Red and processed meat intake and risk of colorectal adenomas: a systematic review and meta-analysis of epidemiological studies (original) (raw)

• Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM (2010) Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 127:2893–2917
  Article PubMed CAS Google Scholar
• Leslie A, Carey FA, Pratt NR, Steele RJ (2002) The colorectal adenoma-carcinoma sequence. Br J Surg 89:845–860
  Article PubMed CAS Google Scholar
• Atkin WS, Morson BC, Cuzick J (1992) Long-term risk of colorectal cancer after excision of rectosigmoid adenomas. N Engl J Med 326:658–662
  Article PubMed CAS Google Scholar
• Atkin WS, Edwards R, Kralj-Hans I et al (2010) Once-only flexible sigmoidoscopy screening in prevention of colorectal cancer: a multicentre randomised controlled trial. Lancet 375:1624–1633
  Article PubMed Google Scholar
• World Cancer Research Fund/American Insitute for Cancer Research Food (2007) Nutrition, physical activity and the prevention of cancer: a global perspective. AICR, Washington, DC
  Google Scholar
• Aune D, Chan DS, Lau R et al (2011) Dietary fibre, whole grains, and risk of colorectal cancer: systematic review and dose-response meta-analysis of prospective studies. BMJ 343:d6617
  Article PubMed Google Scholar
• Aune D, Lau R, Chan DS et al (2011) Nonlinear reduction in risk for colorectal cancer by fruit and vegetable intake based on meta-analysis of prospective studies. Gastroenterology 141:106–118
  Article PubMed Google Scholar
• Aune D, Lau R, Chan DS et al (2012) Dairy products and colorectal cancer risk: a systematic review and meta-analysis of cohort studies. Ann Oncol 23:37–45
  Article PubMed CAS Google Scholar
• Chan DS, Lau R, Aune D et al (2011) Red and processed meat and colorectal cancer incidence: meta-analysis of prospective studies. PLoS ONE 6:e20456
  Article PubMed CAS Google Scholar
• Saebø M, Skjelbred CF, Brekke LK et al (2008) CYP1A2 164 A→C polymorphism, cigarette smoking, consumption of well-done red meat and risk of developing colorectal adenomas and carcinomas. Anticancer Res 28:2289–2295
  PubMed Google Scholar
• Ferrucci LM, Sinha R, Graubard BI et al (2009) Dietary meat intake in relation to colorectal adenoma in asymptomatic women. Am J Gastroenterol 104:1231–1240
  Article PubMed CAS Google Scholar
• Wang H, Yamamoto JF, Caberto C et al (2011) Genetic variation in the bioactivation pathway for polycyclic hydrocarbons and heterocyclic amines in relation to risk of colorectal neoplasia. Carcinogenesis 32:203–209
  Article PubMed CAS Google Scholar
• Northwood EL, Elliott F, Forman D et al (2010) Polymorphisms in xenobiotic metabolizing enzymes and diet influence colorectal adenoma risk. Pharmacogenet Genomics 20:315–326
  Article PubMed CAS Google Scholar
• Ramadas A, Kandiah M (2009) Food intake and colorectal adenomas: a case-control study in Malaysia. Asian Pac J Cancer Prev 10:925–932
  PubMed Google Scholar
• Burnett-Hartman AN, Newcomb PA, Mandelson MT et al (2011) Colorectal polyp type and the association with charred meat consumption, smoking, and microsomal epoxide hydrolase polymorphisms. Nutr Cancer 63:583–592
  Article PubMed Google Scholar
• Fu Z, Shrubsole MJ, Smalley WE et al (2011) Association of meat intake and meat-derived mutagen exposure with the risk of colorectal polyps by histologic type. Cancer Prev Res (Phila) 4:1686–1697
  Article Google Scholar
• Wu K, Giovannucci E, Byrne C et al (2006) Meat mutagens and risk of distal colon adenoma in a cohort of U.S. men. Cancer Epidemiol Biomarkers Prev 15:1120–1125
  Article PubMed CAS Google Scholar
• Cho E, Willett WC, Colditz GA et al (2007) Dietary choline and betaine and the risk of distal colorectal adenoma in women. J Natl Cancer Inst 99:1224–1231
  Article PubMed Google Scholar
• Rohrmann S, Hermann S, Linseisen J (2009) Heterocyclic aromatic amine intake increases colorectal adenoma risk: findings from a prospective European cohort study. Am J Clin Nutr 89:1418–1424
  Article PubMed CAS Google Scholar
