Dietary Inflammatory Index and Risk of Colorectal Cancer: A Case-Control Study in Korea
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Population
2.2. Dietary Assessment and Calculation of the DII
2.3. Data Analysis
3. Results
4. Discussion
Supplementary Materials
Acknowledgments
Author Contributions
Conflicts of Interest
Abbreviations
BMI | Body mass index |
CI | Confidence interval |
DII | Dietary inflammatory index |
FFQ | Food frequency questionnaire |
OR | Odds ratio |
SD | Standard deviation |
T | Tertile |
References
- Coussens, L.M.; Werb, Z. Inflammation and cancer. Nature 2002, 420, 860–867. [Google Scholar] [CrossRef] [PubMed]
- Triantafillidis, J.K.; Nasioulas, G.; Kosmidis, P.A. Colorectal cancer and inflammatory bowel disease: Epidemiology, risk factors, mechanisms of carcinogenesis and prevention strategies. Anticancer Res. 2009, 29, 2727–2737. [Google Scholar] [PubMed]
- Bernstein, C.N.; Blanchard, J.F.; Kliewer, E.; Wajda, A. Cancer risk in patients with inflammatory bowel disease: A population-based study. Cancer 2001, 91, 854–862. [Google Scholar] [CrossRef]
- Flossmann, E.; Rothwell, P.M. Effect of aspirin on long-term risk of colorectal cancer: Consistent evidence from randomised and observational studies. Lancet 2007, 369, 1603–1613. [Google Scholar] [CrossRef]
- Miller, P.E.; Lazarus, P.; Lesko, S.M.; Cross, A.J.; Sinha, R.; Laio, J.; Zhu, J.; Harper, G.; Muscat, J.E.; Hartman, T.J. Meat-related compounds and colorectal cancer risk by anatomical subsite. Nutr. Cancer 2013, 65, 202–226. [Google Scholar] [CrossRef] [PubMed]
- Parr, C.L.; Hjartaker, A.; Lund, E.; Veierod, M.B. Meat intake, cooking methods and risk of proximal colon, distal colon and rectal cancer: The Norwegian Women and Cancer (NOWAC) cohort study. Int. J. Cancer 2013, 133, 1153–1163. [Google Scholar] [CrossRef] [PubMed]
- Song, M.; Garrett, W.S.; Chan, A.T. Nutrients, foods, and colorectal cancer prevention. Gastroenterology 2015, 148, 1244–1260. [Google Scholar] [CrossRef] [PubMed]
- Hu, F.B. Dietary pattern analysis: A new direction in nutritional epidemiology. Curr. Opin. Lipidol. 2002, 13, 3–9. [Google Scholar] [CrossRef] [PubMed]
- Shivappa, N.; Zucchetto, A.; Montella, M.; Serraino, D.; Steck, S.E.; La Vecchia, C.; Hebert, J.R. Inflammatory potential of diet and risk of colorectal cancer: A case-control study from Italy. Br. J. Nutr. 2015, 114, 152–158. [Google Scholar] [CrossRef] [PubMed]
- Shivappa, N.; Steck, S.E.; Hurley, T.G.; Hussey, J.R.; Hebert, J.R. Designing and developing a literature-derived, population-based dietary inflammatory index. Public Health Nutr. 2014, 17, 1689–1696. [Google Scholar] [CrossRef] [PubMed]
