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BMC Cancer
Published in: BMC Cancer 1/2012

Open Access 01-12-2012 | Research article

Interaction between interleukin-10 (IL-10) polymorphisms and dietary fibre in relation to risk of colorectal cancer in a Danish case-cohort study

Authors: Vibeke Andersen, Rikke Egeberg, Anne Tjønneland, Ulla Vogel

Published in: BMC Cancer | Issue 1/2012

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Abstract

Background

More than 50% of the colorectal cancer (CRC) etiology has been attributed to diet. Established or suspected dietary factors modifying risk of CRC are red meat, cereals, fish, and fibre. Diet and lifestyle may be linked to cancer through inflammation. Interleukin-10 (IL-10) is an anti-inflammatory cytokine. We wanted to test if dietary factors and IL10 polymorphisms interact in relation to colorectal carcinogenesis.

Methods

The functional IL10 polymorphism C-592A (rs1800872) and the marker rs3024505 were assessed in relation to diet and lifestyle in a nested case-cohort study of 378 CRC cases and 775 randomly selected participants from a prospective study of 57,053 persons. Genotyping data on the IL10 polymorphism C-592A, smoking and non-steroidal anti-inflammatory drugs (NSAID) was retrieved from Vogel et al. (Mutat Res, 2007; 624:88). Incidence rate ratios (IRR) and 95% Confidence Interval (95% CI) were calculated.

Results

No associations were found between the IL10 rs3024505 polymorphism and risk of CRC. There was interaction between rs3024505 and dietary fibre (P-value for interaction = 0.01). IL10 rs3024505 homozygous wildtype carriers were at 27% reduced risk of CRC per 10 g fibre per day (95% CI: 0.60-0.88) whereas variant carriers had no risk reduction by fibre intake. Also, interaction between IL10 C-592A and intake of fibre was found (P-value for interaction = 0.02). Among those eating <17.0 grams of fibre per day, carriers of an C-592A variant allele had a statistically significantly higher risk of colorectal cancer compared to homozygous wildtypes. No significant differences in colorectal cancer risk were observed between the reference group (CC and <17.0 g/day) and carriers of one C-592A variant allele eating 17.0 or more grams of dietary fibre per day. This suggests that the increased risk due to carrying the variant allele can be overcome by higher fibre intake. No interactions between IL10 polymorphisms and dietary meat, cereal, or fish intake, or between IL10 rs3024505 and smoking or NSAID use were found.

