Abstract
Despite compelling basic science evidence, the search for causal associations linking specific pro- and anti-oxidants to presumably oxidative stress-related neoplasms, such as colorectal adenoma, has produced inconsistent results. We developed an oxidative balance score (OBS) to characterize the pro-oxidant and anti-oxidant exposures of 2,305 participants in a case–control study of colorectal adenoma that used both endoscopy-confirmed and community controls. Twelve lifestyle medical and dietary factors with known pro- or anti-oxidant properties were considered. Each high anti-oxidant exposure and low pro-oxidant exposure was awarded one or two points depending on the level of exposure, and the points for each OBS component were summed. We observed a significant inverse association between OBS (continuous variable) and colorectal adenoma in the analyses with either community, or endoscopy controls (each p-trend < 0.01). When the OBS was treated as an ordinal variable and a score of ≤3 points was used as the referent category, in the analyses with the endoscopy controls the adjusted odds ratios for scores of 4–6, 7–9, 10–12, 13–15, and 16+, were 0.42, 0.32, 0.22, 0.20, and 0.19, respectively, with all 95% confidence intervals excluding 1.0. The corresponding analysis for community controls showed a similar trend. Our findings are in line with the basic science evidence supporting the role of oxidative stress in colorectal neoplasia.
Similar content being viewed by others
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.References
Kovacic P, Jacintho J (2001) Mechanisms of carcinogenesis: focus on oxidative stress and electron transfer. Curr Med Chem 8(7):773–796
Loft S, Poulsen H (1996) Cancer risk and oxidative DNA damage in man. J Mol Med 74(6):297–312. doi:10.1007/BF00207507
Poulsen H, Prieme H, Loft S (1998) Role of oxidative DNA damage in cancer initiation and promotion. Eur J Cancer Prev 7(1):9–16
Ames B (1989) Mutagenesis and carcinogenesis: endogenous and exogenous factors. Environ Mol Mutagen 14(Suppl 16):66–77. doi:10.1002/em.2850140614
Cross C, Halliwell B, Borish E et al (1987) Oxygen radicals and human disease. Ann Intern Med 107(4):526–545
Frenkel K (1992) Carcinogen-mediated oxidant formation and oxidative DNA damage. Pharmacol Ther 53(1):127–166. doi:10.1016/0163-7258(92)90047-4
Valko M, Izakovic M, Mazur M, Rhodes C, Telser J (2004) Role of oxygen radicals in DNA damage and cancer incidence. Mol Cell Biochem 266(1–2):37–56. doi:10.1023/B:MCBI.0000049134.69131.89
Bruce W, Giacca A, Medline A (2000) Possible mechanisms relating diet and risk of colon cancer. Cancer Epidemiol Biomarkers Prev 9(12):1271–1279
van der Vaart H, Postma D, Timens W, ten Hacken N (2004) Acute effects of cigarette smoke on inflammation and oxidative stress: a review. Thorax 59(8):713–721. doi:10.1136/thx.2003.012468
MacNee W (2000) Oxidants/antioxidants and COPD. Chest 117(5 Suppl 1):303S–317S. doi:10.1378/chest.117.5_suppl_1.303S-a
Velthuis-te Wierik E, van den Berg H, Weststrate J, van het Hof K, de Graaf C (1996) Consumption of reduced-fat products: effects on parameters of anti-oxidative capacity. Eur J Clin Nutr 50:214–219
Galli C, Marangoni F (1997) Recent advances in the biology of n-6 fatty acids. Nutrition 13(11–12):978–985. doi:10.1016/S0899-9007(97)00341-9
Swain J, Alekel D, Dent S, Peterson C, Reddy M (2002) Iron indexes and total antioxidant status in response to soy protein intake in perimenopausal women. Am J Clin Nutr 76(1):165–171
Heber D, Lu Q (2002) Overview of mechanisms of action of lycopene. Exp Biol Med (Maywood) 227(10):920–923