• Tantamango YM, Knutsen SF, Beeson WL, Fraser G, Sabate J (2011) Foods and food groups associated with the incidence of colorectal polyps: the adventist health study. Nutr Cancer 63:565–572
  Article PubMed CAS Google Scholar
• Cross AJ, Sinha R, Wood RJ et al (2011) Iron homeostasis and distal colorectal adenoma risk in the prostate, lung, colorectal, and ovarian cancer screening trial. Cancer Prev Res (Phila) 4:1465–1475
  Article CAS Google Scholar
• Ferrucci LM, Sinha R, Huang WY et al (2012) Meat consumption and the risk of incident distal colon and rectal adenoma. Br J Cancer 106:608–616
  Article PubMed CAS Google Scholar
• Yoon H, Benamouzig R, Little J, Francois-Collange M, Tome D (2000) Systematic review of epidemiological studies on meat, dairy products and egg consumption and risk of colorectal adenomas. Eur J Cancer Prev 9:151–164
  Article PubMed CAS Google Scholar
• Xu X, Yu E, Gao X et al (2012) Red and processed meat intake and risk of colorectal adenomas: a meta-analysis of observational studies. Int J Cancer 132:437–448
  Article PubMed Google Scholar
• Stroup DF, Berlin JA, Morton SC et al (2000) Meta-analysis of observational studies in epidemiology: a proposal for reporting. meta-analysis of observational studies in epidemiology (MOOSE) group. JAMA 283:2008–2012
  Article PubMed CAS Google Scholar
• Haile RW, Witte JS, Longnecker MP et al (1997) A sigmoidoscopy-based case-control study of polyps: macronutrients, fiber and meat consumption. Int J Cancer 73:497–502
  Article PubMed CAS Google Scholar
• Sinha R, Chow WH, Kulldorff M et al (1999) Well-done, grilled red meat increases the risk of colorectal adenomas. Cancer Res 59:4320–4324
  PubMed CAS Google Scholar
• Voskuil DW, Kampman E, Grubben MJ et al (2002) Meat consumption and meat preparation in relation to colorectal adenomas among sporadic and HNPCC family patients in The Netherlands. Eur J Cancer 38:2300–2308
  Article PubMed CAS Google Scholar
• Tiemersma EW, Voskuil DW, Bunschoten A et al (2004) Risk of colorectal adenomas in relation to meat consumption, meat preparation, and genetic susceptibility in a Dutch population. Cancer Causes Control 15:225–236
  Article PubMed Google Scholar
• Gunter MJ, Probst-Hensch NM, Cortessis VK, Kulldorff M, Haile RW, Sinha R (2005) Meat intake, cooking-related mutagens and risk of colorectal adenoma in a sigmoidoscopy-based case-control study. Carcinogenesis 26:637–642
  Article PubMed CAS Google Scholar
• Shin A, Shrubsole MJ, Ness RM et al (2007) Meat and meat-mutagen intake, doneness preference and the risk of colorectal polyps: the Tennessee Colorectal Polyp Study. Int J Cancer 121:136–142
  Article PubMed CAS Google Scholar
• Kahn HS, Tatham LM, Thun MJ, Heath CW Jr (1998) Risk factors for self-reported colon polyps. J Gen Intern Med 13:303–310
  Article PubMed CAS Google Scholar
• Nagata C, Shimizu H, Kametani M, Takeyama N, Ohnuma T, Matsushita S (2001) Diet and colorectal adenoma in Japanese males and females. Dis Colon Rectum 44:105–111
  Article PubMed CAS Google Scholar
• Chan AT, Ma J, Tranah GJ et al (2005) Hemochromatosis gene mutations, body iron stores, dietary iron, and risk of colorectal adenoma in women. J Natl Cancer Inst 97:917–926
  Article PubMed CAS Google Scholar
• Benito E, Cabeza E, Moreno V, Obrador A, Bosch FX (1993) Diet and colorectal adenomas: a case-control study in Majorca. Int J Cancer 55:213–219
  Article PubMed CAS Google Scholar
• Macquart-Moulin G, Riboli E, Cornee J, Kaaks R, Berthezene P (1987) Colorectal polyps and diet: a case-control study in Marseilles. Int J Cancer 40:179–188
  Article PubMed CAS Google Scholar
• Erhardt JG, Kreichgauer HP, Meisner C, Bode JC, Bode C (2002) Alcohol, cigarette smoking, dietary factors and the risk of colorectal adenomas and hyperplastic polyps—a case control study. Eur J Nutr 41:35–43
  Article PubMed Google Scholar
• Senesse P, Boutron-Ruault MC, Faivre J, Chatelain N, Belghiti C, Meance S (2002) Foods as risk factors for colorectal adenomas: a case-control study in Burgundy (France). Nutr Cancer 44:7–15
