The association between dietary inflammatory index and risk of colorectal cancer among postmenopausal women: results from the Women’s Health Initiative

Cancer Causes & Control - Tập 26 - Trang 399-408 - 2014
Fred K. Tabung1,2, Susan E. Steck1,2,3, Yunsheng Ma4, Angela D. Liese2,3, Jiajia Zhang2, Bette Caan5, Lifang Hou6, Karen C. Johnson7, Yasmin Mossavar-Rahmani8, Nitin Shivappa1,2, Jean Wactawski-Wende9, Judith K. Ockene4, James R. Hebert1,2,3
1Cancer Prevention and Control Program, University of South Carolina, Columbia, USA
2Department of Epidemiology and Biostatistics, University of South Carolina, Columbia, USA
3Center for Research in Nutrition and Health Disparities, University of South Carolina, Columbia, USA
4Division of Preventive and Behavioral Medicine, Department of Medicine, University of Massachusetts Medical School, Worcester, USA
5Division of Research, Kaiser Permanente, Oakland, USA
6Department of Preventive Medicine and The Robert H. Lurie Comprehensive Cancer Center, Feinberg School of Medicine, Northwestern University, Chicago, USA
7Department of Preventive Medicine, University of Tennessee Health Science Center, Memphis, USA
8Department of Epidemiology and Population Health, Albert Einstein College of Medicine, Bronx, USA
9Department of Epidemiology and Environmental Health, University at Buffalo, The State University of New York, Buffalo, USA

Tóm tắt

Inflammation is a process central to carcinogenesis and in particular to colorectal cancer (CRC). Previously, we developed a dietary inflammatory index (DII) from extensive literature review to assess the inflammatory potential of diet. In the current study, we utilized this novel index in the Women’s Health Initiative to prospectively evaluate its association with risk of CRC in postmenopausal women. The DII was calculated from baseline food frequency questionnaires administered to 152,536 women aged 50–79 years without CRC at baseline between 1993 and 1998 and followed through 30 September 2010. Incident CRC cases were ascertained through a central physician adjudication process. Multiple covariate-adjusted Cox proportional hazards regression models were used to estimate hazard ratios (HR) and 95 % confidence intervals (95 % CI) for colorectal, colon (proximal/distal locations), and rectal cancer risk, by DII quintiles (Q). During an average 11.3 years of follow-up, a total of 1,920 cases of CRC (1,559 colon and 361 rectal) were identified. Higher DII scores (representing a more pro-inflammatory diet) were associated with an increased incidence of CRC (HRQ5–Q1 1.22; 95 % CI 1.05, 1.43; p trend = 0.02) and colon cancer, specifically proximal colon cancer (HRQ5–Q1 1.35; 95 % CI 1.05, 1.67; p trend = 0.01) but not distal colon cancer (HRQ5–Q1 0.84; 95 % CI 0.61, 1.18; p trend = 0.63) or rectal cancer (HRQ5–Q1 1.20; 95 % CI 0.84, 1.72; p trend = 0.65). Consumption of pro-inflammatory diets is associated with an increased risk of CRC, especially cancers located in the proximal colon. The absence of a significant association for distal colon cancer and rectal cancer may be due to the small number of incident cases for these sites. Interventions that may reduce the inflammatory potential of the diet are warranted to test our findings, thus providing more information for colon cancer prevention.