Pohar K, Gong M, Bahnson R, Miller E, Clinton S (2003) Tomatoes, lycopene and prostate cancer: a clinician’s guide for counseling those at risk for prostate cancer. World J Urol 21(1):9–14
DeMichele A, Martin A, Mick R et al (2003) Interleukin-6-174G→C polymorphism is associated with improved outcome in high-risk breast cancer. Cancer Res 63(22):8051–8056
Lipkin M (1987) Biomarkers of increased susceptibility to gastrointestinal cancer. Their development and application to studies of cancer prevention. Gastroenterology 92(4):1083–1086
Rozen P (1992) An evaluation of rectal epithelial proliferation measurement as biomarker of risk for colorectal neoplasia and response in intervention studies. Eur J Cancer Prev 1(3):215–224. doi:10.1097/00008469-199204000-00002
Lok E, Ratnayake W, Scott F et al (1992) Effect of varying the type of fat in a semi-purified AIN-76A diet on cellular proliferation in the mammary gland and intestinal crypts in female Swiss Webster mice. Carcinogenesis 13(10):1735–1741. doi:10.1093/carcin/13.10.1735
Nayini J, Sugie S, el-Bayoumy K et al (1991) Effect of dietary benzylselenocyanate on azoxymethane-induced colon carcinogenesis in male F344 rats. Nutr Cancer 15(2):129–139
Paganelli G, Biasco G, Brandi G et al (1992) Effect of vitamin A, C, and E supplementation on rectal cell proliferation in patients with colorectal adenomas. J Natl Cancer Inst 84(1):47–51. doi:10.1093/jnci/84.1.47
Cahill R, O’Sullivan K, Mathias P, Beattie S, Hamilton H, O’Morain C (1993) Effects of vitamin antioxidant supplementation on cell kinetics of patients with adenomatous polyps. Gut 34(7):963–967. doi:10.1136/gut.34.7.963
World Cancer Research Fund, American Institute for Cancer Research (2007) Food, nutrition and the prevention of cancer: a global perspective. AICR, Washington
Wu K, Willett W, Chan J et al (2002) A prospective study on supplemental vitamin e intake and risk of colon cancer in women and men. Cancer Epidemiol Biomarkers Prev 11(11):1298–1304
Terry P, Jain M, Miller A, Howe G, Rohan T (2002) Dietary carotenoid intake and colorectal cancer risk. Nutr Cancer 42(2):167–172. doi:10.1207/S15327914NC422_3
Slattery ML, Boucher KM, Caan BJ, Potter JD, Ma KN (1998) Eating patterns and risk of colon cancer. Am J Epidemiol 148(1):4–16
Trichopoulou A, Kouris-Blazos A, Wahlqvist M et al (1995) Diet and overall survival in elderly people. BMJ 311(7018):1457–1456
Huijbregts P, Feskens E, Rasanen L et al (1997) Dietary pattern and 20 year mortality in elderly men in Finland, Italy, and The Netherlands: longitudinal cohort study. Bmj 315(7099):13–17
Goodman M, Bostick RM, Dash C, Flanders WD, Mandel JS (2007) Hypothesis: oxidative stress score as a combined measure of pro-oxidant and antioxidant exposures. Ann Epidemiol 17(5):394–399. doi:10.1016/j.annepidem.2007.01.034
Van Hoydonck PG, Temme EH, Schouten EG (2002) A dietary oxidative balance score of vitamin C, beta-carotene and iron intakes and mortality risk in male smoking Belgians. J Nutr 132(4):756–761
Smith-Warner S, Elmer P, Fosdick L et al (2002) Fruits, vegetables, and adenomatous polyps: the Minnesota Cancer Prevention Unit case–control study. Am J Epidemiol 155:1104–1113. doi:10.1093/aje/155.12.1104
O’Brien MJ, Winawer SJ, Zauber AG et al (1990) The national polyp study. Patient and polyp characteristics associated with high-grade dysplasia in colorectal adenomas. Gastroenterology 98(2):371–379
Willett W, Sampson L, Stampfer M et al (1985) Reproducibility and validity of a semiquantitative food frequency questionnaire. Am J Epidemiol 122(1):51–65
Willett W, Sampson L, Browne M et al (1988) The use of a self-administered questionnaire to assess diet four years in the past. Am J Epidemiol 127(1):188–199