- Shivappa, N.; Jackson, M.D.; Bennett, F.; Hebert, J.R. Increased Dietary Inflammatory Index (DII) is associated with increased risk of prostate cancer in Jamaican men. Nutr. Cancer 2015, 67, 941–948. [Google Scholar] [CrossRef] [PubMed]
- Shivappa, N.; Steck, S.E.; Hurley, T.G.; Hussey, J.R.; Ma, Y.; Ockene, I.S.; Tabung, F.; Hebert, J.R. A population-based dietary inflammatory index predicts levels of C-reactive protein in the Seasonal Variation of Blood Cholesterol Study (SEASONS). Public Health Nutr. 2014, 17, 1825–1833. [Google Scholar] [CrossRef] [PubMed]
- Wirth, M.D.; Burch, J.; Shivappa, N.; Violanti, J.M.; Burchfiel, C.M.; Fekedulegn, D.; Andrew, M.E.; Hartley, T.A.; Miller, D.B.; Mnatsakanova, A.; et al. Association of a dietary inflammatory index with inflammatory indices and metabolic syndrome among police officers. J. Occup. Environ. Med. 2014, 56, 986–989. [Google Scholar] [CrossRef] [PubMed]
- Wood, L.G.; Shivappa, N.; Berthon, B.S.; Gibson, P.G.; Hebert, J.R. Dietary inflammatory index is related to asthma risk, lung function and systemic inflammation in asthma. Clin. Exp. Allergy 2015, 45, 177–183. [Google Scholar] [CrossRef] [PubMed]
- Shivappa, N.; Prizment, A.E.; Blair, C.K.; Jacobs, D.R., Jr.; Steck, S.E.; Hebert, J.R. Dietary inflammatory index and risk of colorectal cancer in the Iowa Women’s Health Study. Cancer Epidemiol. Biomark. Prev. 2014, 23, 2383–2392. [Google Scholar] [CrossRef] [PubMed]
- Wirth, M.D.; Shivappa, N.; Steck, S.E.; Hurley, T.G.; Hebert, J.R. The dietary inflammatory index is associated with colorectal cancer in the National Institutes of Health-American Association of Retired Persons Diet and Health Study. Br. J. Nutr. 2015, 113, 1819–1827. [Google Scholar] [CrossRef] [PubMed]
- Tabung, F.K.; Steck, S.E.; Ma, Y.; Liese, A.D.; Zhang, J.; Caan, B.; Hou, L.; Johnson, K.C.; Mossavar-Rahmani, Y.; Shivappa, N.; et al. The association between dietary inflammatory index and risk of colorectal cancer among postmenopaUSAl women: Results from the Women’s Health Initiative. Cancer Causes Control 2015, 26, 399–408. [Google Scholar] [CrossRef] [PubMed]
- Shin, A.; Kim, K.Z.; Jung, K.W.; Park, S.; Won, Y.J.; Kim, J.; Kim, D.Y.; Oh, J.H. Increasing trend of colorectal cancer incidence in Korea, 1999–2009. Cancer Res. Treat. 2012, 44, 219–226. [Google Scholar] [CrossRef] [PubMed]
- Ahn, Y.; Kwon, E.; Shim, J.E.; Park, M.K.; Joo, Y.; Kimm, K.; Park, C.; Kim, D.H. Validation and reproducibility of food frequency questionnaire for Korean genome epidemiologic study. Eur. J. Clin. Nutr. 2007, 61, 1435–1441. [Google Scholar] [CrossRef] [PubMed]
- Tabung, F.K.; Steck, S.E.; Zhang, J.; Ma, Y.; Liese, A.D.; Agalliu, I.; Hingle, M.; Hou, L.; Hurley, T.G.; Jiao, L.; et al. Construct validation of the dietary inflammatory index among postmenopaUSAl women. Ann. Epidemiol. 2015, 25, 398–405. [Google Scholar] [CrossRef] [PubMed]