Tài liệu tham khảo

Villaseñor A, Ambs A, Ballard-Barbash R, Baumgartner KB, McTiernan A, Ulrich CM, Neuhouser ML (2011) Dietary fiber is associated with circulating concentrations of C-reactive protein in breast cancer survivors: the heal Study. Breast Cancer Res Treat 129:485–494 Esmaillzadeh A, Kimiagar M, Mehrabi Y, Azadbakht L, Hu FB, Willett WC (2007) Dietary patterns and markers of systemic inflammation among iranian women. J Nutr 137:992–998 Chrysohoou C, Panagiotakos DB, Pitsavos C, Das UN, Stefanadis C (2004) Adherence to the Mediterranean diet attenuates inflammation and coagulation process in healthy adults: the Attica Study. J Am Coll Cardiol 44:152–158 Galland L (2010) Diet and inflammation. Nutr Clin Pract 25:634–640 Ullman T, Itzkowitz SH (2011) Intestinal inflammation and cancer. Gastroenterology 140:1807–1816 Ananthakrishnan A, Cheng SC, Cai T, Cagan A, Gainer VS, Szolovits P, Shaw SY, Churchill S, Karlson EW, Murphy SN, Kohane I, Liao KP (2014) Serum inflammatory markers and risk of colorectal cancer in patients with inflammatory bowel diseases. Clin Gastroenterol Hepatol 12(1342–8):e1 Dubé C, Rostom A, Lewin G, Tsertsvadze A, Barrowman N, Code C, Sampson M, Moher D, U.S. Preventive Services Task Force (2007) The use of aspirin for primary prevention of colorectal cancer: a systematic review prepared for the U.S. Preventive Services Task Force. Ann Intern Med 146:365–375 Rostom A, Dubé C, Lewin G, Tsertsvadze A, Barrowman N, Code C, Sampson M, Moher D, U.S. Preventive Services Task Force (2007) Nonsteroidal anti-inflammatory drugs and cyclooxygenase-2 inhibitors for primary prevention of colorectal cancer: a systematic review prepared for the U.S. Preventive Services Task Force. Ann Intern Med 146:376–389 Balkwill F, Charles KA, Mantovani A (2005) Smoldering and polarized inflammation in the initiation and promotion of malignant disease. Cancer Cell 7:211–217 Nanri A, Moore MA, Kono S (2007) Impact of C-reactive protein on disease risk and its relation to dietary factors: literature review. Asian Pac J Cancer Prev 8:167–177 Hlebowicz J, Persson M, Gullberg B, Sonestedt E, Wallström P, Drake I, Nilsson J, Hedblad B, Wirfält E (2011) Food patterns, inflammation markers and incidence of cardiovascular disease: the Malmö Diet and Cancer study. J Intern Med 270:365–376 Rennie K, Hughes J, Lang R, Jebb SA (2003) Nutritional management of rheumatoid arthritis: a review of the evidence. J Hum Nutr Diet 16:97–109 Raphael W, Sordillo L (2013) Dietary polyunsaturated fatty acids and inflammation: the role of phospholipid biosynthesis. Int J Mol Sci 14:21167–21188 Liu S, Manson JE, Buring JE, Stampfer MJ, Willett WC, Ridker PM (2002) Relation between a diet with a high glycemic load and plasma concentrations of high-sensitivity C-reactive protein in middle-aged women. Am J Clin Nutr 75:492–498 Peairs A, Rankin JW, Lee YW (2011) Effects of acute ingestion of different fats on oxidative stress and inflammation in overweight and obese adults. Nutr J 10:122 World Cancer Research Fund and the American Institute for Cancer Research (2007) Food, nutrition and prevention of cancer: a global perspective. American Institute for Cancer Research, Washington Hu F (2002) Dietary pattern analysis: a new direction in nutritional epidemiology. Curr Opin Lipidol 13:3–9 Randall E, Marshall JR, Graham S, Brasure J (1990) Patterns in food use and their associations with nutrient intakes. Am J Clin Nutr 52:739–745 Kant AK (1996) Indexes of overall diet quality: a review. J Am Diet Assoc 96:785–791 Shivappa N, Steck SE, Hurley TG, Hussey JR, Hebert JR (2013) Designing and developing a literature-derived, population-based dietary inflammatory index. Public Health Nutr 17:1689–1696 Shivappa N, Steck SE, Hurley TG, Hussey JR, Ma Y, Ockene IS, Tabung FK, Hebert JR (2013) A population-based dietary inflammatory index predicts levels of C-reactive protein in the Seasonal Variation of Blood Cholesterol Study (SEASONS). Public Health Nutrition. 