Conclusions

In this northern Caucasian cohort we found interaction between IL10 and dietary fibre in CRC carcinogenesis. High intake of fibre seems to protect against CRC among individuals with IL10 related genetic susceptibility to CRC. This finding should be evaluated in other prospective and population-based cohorts with different ethnic groups.
Literature
1.
Huxley RR, nsary-Moghaddam A, Clifton P, Czernichow S, Parr CL, Woodward M: The impact of dietary and lifestyle risk factors on risk of colorectal cancer: a quantitative overview of the epidemiological evidence. Int J Cancer. 2009, 125: 171-180. 10.1002/ijc.24343.CrossRefPubMed
2.
Karsa LV, Lignini TA, Patnick J, Lambert R, Sauvaget C: The dimensions of the CRC problem. Best Pract Res Clin Gastroenterol. 2010, 24: 381-396. 10.1016/j.bpg.2010.06.004.CrossRefPubMed
3.
Johnson IT: New approaches to the role of diet in the prevention of cancers of the alimentary tract. Mutat Res. 2004, 551: 9-28. 10.1016/j.mrfmmm.2004.02.017.CrossRefPubMed
4.
5.
Bingham SA, Day NE, Luben R, Ferrari P, Slimani N, Norat T, et al: Dietary fibre in food and protection against colorectal cancer in the European Prospective Investigation into Cancer and Nutrition (EPIC): an observational study. Lancet. 2003, 361: 1496-1501. 10.1016/S0140-6736(03)13174-1.CrossRefPubMed
6.
Santarelli RL, Pierre F, Corpet DE: Processed meat and colorectal cancer: a review of epidemiologic and experimental evidence. Nutr Cancer. 2008, 60: 131-144. 10.1080/01635580701684872.CrossRefPubMedPubMedCentral
7.
Khalil A, Villard PH, Dao MA, Burcelin R, Champion S, Fouchier F, et al: Polycyclic aromatic hydrocarbons potentiate high-fat diet effects on intestinal inflammation. Toxicol Lett. 2010, 196: 161-167. 10.1016/j.toxlet.2010.04.010.CrossRefPubMed
8.
Peluso M, Airoldi L, Munnia A, Colombi A, Veglia F, Autrup H, et al: Bulky DNA adducts, 4-aminobiphenyl-haemoglobin adducts and diet in the European Prospective Investigation into Cancer and Nutrition (EPIC) prospective study. Br J Nutr. 2008, 100: 489-495. 10.1017/S0007114508911600.CrossRefPubMed
9.
Hansen L, Skeie G, Landberg R, Lund E, Palmqvist R, Johansson I, et al: Intake of dietary fiber, especially from cereal foods, is associated with lower incidence of colon cancer in the HELGA cohort. Int J Cancer. 2011, 10:
10.
Gonzalez CA, Riboli E: Diet and cancer prevention: where we are, where we are going. Nutr Cancer. 2006, 56: 225-231. 10.1207/s15327914nc5602_14.CrossRefPubMed
11.
Gonzalez CA: The European Prospective Investigation into Cancer and Nutrition (EPIC). Public Health Nutr. 2006, 9: 124-126.CrossRefPubMed
12.
Joensen AM, Schmidt EB, Dethlefsen C, Johnsen SP, Tjonneland A, Rasmussen LH, et al: Dietary intake of total marine n-3 polyunsaturated fatty acids, eicosapentaenoic acid, docosahexaenoic acid and docosapentaenoic acid and the risk of acute coronary syndrome - a cohort study. Br J Nutr. 2010, 103: 602-607. 10.1017/S0007114509992170.CrossRefPubMed
13.
Liang PS, Chen TY, Giovannucci E: Cigarette smoking and colorectal cancer incidence and mortality: systematic review and meta-analysis. Int J Cancer. 2009, 124: 2406-2415. 10.1002/ijc.24191.CrossRefPubMed
14.
Tsoi KK, Pau CY, Wu WK, Chan FK, Griffiths S, Sung JJ: Cigarette smoking and the risk of colorectal cancer: a meta-analysis of prospective cohort studies. Clin Gastroenterol Hepatol. 2009, 7: 682-688. 10.1016/j.cgh.2009.02.016.CrossRefPubMed
15.
Hermann M, Krum H, Ruschitzka F: To the heart of the matter: coxibs, smoking, and cardiovascular risk. Circulation. 2005, 112: 941-945. 10.1161/CIRCULATIONAHA.105.567842.CrossRefPubMed
16.
Friis S, Poulsen AH, Sorensen HT, Tjonneland A, Overvad K, Vogel U, et al: Aspirin and other non-steroidal anti-inflammatory drugs and risk of colorectal cancer: a Danish cohort study. Cancer Causes Control. 2009, 20: 731-740. 10.1007/s10552-008-9286-7.CrossRefPubMed
17.
Flossmann E, Rothwell PM: Effect of aspirin on long-term risk of colorectal cancer: consistent evidence from randomised and observational studies. Lancet. 2007, 369: 1603-1613. 10.1016/S0140-6736(07)60747-8.CrossRefPubMed