- Willett, W.C. Nutritional Epidemiology, 3rd ed.; Oxford University Press: New York, NY, USA, 2012. [Google Scholar]
- World Health Organization. International Statistical Classification of Diseases and Related Health Problems; 10th revision; World Health Organization: Geneva, Switzerland, 2011. [Google Scholar]
- D’Avanzo, B.; La Vecchia, C.; Katsouyanni, K.; Negri, E.; Trichopoulos, D. An assessment, and reproducibility of food frequency data provided by hospital controls. Eur. J. Cancer Prev. 1997, 6, 288–293. [Google Scholar] [CrossRef] [PubMed]
- Sijtsma, F.P.; Meyer, K.A.; Steffen, L.M.; Shikany, J.M.; Van Horn, L.; Harnack, L.; Kromhout, D.; Jacobs, D.R., Jr. Longitudinal trends in diet and effects of sex, race, and education on dietary quality score change: The Coronary Artery Risk Development in Young Adults study. Am. J. Clin. Nutr. 2012, 95, 580–586. [Google Scholar] [CrossRef] [PubMed]
- Zamora-Ros, R.; Shivappa, N.; Steck, S.E.; Canzian, F.; Landi, S.; Alonso, M.H.; Hébert, J.R.; Moreno, V. Dietary inflammatory index and inflammatory gene interactions in relation to colorectal cancer risk in the Bellvitge colorectal cancer case-control study. Genes Nutr. 2015, 10. [Google Scholar] [CrossRef] [PubMed]
- Magalhaes, B.; Peleteiro, B.; Lunet, N. Dietary patterns and colorectal cancer: Systematic review and meta-analysis. Eur. J. Cancer Prev. 2012, 21, 15–23. [Google Scholar] [CrossRef] [PubMed]
- Miller, P.E.; Lesko, S.M.; Muscat, J.E.; Lazarus, P.; Hartman, T.J. Dietary patterns and colorectal adenoma and cancer risk: A review of the epidemiological evidence. Nutr. Cancer 2010, 62, 413–424. [Google Scholar] [CrossRef] [PubMed]
- Kim, M.K.; Sasaki, S.; Otani, T.; Tsugane, S. Dietary patterns and subsequent colorectal cancer risk by subsite: A prospective cohort study. Int. J. Cancer 2005, 115, 790–798. [Google Scholar] [CrossRef] [PubMed]
- 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. [Google Scholar] [CrossRef] [PubMed]
- Festa, A.; D’Agostino, R., Jr.; Howard, G.; Mykkanen, L.; Tracy, R.P.; Haffner, S.M. Chronic subclinical inflammation as part of the insulin resistance syndrome: The Insulin Resistance Atherosclerosis Study (IRAS). Circulation 2000, 102, 42–47. [Google Scholar] [CrossRef] [PubMed]
- Bruce, W.R.; Giacca, A.; Medline, A. Possible mechanisms relating diet and risk of colon cancer. Cancer Epidemiol. Biomark. Prev. 2000, 9, 1271–1279. [Google Scholar]
- Giovannucci, E. Insulin and colon cancer. Cancer Causes Control 1995, 6, 164–179. [Google Scholar] [CrossRef] [PubMed]
