention trial. BMC Med 11:164, 2013
- Fernández-Montero A, Bes-Rastrollo M, Barrio-López MT, et al. : Nut consumption and 5-y all-cause mortality in a Mediterranean cohort: The SUN project. Nutrition 30:1022-1027, 2014
- Bonaccio M, Di Castelnuovo A, De Curtis A, et al. : Nut consumption is inversely associated with both cancer and total mortality in a Mediterranean population: Prospective results from the Moli-sani study. Br J Nutr 114:804-811, 2015
- Jiang R, Manson JE, Stampfer MJ, et al. : Nut and peanut butter consumption and risk of type 2 diabetes in women. JAMA 288:2554-2560, 2002
- Villegas R, Gao Y-T, Yang G, et al. : Legume and soy food intake and the incidence of type 2 diabetes in the Shanghai Women’s Health Study. Am J Clin Nutr 87:162-167, 2008
- Pan A, Sun Q, Manson JE, et al. : Walnut consumption is associated with lower risk of type 2 diabetes in women. J Nutr 143:512-518, 2013
- Fernández-Montero A, Bes-Rastrollo M, Beunza JJ, et al. : Nut consumption and incidence of metabolic syndrome after 6-year follow-up: The SUN (Seguimiento Universidad de Navarra, University of Navarra Follow-up) cohort. Public Health Nutr 16:2064-2072, 2013
- Singh PN, Fraser GE: Dietary risk factors for colon cancer in a low-risk population. Am J Epidemiol 148:761-774, 1998
- Djoussé L, Rudich T, Gaziano JM: Nut consumption and risk of hypertension in US male physicians. Clin Nutr 28:10-14, 2009
- Tsai C-J, Leitzmann MF, Hu FB, et al. : A prospective cohort study of nut consumption and the risk of gallstone disease in men. Am J Epidemiol 160:961-968, 2004
- Tsai C-J, Leitzmann MF, Hu FB, et al. : Frequent nut consumption and decreased risk of cholecystectomy in women. Am J Clin Nutr 80:76-81, 2004
- Strate LL, Liu YL, Syngal S, et al. : Nut, corn, and popcorn consumption and the incidence of diverticular disease. JAMA 300:907-914, 2008
- Gopinath B, Buyken AE, Flood VM, et al. : Consumption of polyunsaturated fatty acids, fish, and nuts and risk of inflammatory disease mortality. Am J Clin Nutr 93:1073-1079, 2011
- Torabian S, Haddad E, Rajaram S, et al. : Acute effect of nut consumption on plasma total polyphenols, antioxidant capacity and lipid peroxidation. J Hum Nutr Diet 22:64-71, 2009
- Ma Y, Njike VY, Millet J, et al. : Effects of walnut consumption on endothelial function in type 2 diabetic subjects: A randomized controlled crossover trial. Diabetes Care 33:227-232, 2010
- Tapsell LC, Batterham MJ, Teuss G, et al. : Long-term effects of increased dietary polyunsaturated fat from walnuts on metabolic parameters in type II diabetes. Eur J Clin Nutr 63:1008-1015, 2009
- Lux S, Scharlau D, Schlörmann W, et al. : In vitro fermented nuts exhibit chemopreventive effects in HT29 colon cancer cells. Br J Nutr 108:1177-1186, 2012
- Nagel JM, Brinkoetter M, Magkos F, et al. : Dietary walnuts inhibit colorectal cancer growth in mice by suppressing angiogenesis. Nutrition 28:67-75, 2012
- DeStefano F, Anda RF, Kahn HS, et al. : Dental disease and risk of coronary heart disease and mortality. BMJ 306:688-691, 1993
- Joshipura KJ, Hung H-C, Rimm EB, et al. : Periodontal disease, tooth loss, and incidence of ischemic stroke. Stroke 34:47-52, 2003
- Jimenez M, Krall EA, Garcia RI, et al. : Periodontitis and incidence of cerebrovascular disease in men. Ann Neurol 66:505-512, 2009
- Watt RG, Tsakos G, de Oliveira C, et al. : Tooth loss and cardiovascular disease mortality risk: Results from the Scottish Health Survey. PLoS One 7:e30797, 2012
- Desvarieux M, Demmer RT, Rundek T, et al. : Relationship between periodontal disease, tooth loss, and carotid artery plaque: The Oral Infections and Vascular Disease Epidemiology Study (INVEST). Stroke 34:2120-2125, 2003
- Dietrich T, Jimenez M, Krall Kaye EA, et al. : Age-dependent associations between chronic periodontitis/edentulism and risk of coronary heart disease. Circulation 117:1668-1674, 2008
- Tu Y-K, Galobardes B, Smith GD, et al. : Associations between tooth loss and mortality patterns in the Glasgow Alumni Cohort. Heart 93:1098-1103, 2007
- Migliorati CA: Periodontal diseases and cancer. Lancet Oncol 9:510-512, 2008
- Michaud DS, Liu Y, Meyer M, et al. : Periodontal disease, tooth loss, and cancer risk in male health professionals: A prospective cohort study. Lancet Oncol 9:550-558, 2008
- Abnet CC, Qiao Y-L, Mark SD, et al. : Prospective study of tooth loss and incident esophageal and gastric cancers in China. Cancer Causes Control 12:847-854, 2001
- Garrote LF, Herrero R, Reyes RMO, et al. : Risk factors for cancer of the oral cavity and oro-pharynx in Cuba. Br J Cancer 85:46-54, 2001
- Hiraki A, Matsuo K, Suzuki T, et al. : Teeth loss and risk of cancer at 14 common sites in Japanese. Cancer Epidemiol Biomarkers Prev 17:1222-1227, 2008
- Abnet CC, Kamangar F, Dawsey SM, et al. : Tooth loss is associated with increased risk of gastric non-cardia adenocarcinoma in a cohort of Finnish smokers. Scand J Gastroenterol 40:681-687, 2005
- Boylan MR, Khalili H, Huang ES, et al. : A prospective study of periodontal disease and risk of gastric and duodenal ulcer in male health professionals. Clin Transl Gastroenterol 5:e49, 2014
- Hujoel PP, Drangsholt M, Spiekerman C, et al. : An exploration of the periodontitis-cancer association. Ann Epidemiol 13:312-316, 2003
- Momen-Heravi F, Babic A, Tworoger SS, et al. : Periodontal disease, tooth loss and colorectal cancer risk: Results from the Nurses’ Health Study. Int J Cancer 140:646-652, 2017
- Michaud DS, Fuchs CS, Liu S, et al. : Dietary glycemic load, carbohydrate, sugar, and colorectal cancer risk in men and women. Cancer Epidemiol Biomarkers Prev 14:138-147, 2005
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