17:1825–1833 Shivappa N, Prizment AE, Blair CK, Jacobs DR Jr, Steck SE, Hebert JR (2014) Dietary inflammatory index (DII) and risk of colorectal cancer in Iowa Women’s Health Study. Cancer Epidemiol Biomark Prev 23:2383–2392 Zamora-Ros R, Shivappa N, Steck SE et al (2015) Dietary inflammatory index and inflammatory gene interactions in relation to colorectal cancer risk in the Bellvitge colorectal cancer case–control study. Genes Nutr 10:447 Women’s Health Initiative Study Group (1998) Design of the Women’s Health Initiative clinical trial and observational study. Control Clin Trials 19:61–109 Patterson R, Kristal AR, Tinker LF, Carter RA, Bolton MP, Agurs-Collins T (1999) Measurement characteristics of the Women’s Health Initiative food frequency questionnaire. Ann Epidemiol 9:178–187 Ma Y, Hébert JR, Li W, Bertone-Johnson ER, Olendzki B, Pagoto SL, Tinker L, Rosal MC, Ockene IS, Ockene JK, Griffith JA, Liu S (2008) Association between dietary fiber and markers of systemic inflammation in the Women’s Health Initiative Observational Study. Nutrition 24:941–949 Patterson RE, Kristal A, Rodabough R et al (2003) Changes in food sources of dietary fat in response to an intensive low-fat dietary intervention: early results from the Women’s Health Initiative. J Am Diet Assoc 103:454–460 Nutrition Coordinating Center at the University of Minnesota M, MN (2013) Nutrition Data System for Research (NDSR). University of Minnesota, Minneapolis, MN Neuhouser ML, Tinker L, Shaw PA et al (2008) Use of recovery biomarkers to calibrate nutrient consumption self-reports in the Women’s Health Initiative. Am J Epidemiol 167:1247–1259 Prentice RL, Mossavar-Rahmani Y, Huang Y et al (2011) Evaluation and comparison of food records, recalls, and frequencies for energy and protein assessment by using recovery biomarkers. Am J Epidemiol 174:591–603 Curb J, McTiernan A, Heckbert SR, Kooperberg C, Stanford J, Nevitt M, Johnson KC, Proulx-Burns L, Pastore L, Criqui M, Daugherty S, WHI Morbidity and Mortality Committee (2003) Outcomes ascertainment and adjudication methods in the Women’s Health Initiative. Ann Epidemiol 13:S122–S128 Department of Health and Human Services (2008) Physical activity guidelines for Americans. DHHS, Washington DC Miller P, Cross AJ, Subar AF, Krebs-Smith SM, Park Y, Powell-Wiley T, Hollenbeck A, Reedy J (2013) Comparison of 4 established DASH diet indexes: examining associations of index scores and colorectal cancer. Am J Clin Nutr 98:794–803 Fung T, Hu FB, Wu K, Chiuve SE, Fuchs CS, Giovannucci E (2010) The Mediterranean and Dietary Approaches to Stop Hypertension (DASH) diets and colorectal cancer. Am J Clin Nutr 92:1429–1435 Reedy J, Mitrou PN, Krebs-Smith SM, Wirfält E, Flood A, Kipnis V, Leitzmann M, Mouw T, Hollenbeck A, Schatzkin A, Subar AF (2008) Index-based dietary patterns and risk of colorectal cancer. Am J Epidemiol 168:38–48 Romaguera D, Vergnaud AC, Peeters PH, van Gils CH, Chan DS, Ferrari P, Romieu I, Jenab M, Slimani N, Clavel-Chapelon F, Fagherazzi G, Perquier F, Kaaks R, Teucher B, Boeing H, von Rüsten A, Tjønneland A, Olsen A, Dahm CC, Overvad K, Quirós JR, Gonzalez CA, Sánchez MJ, Navarro C, Barricarte A, Dorronsoro M, Khaw KT, Wareham NJ, Crowe FL, Key TJ, Trichopoulou A, Lagiou P, Bamia C, Masala G, Vineis P, Tumino R, Sieri S, Panico S, May AM, Bueno-de-Mesquita HB, Büchner FL, Wirfält E, Manjer J, Johansson I, Hallmans G, Skeie G, Benjaminsen Borch K, Parr CL, Riboli E, Norat T (2012) 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 96:150–163 Steck S, Shivappa N, Tabung FK, Harmon BE, Wirth MD, Hurley TG, Hebert JR (2014) The dietary inflammatory index: a new tool for assessing diet quality based on inflammatory potential. Digest 49:1–9 Beresford S, Johnson KC, Ritenbaugh C, Lasser NL, Snetselaar LG, Black HR, Anderson GL, Assaf