Ascherio A, Stampfer MJ, Colditz GA, Rimm EB, Litin L, Willett WC (1992) Correlations of vitamin A and E intakes with the plasma concentrations of carotenoids and tocopherols among American men and women. J Nutr 122(9):1792–1801
Willett WC, Stampfer MJ, Underwood BA, Speizer FE, Rosner B, Hennekens CH (1983) Validation of a dietary questionnaire with plasma carotenoid and alpha-tocopherol levels. Am J Clin Nutr 38(4):631–639
Ascherio A, Rimm EB, Stampfer MJ, Giovannucci EL, Willett WC (1995) Dietary intake of marine n-3 fatty acids, fish intake, and the risk of coronary disease among men. N Engl J Med 332(15):977–982. doi:10.1056/NEJM199504133321501
Holmes MD, Powell IJ, Campos H, Stampfer MJ, Giovannucci EL, Willett WC (2007) Validation of a food frequency questionnaire measurement of selected nutrients using biological markers in African-American men. Eur J Clin Nutr 61(11):1328–1336. doi:10.1038/sj.ejcn.1602641
Lieberman DA, Prindiville S, Weiss DG, Willett W (2003) Risk factors for advanced colonic neoplasia and hyperplastic polyps in asymptomatic individuals. Jama 290(22):2959–2967. doi:10.1001/jama.290.22.2959
Dube C, Rostom A, Lewin G et al (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(5):365–375
Rostom A, Dube C, Lewin G et al (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(5):376–389
Dodig S, Cepelak I (2004) The facts and controversies about selenium. Acta Pharm 54(4):261–276
Goldbohm R, van ‘t Veer P, van den Brandt P et al (1995) Reproducibility of a food frequency questionnaire and stability of dietary habits determined from five annually repeated measurements. Eur J Clin Nutr 49(6):420–429
Estruch R, Sacanella E, Badia E et al (2004) Different effects of red wine and gin consumption on inflammatory biomarkers of atherosclerosis: a prospective randomized crossover trial. Effects of wine on inflammatory markers. Atherosclerosis 175(1):117–123. doi:10.1016/j.atherosclerosis.2004.03.006
Imhof A, Woodward M, Doering A et al (2004) Overall alcohol intake, beer, wine, and systemic markers of inflammation in western Europe: results from three MONICA samples (Augsburg, Glasgow, Lille). Eur Heart J 25(23):2092–2100. doi:10.1016/j.ehj.2004.09.032
Kloner RA, Rezkalla SH (2007) To drink or not to drink? That is the question. Circulation 116(11):1306–1317. doi:10.1161/CIRCULATIONAHA.106.678375
Maraldi C, Volpato S, Kritchevsky SB et al (2006) Impact of inflammation on the relationship among alcohol consumption, mortality, and cardiac events: the health, aging, and body composition study. Arch Intern Med 166(14):1490–1497. doi:10.1001/archinte.166.14.1490
Willett W, Stampfer M (1986) Total energy intake: implications for epidemiologic analyses. Am J Epidemiol 124(1):17–27
Mayne ST, Wright ME, Albanes D (2007) Re: Hypothesis: oxidative stress score as a combined measure of pro-oxidant and antioxidant exposures. Ann Epidemiol 17(11):930; author reply 931. doi:10.1016/j.annepidem.2007.06.012
Kleinbaum D, Klein M (2002) Logistic regression: a self-learning text. Springer-Verlag, New York
Boyle P, Leon M (2002) Epidemiology of colorectal cancer. Br Med Bull 64:1–25. doi:10.1093/bmb/64.1.1
Gaard M, Tretli S, Loken E (1996) Dietary factors and risk of colon cancer: a prospective study of 50,535 young Norwegian men and women. Eur J Cancer Prev 5(6):445–454
Bostick R, Potter J, Kushi L et al (1994) Sugar, meat, and fat intake, and non-dietary risk factors for colon cancer incidence in Iowa women (United States). Cancer Causes Control 5(1):38–52. doi:10.1007/BF01830725
Giovannucci E, Rimm E, Stampfer M, Colditz G, Ascherio A, Willett W (1994) Intake of fat, meat, and fiber in relation to risk of colon cancer in men. Cancer Res 54(9):2390–2397