  Article PubMed Google Scholar
• Ward MH, Cross AJ, Divan H et al (2007) Processed meat intake, CYP2A6 activity and risk of colorectal adenoma. Carcinogenesis 28:1210–1216
  Article PubMed CAS Google Scholar
• Kune GA, Kune S, Read A, MacGowan K, Penfold C, Watson LF (1991) Colorectal polyps, diet, alcohol, and family history of colorectal cancer: a case-control study. Nutr Cancer 16:25–30
  Article PubMed CAS Google Scholar
• Sandler RS, Lyles CM, Peipins LA, McAuliffe CA, Woosley JT, Kupper LL (1993) Diet and risk of colorectal adenomas: macronutrients, cholesterol, and fiber. J Natl Cancer Inst 85:884–891
  Article PubMed CAS Google Scholar
• Lubin F, Rozen P, Arieli B et al (1997) Nutritional and lifestyle habits and water-fiber interaction in colorectal adenoma etiology. Cancer Epidemiol Biomarkers Prev 6:79–85
  PubMed CAS Google Scholar
• Breuer-Katschinski B, Nemes K, Marr A et al (2001) Colorectal adenomas and diet: a case-control study. Colorectal Adenoma Study Group. Dig Dis Sci 46:86–95
  Article PubMed CAS Google Scholar
• Chiu BC, Gapstur SM (2004) Changes in diet during adult life and risk of colorectal adenomas. Nutr Cancer 49:49–58
  Article PubMed Google Scholar
• Probst-Hensch NM, Sinha R, Longnecker MP et al (1997) Meat preparation and colorectal adenomas in a large sigmoidoscopy-based case-control study in California (United States). Cancer Causes Control 8:175–183
  Article PubMed CAS Google Scholar
• Shin A, Shrubsole MJ, Rice JM et al (2008) Meat intake, heterocyclic amine exposure, and metabolizing enzyme polymorphisms in relation to colorectal polyp risk. Cancer Epidemiol Biomarkers Prev 17:320–329
  Article PubMed CAS Google Scholar
• Giovannucci E, Stampfer MJ, Colditz G, Rimm EB, Willett WC (1992) Relationship of diet to risk of colorectal adenoma in men. J Natl Cancer Inst 84:91–98
  Article PubMed CAS Google Scholar
• Lieberman DA, Prindiville S, Weiss DG, Willett W (2003) Risk factors for advanced colonic neoplasia and hyperplastic polyps in asymptomatic individuals. JAMA 290:2959–2967
  Article PubMed Google Scholar
• Wu K, Hu FB, Fuchs C, Rimm EB, Willett WC, Giovannucci E (2004) Dietary patterns and risk of colon cancer and adenoma in a cohort of men (United States). Cancer Causes Control 15:853–862
  Article PubMed Google Scholar
• Sinha R, Peters U, Cross AJ et al (2005) Meat, meat cooking methods and preservation, and risk for colorectal adenoma. Cancer Res 65:8034–8041
  Article PubMed CAS Google Scholar
• Sinha R, Kulldorff M, Gunter MJ, Strickland P, Rothman N (2005) Dietary benzo[a]pyrene intake and risk of colorectal adenoma. Cancer Epidemiol Biomarkers Prev 14:2030–2034
  Article PubMed CAS Google Scholar
• Sinha R, Kulldorff M, Chow WH, Denobile J, Rothman N (2001) Dietary intake of heterocyclic amines, meat-derived mutagenic activity, and risk of colorectal adenomas. Cancer Epidemiol Biomarkers Prev 10:559–562
  PubMed CAS Google Scholar
• Diergaarde B, Tiemersma EW, Braam H et al (2005) Dietary factors and truncating APC mutations in sporadic colorectal adenomas. Int J Cancer 113:126–132
  Article PubMed CAS Google Scholar
• Almendingen K, Hofstad B, Trygg K, Hoff G, Hussain A, Vatn M (2001) Current diet and colorectal adenomas: a case-control study including different sets of traditionally chosen control groups. Eur J Cancer Prev 10:395–406
  Article PubMed CAS Google Scholar
• Almendingen K, Hofstad B, Vatn MH (2004) Dietary habits and growth and recurrence of colorectal adenomas: results from a three-year endoscopic follow-up study. Nutr Cancer 49:131–138
  Article PubMed Google Scholar
• Wark PA, Van der KW, Ploemacher J et al (2006) Diet, lifestyle and risk of K-ras mutation-positive and -negative colorectal adenomas. Int J Cancer 119:398–405
  Article PubMed CAS Google Scholar
• Ferrucci LM, Cross AJ, Gunter MJ et al (2010) Xenobiotic metabolizing genes, meat-related exposures, and risk of advanced colorectal adenoma. World Rev Nutr Diet 101:34–45