AR, Bassford T, Bowen D, Brunner RL, Brzyski RG, Caan B, Chlebowski RT, Gass M, Harrigan RC, Hays J, Heber D, Heiss G, Hendrix SL, Howard BV, Hsia J, Hubbell FA, Jackson RD, Kotchen JM, Kuller LH, LaCroix AZ, Lane DS, Langer RD, Lewis CE, Manson JE, Margolis KL, Mossavar-Rahmani Y, Ockene JK, Parker LM, Perri MG, Phillips L, Prentice RL, Robbins J, Rossouw JE, Sarto GE, Stefanick ML, Van Horn L, Vitolins MZ, Wactawski-Wende J, Wallace RB, Whitlock E (2006) Low-fat dietary pattern and risk of colorectal cancer: the Women’s Health Initiative Randomized Controlled Dietary Modification Trial. J Am Med Assoc 295:643–654 Caan B, Coates AO, Slattery ML, Potter JD, Quesenberry CP Jr, Edwards SM (1998) Body size and the risk of colon cancer in a large case–control study. Int J Obes Relat Metab Disord 22:178–184 Slattery M, Caan BJ, Benson J, Murtaugh M (2003) Energy balance and rectal cancer: an evaluation of energy intake, energy expenditure, and body mass index. Nutr Cancer 46:166–171 Slattery M, Curtin K, Wolff RK, Boucher KM, Sweeney C, Edwards S, Caan BJ, Samowitz W (2009) A comparison of colon and rectal somatic DNA alterations. Dis Colon Rectum 52:1304–1311 Rosenberg R, Maak M, Schuster T, Becker K, Friess H, Gertler R (2010) Does a rectal cancer of the upper third behave more like a colon or a rectal cancer? Dis Colon Rectum 53:761–770 Konishi K, Fujii T, Boku N, Kato S, Koba I, Ohtsu A, Tajiri H, Ochiai A, Yoshida S (1999) Clinicopathological differences between colonic and rectal carcinomas: Are they based on the same mechanism of carcinogenesis? Gut 45:818–821 Tabung FK, Steck SE, Burch JB, Chen CF, Zhang H, Hurley TG, Cavicchia P, Alexander M, Shivappa N, Creek KE, Lloyd SC, Hebert JR (2014) A healthy lifestyle index is associated with reduced risk of colorectal adenomatous polyps among non-users of non-steroidal anti-inflammatory drugs. J Prim Prevent 1–11. Epub ahead of print. doi:10.1007/s10935-014-0372-1 Hauret KG, Bostick RM, Matthews CE, Hussey JR, Fina MF, Geisinger KR, Roufail WM (2004) Physical activity and reduced risk of incident sporadic colorectal adenomas: observational support for mechanisms involving energy balance and inflammation modulation. Am J Epidemiol 159:983–992 Hartman TJ, Yu B, Albert PS, Slattery ML, Paskett E, Kikendall JW, Iber F, Brewer BK, Schatzkin A, Lanza E (2005) Does nonsteroidal anti-inflammatory drug use modify the effect of a low-fat, high-fiber diet on recurrence of colorectal adenomas? Cancer Epidemiol Biomark Prev 14:2359–2365 Monteleone G, Pallone F, Stolfi C (2012) The dual role of inflammation in colon carcinogenesis. Int J Mol Sci 13:11071–11084 Balkwill F (2004) Cancer and the chemokine network. Nat Rev Cancer 4:540–550 Taniguchi K, Karin M (2014) IL-6 and related cytokines as the critical lynchpins between inflammation and cancer. Semin Immunol 26:54–74. Toriola A, Cheng TY, Neuhouser ML, Wener MH, Zheng Y, Brown E, Miller JW, Song X, Beresford SA, Gunter MJ, Caudill MA, Ulrich CM (2013) Biomarkers of inflammation are associated with colorectal cancer risk in women but are not suitable as early detection markers. Int J Cancer 132:2648–2658 Wu J, Cai Q, Li H, Cai H, Gao J, Yang G, Zheng W, Xiang YB, Shu XO (2013) Circulating C-reactive protein and colorectal cancer risk: a report from the shanghai men’s health study. Carcinogenesis 34:2799–2803 Bruce W, Wolever TM, Giacca A (2000) Mechanisms linking diet and colorectal cancer: the possible role of insulin resistance. Nutr Cancer 37:19–26 Giovannucci E (1995) Insulin and colon cancer. Cancer Causes Control 6:164–179 Wirth M, Burch J, Shivappa N, Violanti JM, Burchfiel CM, Fekedulegn D, Andrew ME, Hartley TA, Miller DB, Mnatsakanova A, Charles LE, Steck SE, Hurley TG, Vena JE, Hébert JR (2014) Association of a dietary inflammatory index with inflammatory indices and metabolic syndrome among police officers. J Occup Environ Med 56:986–989