Goldbohm R, van den Brandt P, van ‘t Veer P et al (1994) A prospective cohort study on the relation between meat consumption and the risk of colon cancer. Cancer Res 54(3):718–723
Hsing A, McLaughlin J, Chow W et al (1998) Risk factors for colorectal cancer in a prospective study among U.S. white men. Int J Cancer 77(4):549–553. doi:10.1002/(SICI)1097-0215(19980812)77:4<549::AID-IJC13>3.0.CO;2-1
Knekt P, Steineck G, Jarvinen R, Hakulinen T, Aromaa A (1994) Intake of fried meat and risk of cancer: a follow-up study in Finland. Int J Cancer 59(6):756–760. doi:10.1002/ijc.2910590608
Thun M, Calle E, Namboodiri M et al (1992) Risk factors for fatal colon cancer in a large prospective study. J Natl Cancer Inst 84(19):1491–1500. doi:10.1093/jnci/84.19.1491
Phillips R, Snowdon D (1985) Dietary relationships with fatal colorectal cancer among Seventh-Day Adventists. J Natl Cancer Inst 74(2):307–317
Sellers T, Bazyk A, Bostick R et al (1998) 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 9(4):357–367. doi:10.1023/A:1008886715597
Longnecker M, Martin-Moreno J, Knekt P et al (1992) Serum alpha-tocopherol concentration in relation to subsequent colorectal cancer: pooled data from five cohorts. J Natl Cancer Inst 84(6):430–435. doi:10.1093/jnci/84.6.430
Bostick R, Potter J, McKenzie D et al (1993) Reduced risk of colon cancer with high intake of vitamin E: the Iowa Women’s Health Study. Cancer Res 53(18):4230–4237
Hofstad B, Almendingen K, Vatn M et al (1998) Growth and recurrence of colorectal polyps: a double-blind 3-year intervention with calcium and antioxidants. Digestion 59(2):148–156. doi:10.1159/000007480
Greenberg E, Baron J, Tosteson T et al (1994) A clinical trial of antioxidant vitamins to prevent colorectal adenoma. Polyp Prevention Study Group. N Engl J Med 331(3):141–147. doi:10.1056/NEJM199407213310301
Coulter I, Hardy M, Morton S et al (2006) Antioxidants vitamin C and vitamin e for the prevention and treatment of cancer. J Gen Intern Med 21(7):735–744. doi:10.1111/j.1525-1497.2006.00483.x
Goodman G, Thornquist M, Balmes J et al (2004) The Beta-Carotene and Retinol Efficacy Trial: incidence of lung cancer and cardiovascular disease mortality during 6-year follow-up after stopping beta-carotene and retinol supplements. J Natl Cancer Inst 96(23):1743–1750
Wright M, Mayne S, Stolzenberg-Solomon R et al (2004) Development of a comprehensive dietary antioxidant index and application to lung cancer risk in a cohort of male smokers. Am J Epidemiol 160(1):68–76. doi:10.1093/aje/kwh173
Terry P, Lagergren J, Ye W, Nyren O, Wolk A (2000) Antioxidants and cancers of the esophagus and gastric cardia. Int J Cancer 87(5):750–754. doi:10.1002/1097-0215(20000901)87:5<750::AID-IJC19>3.0.CO;2-6
Potosky AL, Reeve BB, Clegg LX et al (2002) Quality of life following localized prostate cancer treated initially with androgen deprivation therapy or no therapy. J Natl Cancer Inst 94(6):430–437
Thorngren-Jerneck K, Herbst A (2001) Low 5-minute Apgar score: a population-based register study of 1 million term births. Obstet Gynecol 98(1):65–70. doi:10.1016/S0029-7844(01)01370-9
Fung T, Hu FB, Fuchs C et al (2003) Major dietary patterns and the risk of colorectal cancer in women. Arch Intern Med 163(3):309–314. doi:10.1001/archinte.163.3.309
Kesse E, Clavel-Chapelon F, Boutron-Ruault MC (2006) Dietary patterns and risk of colorectal tumors: a cohort of French women of the National Education System (E3N). Am J Epidemiol 164(11):1085–1093. doi:10.1093/aje/kwj324
Kim MK, Sasaki S, Otani T, Tsugane S (2005) Dietary patterns and subsequent colorectal cancer risk by subsite: a prospective cohort study. Int J Cancer 115(5):790–798. doi:10.1002/ijc.20943