- Chan, A.T.; Giovannucci, E.L. Primary prevention of colorectal cancer. Gastroenterology 2010, 138, 2029–2043. [Google Scholar] [CrossRef] [PubMed]
- Vargas, A.J.; Thompson, P.A. Diet and nutrient factors in colorectal cancer risk. Nutr. Clin. Pract. 2012, 27, 613–623. [Google Scholar] [CrossRef] [PubMed]
- Wei, E.K.; Giovannucci, E.; Wu, K.; Rosner, B.; Fuchs, C.S.; Willett, W.C.; Colditz, G.A. ComParison of risk factors for colon and rectal cancer. Int. J. Cancer 2004, 108, 433–442. [Google Scholar] [CrossRef] [PubMed]
- Iacopetta, B. Are there two sides to colorectal cancer? Int. J. Cancer 2002, 101, 403–408. [Google Scholar] [CrossRef] [PubMed]
- Terry, P.D.; Miller, A.B.; Rohan, T.E. Obesity and colorectal cancer risk in women. Gut 2002, 51, 191–194. [Google Scholar] [CrossRef] [PubMed]
- Chlebowski, R.T.; Wactawski-Wende, J.; Ritenbaugh, C.; Hubbell, F.A.; Ascensao, J.; Rodabough, R.J.; Rosenberg, C.A.; Taylor, V.M.; Harris, R.; Chen, C.; et al. Estrogen plus progestin and colorectal cancer in postmenopaUSAl women. N. Engl. J. Med. 2004, 350, 991–1004. [Google Scholar] [CrossRef] [PubMed]
- US Preventive Services Task Force. Screening for colorectal cancer: US preventive services task force recommendation statement. Ann. Intern. Med. 2008, 149, 627–637. [Google Scholar]
- Pischon, T.; Hankinson, S.E.; Hotamisligil, G.S.; Rifai, N.; Rimm, E.B. Leisure-time physical activity and reduced plasma levels of obesity-related inflammatory markers. Obes. Res. 2003, 11, 1055–1064. [Google Scholar] [CrossRef] [PubMed]
- Song, M.; Wu, K.; Ogino, S.; Fuchs, C.S.; Giovannucci, E.L.; Chan, A.T. A prospective study of plasma inflammatory markers and risk of colorectal cancer in men. Br. J. Cancer 2013, 108, 1891–1898. [Google Scholar] [CrossRef] [PubMed]
Controls (n = 1846) | Cases (n = 923) | p-Value | |
---|---|---|---|
Age (years) | 56.1 ± 9.1 | 56.6 ± 9.7 | 0.20 |
FeMale | 596 (32.3) | 298 (32.3) | >0.99 |
Family history of colorectal cancer | 99 (5.4) | 99 (10.7) | <0.001 |
BMI (kg/m2) | |||
<25 | 1226 (66.4) | 640 (69.3) | 0.12 |
≥25 | 620 (33.6) | 283 (30.7) | |
Educational level | |||
Middle school or less | 282 (15.6) | 321 (34.8) | <0.001 |
High school | 587 (32.6) | 369 (40.0) | |
College or more | 934 (51.8) | 233 (25.2) | |
Occupation | |||
Professional, office | 481 (26.4) | 189 (20.5) | <0.001 |
Service, sales | 403 (22.1) | 38 (4.1) | |
Agriculture, mining, manufacturing | 241 (13.2) | 141 (15.3) | |
Housewife, other | 698 (38.3) | 555 (60.1) | |
Monthly Household Income 2 | |||
<200 | 388 (23.0) | 321 (34.8) | <0.001 |
200−<400 | 754 (44.7) | 387 (41.9) | |
≥400 | 545 (32.3) | 215 (23.3) | |
Marital Status | |||
Married | 1654 (90.4) | 773 (83.8) | <0.001 |
Unmarried | 176 (9.6) | 150 (16.3) | |
Smoking status | |||