18.
Ouyang W, Rutz S, Crellin NK, Valdez PA, Hymowitz SG: Regulation and functions of the IL-10 family of cytokines in inflammation and disease. Annu Rev Immunol. 2011, 29: 71-109. 10.1146/annurev-immunol-031210-101312. 71–109CrossRefPubMed
19.
Sabat R, Grutz G, Warszawska K, Kirsch S, Witte E, Wolk K, et al: Biology of interleukin-10. Cytokine Growth Factor Rev. 2010, 21: 331-344. 10.1016/j.cytogfr.2010.09.002.CrossRefPubMed
20.
Battaglia M, Gianfrani C, Gregori S, Roncarolo MG: IL-10-producing T regulatory type 1 cells and oral tolerance. Ann N Y Acad Sci. 2004, 1029: 142-53. 10.1196/annals.1309.031.CrossRefPubMed
21.
Erdman SE, Rao VP, Poutahidis T, Ihrig MM, Ge Z, Feng Y, et al: CD4(+)CD25(+) regulatory lymphocytes require interleukin 10 to interrupt colon carcinogenesis in mice. Cancer Res. 2003, 63: 6042-6050.PubMed
22.
Westbrook AM, Szakmary A, Schiestl RH: Mechanisms of intestinal inflammation and development of associated cancers: lessons learned from mouse models. Mutat Res. 2010, 705: 40-59. 10.1016/j.mrrev.2010.03.001.CrossRefPubMedPubMedCentral
23.
Shkoda A, Ruiz PA, Daniel H, Kim SC, Rogler G, Sartor RB, et al: Interleukin-10 blocked endoplasmic reticulum stress in intestinal epithelial cells: impact on chronic inflammation. Gastroenterology. 2007, 132: 190-207. 10.1053/j.gastro.2006.10.030.CrossRefPubMed
24.
Al-Ashy R, Chakroun I, El-Sabban ME, Homaidan FR: The role of NF-kappaB in mediating the anti-inflammatory effects of IL-10 in intestinal epithelial cells. Cytokine. 2006, 36: 1-8. 10.1016/j.cyto.2006.10.003.CrossRefPubMed
25.
Duell BL, Tan CK, Carey AJ, Wu F, Cripps AW, Ulett GC: Recent insights into microbial triggers of interleukin-10 production in the host and the impact on infectious disease pathogenesis. FEMS Immunol Med Microbiol. 2012, 10: 695X-
26.
Mazmanian SK, Round JL, Kasper DL: A microbial symbiosis factor prevents intestinal inflammatory disease. Nature. 2008, 453: 620-625. 10.1038/nature07008.CrossRefPubMed
27.
28.
Zhu Y, Michelle LT, Jobin C, Young HA: Gut microbiota and probiotics in colon tumorigenesis. Cancer Lett. 2011, 309: 119-127. 10.1016/j.canlet.2011.06.004.CrossRefPubMedPubMedCentral
29.
30.
Andersen V, Christensen J, Overvad K, Tjonneland A, Vogel U: Heme oxygenase-1 (HO-1) polymorphism is not associated with risk of colorectal cancer; a Danish prospective study. Eur J Gastroenterol Hepatol. 2011, 23: 282-5. 10.1097/MEG.0b013e3283417f76.CrossRefPubMed
31.
Andersen V, Christensen J, Overvad K, Tjonneland A, Vogel U: Polymorphisms in NFkB, PXR, LXR and risk of colorectal cancer in a prospective study of Danes. BMC Cancer. 2010, 10: 484-10.1186/1471-2407-10-484.CrossRefPubMedPubMedCentral
32.
Andersen V, Ostergaard M, Christensen J, Overvad K, Tjonneland A, Vogel U: Polymorphisms in the xenobiotic transporter Multidrug Resistance 1 (MDR1) gene and interaction with meat intake in relation to risk of colorectal cancer in a Danish prospective case-cohort study. BMC Cancer. 2009, 9: 407-10.1186/1471-2407-9-407.CrossRefPubMedPubMedCentral
33.
Turner DM, Williams DM, Sankaran D, Lazarus M, Sinnott PJ, Hutchinson IV: An investigation of polymorphism in the interleukin-10 gene promoter. Eur J Immunogenet. 1997, 24: 1-8. 10.1111/j.1365-2370.1997.tb00001.x.CrossRefPubMed
34.
Yilmaz V, Yentur SP, Saruhan-Direskeneli G: IL-12 and IL-10 polymorphisms and their effects on cytokine production. Cytokine. 2005, 30: 188-194. 10.1016/j.cyto.2005.01.006.CrossRefPubMed
35.
Crawley E, Kay R, Sillibourne J, Patel P, Hutchinson I, Woo P: Polymorphic haplotypes of the interleukin-10 5' flanking region determine variable interleukin-10 transcription and are associated with particular phenotypes of juvenile rheumatoid arthritis. Arthritis Rheum. 1999, 42: 1101-1108. 10.1002/1529-0131(199906)42:6<1101::AID-ANR6>3.0.CO;2-Y.CrossRefPubMed
36.