Rouillier P, Senesse P, Cottet V, Valleau A, Faivre J, Boutron-Ruault MC (2005) Dietary patterns and the adenomacarcinoma sequence of colorectal cancer. Eur J Nutr 44(5):311–318. doi:10.1007/s00394-004-0525-8
Terry P, Hu FB, Hansen H, Wolk A (2001) Prospective study of major dietary patterns and colorectal cancer risk in women. Am J Epidemiol 154(12):1143–1149. doi:10.1093/aje/154.12.1143
Gleason D (1996) Undergrading of prostate cancer biopsies: a paradox inherent in all biologic bivariate distributions. Urology 47(3):289–291. doi:10.1016/S0090-4295(99)80441-5
O’Donnell C, Kamlin C, Davis P, Carlin J, Morley C (2006) Interobserver variability of the 5-minute Apgar score. J Pediatr 149(4):486–489. doi:10.1016/j.jpeds.2006.05.040
Vanier M, Mazaux J, Lambert J, Dassa C, Levin H (2000) Assessment of neuropsychologic impairments after head injury: interrater reliability and factorial and criterion validity of the Neurobehavioral Rating Scale-Revised. Arch Phys Med Rehabil 81(6):796–806
Gordis L (2000) Epidemiology. WB Saunders Company, Philadelphia
Rosario A, Wellmann J, Heid I, Wichmann H (2006) Radon epidemiology: continuous and categorical trend estimators when the exposure distribution is skewed and outliers may be present. J Toxicol Environ Health A 69(7):681–700. doi:10.1080/15287390500261190
Conti DV, Cortessis V, Molitor J, Thomas DC (2003) Bayesian modeling of complex metabolic pathways. Hum Hered 56(1–3):83–93. doi:10.1159/000073736
Blazer D, Umbach D, Bostick R, Taylor J (2000) Vitamin D receptor polymorphisms and prostate cancer. Mol Carcinog 27(1):18–23. doi:10.1002/(SICI)1098-2744(200001)27:1<18::AID-MC4>3.0.CO;2-O
Boyapati S, Bostick R, McGlynn K et al (2004) Folate intake, MTHFR C677T polymorphism, alcohol consumption and risk for sporadic colorectal adenoma. Cancer Cause Control 15:493–501. doi:10.1023/B:CACO.0000036447.45446.2c
Hauret K, Bostick R, Matthews C et al (2004) Energy balance and risk for incident sporadic colorectal adenomas. Am J Epidemiol 159:983–992. doi:10.1093/aje/kwh130
van Gils C, Bostick R, Stern M, Taylor J (2002) Differences in base excision repair capacity may modulate the effect of dietary antioxidant intake on prostate cancer risk: an example of polymorphisms in the XRCC1 gene. Cancer Epidemiol Biomarkers Prev 11(11):1279–1284
Wolf LA, Terry PD, Potter JD, Bostick RM (2007) Do factors related to endogenous and exogenous estrogens modify the relationship between obesity and risk of colorectal adenomas in women? Cancer Epidemiol Biomarkers Prev. 16(4):676–683. doi:10.1158/1055-9965.EPI-06-0883
Hernan MA, Hernandez-Diaz S, Robins JM (2004) A structural approach to selection bias. Epidemiology 15(5):615–625. doi:10.1097/01.ede.0000135174.63482.43
Lear J, Smith A, Strange R, Fryer A (2000) Detoxifying enzyme genotypes and susceptibility to cutaneous malignancy. Br J Dermatol 142(1):8–15. doi:10.1046/j.1365-2133.2000.03339.x
Boiteux S, Radicella J (2000) The human OGG1 gene: structure, functions, and its implication in the process of carcinogenesis. Arch Biochem Biophys 377(1):1–8. doi:10.1006/abbi.2000.1773
Valko M, Rhodes C, Moncol J, Izakovic M, Mazur M (2006) Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem Biol Interact 160(1):1–40. doi:10.1016/j.cbi.2005.12.009
Young A, Lowe G (2001) Antioxidant and prooxidant properties of carotenoids. Arch Biochem Biophys 385(1):20–27. doi:10.1006/abbi.2000.2149
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Goodman, M., Bostick, R.M., Dash, C. et al. A summary measure of pro- and anti-oxidant exposures and risk of incident, sporadic, colorectal adenomas. Cancer Causes Control 19, 1051–1064 (2008). https://doi.org/10.1007/s10552-008-9169-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10552-008-9169-y