Non-smoker | 818 (44.3) | 409 (44.3) | 0.16 |
Former smoker | 687 (37.2) | 318 (34.5) | |
Current smoker | 341 (18.5) | 196 (21.2) | |
Alcohol Consumption | |||
Non-drinker | 560 (30.3) | 279 (30.2) | <0.001 |
Former drinker | 169 (9.2) | 129(14.0) | |
Current drinker | 1117 (60.5) | 515 (55.8) | |
Total caloric intake (Kcal/day) | 1689.6 ± 560.4 | 2026.3 ± 534.0 | <0.001 |
Sum of DII | 1.07 ± 2.24 | 1.80 ± 1.97 | <0.001 |
Physical activity (yes) | 1047 (58.2) | 311 (33.7) | <0.001 |
DII Score | No. Controls/Cases | Crude OR (95% CI) | Adjusted 2 OR (95% CI) |
---|---|---|---|
Colorectal Cancer | |||
T1 | 616/197 | 1.0 (ref.) | 1.0 (ref.) |
T2 | 615/319 | 1.62 (1.32, 2.00) | 1.99 (1.57, 2.53) |
T3 | 615/407 | 2.07 (1.69, 2.54) | 2.16 (1.71, 2.73) |
p for trend | <0.001 | <0.001 | |
Colon Cancer | |||
T1 | 616/102 | 1.0 (ref.) | 1.0 (ref.) |
T2 | 615/168 | 1.65 (1.26, 2.16) | 2.08 (1.55, 2.79) |
T3 | 615/190 | 1.87 (1.43, 2.43) | 2.05 (1.53, 2.74) |
p for trend | <0.001 | <0.001 | |
Proximal Colon Cancer | |||
T1 | 616/38 | 1.0 (ref.) | 1.0 (ref.) |
T2 | 615/66 | 1.74 (1.15, 2.63) | 2.11 (1.37, 3.27) |
T3 | 615/61 | 1.61 (1.06, 2.45) | 1.68 (1.08, 2.61) |
p for trend | 0.02 | 0.02 | |
Distal Colon Cancer | |||
T1 | 616/64 | 1.0 (ref.) | 1.0 (ref.) |
T2 | 615/102 | 1.60 (1.15, 2.23) | 2.06 (1.44, 2.93) |
T3 | 615/129 | 2.02 (1.47, 2.78) | 2.28 (1.61, 3.21) |
p for trend | <0.001 | <0.001 | |
Rectal Cancer | |||
T1 | 616/92 | 1.0 (ref.) | 1.0 (ref.) |
T2 | 615/147 | 1.60 (1.21, 2.13) | 1.90 (1.40, 2.59) |
T3 | 615/205 | 2.23 (1.70, 2.92) | 2.23 (1.66, 3.00) |
p for trend | <0.001 | <0.001 |
DII Score | Men | Women | ||||
---|---|---|---|---|---|---|
No. Controls/Cases | Crude OR (95% CI) | Adjusted OR 2 (95% CI) | No. Controls/Cases | Crude OR (95% CI) | Adjusted OR 2 (95% CI) | |
Colorectal Cancer | ||||||
T1 | 417/150 | 1.0 (ref.) | 1.0 (ref.) | 199/56 | 1.0 (ref.) | 1.0 (ref.) |
T2 | 417/211 | 1.41 (1.10, 1.81) | 1.68 (1.26, 2.24) | 199/98 | 1.75 (1.19, 2.57) | 1.92 (1.24, 2.98) 3.57) |
T3 | 416/264 | 1.80 (1.39, 2.25) | 1.72 (1.30, 2.28) | 198/144 | 2.58 (1.79, 3.73) | 2.50 (1.64, 3.82) |
p for trend | <0.001 | <0.001 | <0.001 | <0.001 | ||
Colon Cancer | ||||||
T1 | 417/73 | 1.0 (ref.) | 1.0 (ref.) | 199/31 | 1.0 (ref.) | 1.0 (ref.) |
T2 | 417/100 | 1.37 (0.98, 1.91) | 1.70 (1.18, 2.44) | 199/58 | 1.87 (1.16, 3.02) | 2.07 (1.22, 3.51) |
T3 | 416/120 | 1.65 (1.20, 2.27) | 1.67 (1.18, 2.37) | 199/78 | 2.53 (1.60, 4.01) | 2.52 (1.51, 4.21) |
p for trend | 0.002 | 0.004 | <0.001 | <0.001 | ||
Proximal Colon Cancer | ||||||
T1 | 417/27 | 1.0 (ref.) | 1.0 (ref.) | 199/11 | 1.0 (ref.) | 1.0 (ref.) |
T2 | 417/45 | 1.67 (1.02, 2.74) | 2.08 (1.23, 3.50) | 199/16 | 1.46 (0.66, 3.21) | 1.48 (0.64, 3.41) |