Shin HD, Winkler C, Stephens JC, Bream J, Young H, Goedert JJ, et al: Genetic restriction of HIV-1 pathogenesis to AIDS by promoter alleles of IL10. Proc Natl Acad Sci USA. 2000, 19 (97): 14467-14472.CrossRef
37.
Cacev T, Radosevic S, Krizanac S, Kapitanovic S: Influence of interleukin-8 and interleukin-10 on sporadic colon cancer development and progression. Carcinogenesis. 2008, 29: 1572-1580. 10.1093/carcin/bgn164.CrossRefPubMed
38.
Vogel U, Christensen J, Dybdahl M, Friis S, Hansen RD, Wallin H, et al: Prospective study of interaction between alcohol, NSAID use and polymorphisms in genes involved in the inflammatory response in relation to risk of colorectal cancer. Mutat Res. 2007, 624: 88-100. 10.1016/j.mrfmmm.2007.04.006.CrossRefPubMed
39.
Tsilidis KK, Helzlsouer KJ, Smith MW, Grinberg V, Hoffman-Bolton J, Clipp SL, et al: Association of common polymorphisms in IL10, and in other genes related to inflammatory response and obesity with colorectal cancer. Cancer Causes Control. 2009, 20: 1739-1751. 10.1007/s10552-009-9427-7.CrossRefPubMedPubMedCentral
40.
Wilkening S, Tavelin B, Canzian F, Enquist K, Palmqvist R, Altieri A, et al: Interleukin promoter polymorphisms and prognosis in colorectal cancer. Carcinogenesis. 2008, 29: 1202-1206. 10.1093/carcin/bgn101.CrossRefPubMed
41.
Franke A, Balschun T, Karlsen TH, Sventoraityte J, Nikolaus S, Mayr G, et al: Sequence variants in IL10, ARPC2 and multiple other loci contribute to ulcerative colitis susceptibility. Nat Genet. 2008, 40: 1319-1323. 10.1038/ng.221.CrossRefPubMed
42.
Andersen V, Ernst A, Christensen J, Ostergaard M, Jacobsen BA, Tjonneland A, et al: The polymorphism rs3024505 proximal to IL-10 is associated with risk of ulcerative colitis and Crohns disease in a Danish case–control study. BMC Med Genet. 2010, 11: 82-CrossRefPubMedPubMedCentral
43.
Tjonneland A, Olsen A, Boll K, Stripp C, Christensen J, Engholm G, et al: Study design, exposure variables, and socioeconomic determinants of participation in Diet, Cancer and Health: a population-based prospective cohort study of 57,053 men and women in Denmark. Scand J Public Health. 2007, 35: 432-441. 10.1080/14034940601047986.CrossRefPubMed
44.
45.
Slimani N, Deharveng G, Unwin I, Southgate DA, Vignat J, Skeie G, et al: The EPIC nutrient database project (ENDB): a first attempt to standardize nutrient databases across the 10 European countries participating in the EPIC study. Eur J Clin Nutr. 2007, 61: 1037-1056. 10.1038/sj.ejcn.1602679.CrossRefPubMed
46.
Prosky L, Asp NG, Furda I, DeVries JW, Schweizer TF, Harland BF: Determination of total dietary fiber in foods and food products: collaborative study. J Assoc Off Anal Chem. 1985, 68: 677-679.PubMed
47.
Slimani N, Kaaks R, Ferrari P, Casagrande C, Clavel-Chapelon F, Lotze G, et al: European Prospective Investigation into Cancer and Nutrition (EPIC) calibration study: rationale, design and population characteristics. Public Health Nutr. 2002, 5: 1125-1145. 10.1079/PHN2002395.CrossRefPubMed
48.
Tjonneland A, Overvad K, Haraldsdottir J, Bang S, Ewertz M, Jensen OM: Validation of a semiquantitative food frequency questionnaire developed in Denmark. Int J Epidemiol. 1991, 20: 906-912. 10.1093/ije/20.4.906.CrossRefPubMed
49.
Tjonneland A, Haraldsdottir J, Overvad K, Stripp C, Ewertz M, Jensen OM: Influence of individually estimated portion size data on the validity of a semiquantitative food frequency questionnaire. Int J Epidemiol. 1992, 21: 770-777. 10.1093/ije/21.4.770.CrossRefPubMed
50.
Miller SA, Dykes DD, Polesky HF: A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res. 1988, 16: 1215-10.1093/nar/16.3.1215.CrossRefPubMedPubMedCentral
51.
Macarthur M, Sharp L, Hold GL, Little J, El-Omar EM: The role of cytokine gene polymorphisms in colorectal cancer and their interaction with aspirin use in the northeast of Scotland. Cancer Epidemiol Biomarkers Prev. 2005, 14: 1613-1618. 10.1158/1055-9965.EPI-04-0878.CrossRefPubMed
52.
Barlow WE, Ichikawa L, Rosner D, Izumi S: Analysis of case-cohort designs. J Clin Epidemiol. 1999, 52: 1165-1172. 10.1016/S0895-4356(99)00102-X.CrossRefPubMed
53.
Barlow WE: Robust variance estimation for the case-cohort design. Biometrics. 1994, 50: 1064-1072. 10.2307/2533444.CrossRefPubMed
54.
Walker AW, Ince J, Duncan SH, Webster LM, Holtrop G, Ze X, et al: Dominant and diet-responsive groups of bacteria within the human colonic microbiota. ISME J. 2011, 5: 220-230. 10.1038/ismej.2010.118.CrossRefPubMed
55.
Lee YK, Mazmanian SK: Has the microbiota played a critical role in the evolution of the adaptive immune system?. Science. 2010, 330: 1768-1773. 10.1126/science.1195568.CrossRefPubMedPubMedCentral
56.
Mazmanian SK, Liu CH, Tzianabos AO, Kasper DL: An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell. 2005, 122: 107-118. 10.1016/j.cell.2005.05.007.CrossRefPubMed
57.
Gaboriau-Routhiau V, Rakotobe S, Lecuyer E, Mulder I, Lan A, Bridonneau C, et al: The key role of segmented filamentous bacteria in the coordinated maturation of gut helper T cell responses. Immunity. 2009, 31: 677-689. 10.1016/j.immuni.2009.08.020.CrossRefPubMed
58.
Ivanov II, Atarashi K, Manel N, Brodie EL, Shima T, Karaoz U, et al: Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell. 2009, 139: 485-498. 10.1016/j.cell.2009.09.033.CrossRefPubMedPubMedCentral
59.
Kohl A, Gogebakan O, Mohlig M, Osterhoff M, Isken F, Pfeiffer AF, et al: Increased interleukin-10 but unchanged insulin sensitivity after 4 weeks of (1, 3)(1, 6)-beta-glycan consumption in overweight humans. Nutr Res. 2009, 29: 248-254.CrossRefPubMed
60.
Kim J, Cho YA, Choi IJ, Lee YS, Kim SY, Shin A, et al: Effects of interleukin-10 polymorphisms, Helicobacter pylori infection, and smoking on the risk of noncardia gastric cancer. PLoS One. 2012, 7: e29643-10.1371/journal.pone.0029643.CrossRefPubMedPubMedCentral
61.
Wang J, Ding Q, Shi Y, Cao Q, Qin C, Zhu J, et al: The interleukin-10-1082 promoter polymorphism and cancer risk: a meta-analysis. Mutagenesis. 2012, 27: 305-12. 10.1093/mutage/ger078.CrossRefPubMed
62.
He JR, Chen LJ, Su Y, Cen YL, Tang LY, Yu DD, et al: Joint effects of Epstein-Barr virus and polymorphisms in interleukin-10 and interferon-gamma on breast cancer risk. J Infect Dis. 2012, 205: 64-71. 10.1093/infdis/jir710.CrossRefPubMed
63.
Pan F, Tian J, Pan YY, Zhang Y: Association of IL-10-1082 promoter polymorphism with susceptibility to gastric cancer: evidence from 22 case–control studies. Mol Biol Rep. 2012
64.
Ni P, Xu H, Xue H, Lin B, Lu Y: A Meta-Analysis of Interleukin-10-1082 Promoter Polymorphism Associated with Gastric Cancer Risk. DNA Cell Biol. 2012, 31: 582-91. 10.1089/dna.2011.1440.CrossRefPubMedPubMedCentral
65.
Vogel U, Christensen J, Wallin H, Friis S, Nexo BA, Raaschou-Nielsen O, et al: Polymorphisms in genes involved in the inflammatory response and interaction with NSAID use or smoking in relation to lung cancer risk in a prospective study. Mutat Res. 2008, 639: 89-100. 10.1016/j.mrfmmm.2007.11.004.CrossRefPubMed
66.
Hart K, Landvik NE, Lind H, Skaug V, Haugen A, Zienolddiny S: A combination of functional polymorphisms in the CASP8, MMP1, IL10 and SEPS1 genes affects risk of non-small cell lung cancer. Lung Cancer. 2011, 71: 123-129. 10.1016/j.lungcan.2010.04.016.CrossRefPubMed
67.
Ogino S, Chan AT, Fuchs CS, Giovannucci E: Molecular pathological epidemiology of colorectal neoplasia: an emerging transdisciplinary and interdisciplinary field. Gut. 2011, 60: 397-411. 10.1136/gut.2010.217182.CrossRefPubMed
68.
Daley D: The identification of colon cancer susceptibility genes by using genome-wide scans. Methods Mol Biol. 2010, 653: 3-21. 10.1007/978-1-60761-759-4_1. 3–21CrossRefPubMed
69.
Metadata
Title
Interaction between interleukin-10 (IL-10) polymorphisms and dietary fibre in relation to risk of colorectal cancer in a Danish case-cohort study
Authors
Vibeke Andersen
Rikke Egeberg
Anne Tjønneland
Ulla Vogel
Publication date
01-12-2012
Publisher
BioMed Central
Published in
BMC Cancer / Issue 1/2012
Electronic ISSN: 1471-2407
DOI
https://doi.org/10.1186/1471-2407-12-183

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