T3 | 416/40 | 1.49 (0.90, 2.47) | 1.51 (0.89, 2.57) | 198/26 | 2.38 (1.14, 4.94) | 2.23 (1.02, 4.89) |
p for trend | 0.11 | 0.10 | 0.02 | 0.04 | ||
Distal Colon Cancer | ||||||
T1 | 417/46 | 1.0 (ref.) | 1.0 (ref.) | 199/20 | 1.0 (ref.) | 1.0 (ref.) |
T2 | 417/55 | 1.20 (0.79, 1.81) | 1.48 (0.96, 2.30) | 199/42 | 2.10 (1.19, 3.70) | 2.42 (1.31, 4.48) |
T3 | 416/80 | 1.74 (1.18, 2.57) | 1.76 (1.17, 2.66) | 198/52 | 2.61 (1.51, 4.54) | 2.69 (1.47, 4.92) |
p for trend | 0.005 | 0.007 | <0.001 | 0.002 | ||
Rectal Cancer | ||||||
T1 | 417/76 | 1.0 (ref.) | 1.0 (ref.) | 199/23 | 1.0 (ref.) | 1.0 (ref.) |
T2 | 417/106 | 1.40 (1.01, 1.93) | 1.61 (1.12, 2.31) | 199/40 | 1.74 (1.00, 3.01) | 1.85 (1.02, 3.36) |
T3 | 416/138 | 1.82 (1.33, 2.48) | 1.73 (1.23, 2.44) | 198/61 | 2.67 (1.59, 4.48) | 2.44 (1.38, 4.32) |
p for trend | <0.001 | 0.002 | <0.001 | 0.002 |
Dietary Inflammatory Index | p for Interaction | ||||||
---|---|---|---|---|---|---|---|
T1 | T2 | T3 | |||||
No. Controls/Cases | OR (95% CI) 2 | No. Controls/Cases | OR (95% CI) 2 | No. Controls/Cases | OR (95% CI) 2 | ||
Age | |||||||
<50 years old | 116/55 | 1.0 (ref.) | 135/57 | 0.94 (0.58, 1.55) | 169/98 | 1.17 (0.75, 1.85) | 0.004 |
≥50 years old | 500/142 | 1.0 (ref.) | 480/262 | 2.48 (1.87, 3.28) | 446/309 | 2.61 (1.98, 3.43) | |
BMI (kg/m2) | |||||||
<25 | 399/126 | 1.0 (ref.) | 421/231 | 2.23 (1.65, 3.00) | 406/283 | 2.34 (1.75, 3.14) | 0.58 |
≥25 | 217/71 | 1.0 (ref.) | 194/88 | 1.65 (1.09, 2.49) | 209/124 | 1.84 (1.25, 2.72) | |
Physical Activity | |||||||
No | 195/134 | 1.0 (ref.) | 254/211 | 1.54 (1.12, 2.13) | 304/267 | 1.49 (1.09, 2.03) | <0.001 |
Yes | 411/63 | 1.0 (ref.) | 341/108 | 2.67 (1.83, 3.89) | 295/140 | 3.42 (2.37, 4.95) | |
Smoking Status | |||||||
Never | 310/91 | 1.0 (ref.) | 270/156 | 2.63 (1.85, 3.75) | 239/162 | 2.58 (1.81, 3.68) | 0.03 |
Ever | 307/106 | 1.0 (ref.) | 345/163 | 1.50 (1.07, 2.09) | 376/245 | 1.79 (1.31, 2.45) |
© 2016 by the authors; licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC-BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Cho, Y.A.; Lee, J.; Oh, J.H.; Shin, A.; Kim, J. Dietary Inflammatory Index and Risk of Colorectal Cancer: A Case-Control Study in Korea. Nutrients 2016, 8, 469. https://doi.org/10.3390/nu8080469
Cho YA, Lee J, Oh JH, Shin A, Kim J. Dietary Inflammatory Index and Risk of Colorectal Cancer: A Case-Control Study in Korea. Nutrients. 2016; 8(8):469. https://doi.org/10.3390/nu8080469
Chicago/Turabian StyleCho, Young Ae, Jeonghee Lee, Jae Hwan Oh, Aesun Shin, and Jeongseon Kim. 2016. "Dietary Inflammatory Index and Risk of Colorectal Cancer: A Case-Control Study in Korea" Nutrients 8, no. 8: 469. https://doi.org/10.3390/nu8080469