  Article PubMed CAS Google Scholar
• Kato I, Tominaga S, Matsuura A, Yoshii Y, Shirai M, Kobayashi S (1990) A comparative case-control study of colorectal cancer and adenoma. Jpn J Cancer Res 81:1101–1108
  Article PubMed CAS Google Scholar
• Kono S, Shinchi K, Ikeda N, Yanai F, Imanishi K (1991) Physical activity, dietary habits and adenomatous polyps of the sigmoid colon: a study of self-defense officials in Japan. J Clin Epidemiol 44:1255–1261
  Article PubMed CAS Google Scholar
• Kono S, Imanishi K, Shinchi K, Yanai F (1993) Relationship of diet to small and large adenomas of the sigmoid colon. Jpn J Cancer Res 84:13–19
  Article PubMed CAS Google Scholar
• Todoroki I, Kono S, Shinchi K et al (1995) Relationship of cigarette smoking, alcohol use, and dietary habits with sigmoid colon adenomas. Ann Epidemiol 5:478–483
  Article PubMed CAS Google Scholar
• Neugut AI, Garbowski GC, Lee WC et al (1993) Dietary risk factors for the incidence and recurrence of colorectal adenomatous polyps. A case-control study. Ann Intern Med 118:91–95
  PubMed CAS Google Scholar
• Faivre J, Boutron MC, Senesse P, Couillault C, Belighiti C, Meny B (1997) Environmental and familial risk factors in relation to the colorectal adenoma–carcinoma sequence: results of a case-control study in Burgundy (France). Eur J Cancer Prev 6:127–131
  PubMed CAS Google Scholar
• Hoshiyama Y, Kono S, Sasaba T, Shigematsu T, Kawaguchi T (2000) Relation of cigarette smoking, alcohol use, and dietary habits to colon adenomas: a case-control study in Saitama, Japan. Asian Pac J Cancer Prev 1:139–146
  PubMed Google Scholar
• Skjelbred CF, Saebø M, Hjartaker A et al (2007) Meat, vegetables and genetic polymorphisms and the risk of colorectal carcinomas and adenomas. BMC Cancer 7:228
  Article PubMed Google Scholar
• Wallace K, Grau MV, Ahnen D et al (2009) The association of lifestyle and dietary factors with the risk for serrated polyps of the colorectum. Cancer Epidemiol Biomarkers Prev 18:2310–2317
  Article PubMed Google Scholar
• Robertson DJ, Sandler RS, Haile R et al (2005) Fat, fiber, meat and the risk of colorectal adenomas. Am J Gastroenterol 100:2789–2795
  Article PubMed Google Scholar
• Tseng M, Sandler RS, Greenberg ER, Mandel JS, Haile RW, Baron JA (1997) Dietary iron and recurrence of colorectal adenomas. Cancer Epidemiol Biomarkers Prev 6:1029–1032
  PubMed CAS Google Scholar
• Mathew A, Sinha R, Burt R et al (2004) Meat intake and the recurrence of colorectal adenomas. Eur J Cancer Prev 13:159–164
  Article PubMed CAS Google Scholar
• DerSimonian R, Kacker R (2007) Random-effects model for meta-analysis of clinical trials: an update. Contemp Clin Trials 28:105–114
  Article PubMed Google Scholar
• Greenland S, Longnecker MP (1992) Methods for trend estimation from summarized dose-response data, with applications to meta-analysis. Am J Epidemiol 135:1301–1309
  PubMed CAS Google Scholar
• Norat T, Lukanova A, Ferrari P, Riboli E (2002) Meat consumption and colorectal cancer risk: dose-response meta-analysis of epidemiological studies. Int J Cancer 98:241–256
  Article PubMed CAS Google Scholar
• Royston P (2000) A strategy for modelling the effect of a continuous covariate in medicine and epidemiology. Stat Med 19:1831–1847
  Article PubMed CAS Google Scholar
• Higgins JP, Thompson SG (2002) Quantifying heterogeneity in a meta-analysis. Stat Med 21:1539–1558
  Article PubMed Google Scholar
• Egger M, Davey SG, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315:629–634
  Article PubMed CAS Google Scholar
• Begg CB, Mazumdar M (1994) Operating characteristics of a rank correlation test for publication bias. Biometrics 50:1088–1101
  Article PubMed CAS Google Scholar
• Martinez ME, Jacobs ET, Ashbeck EL et al (2007) Meat intake, preparation methods, mutagens and colorectal adenoma recurrence. Carcinogenesis 28:2019–2027
  Article PubMed CAS Google Scholar
• Ohgaki H, Kusama K, Matsukura N et al (1984) Carcinogenicity in mice of a mutagenic compound, 2-amino-3-methylimidazo[4,5-f]quinoline, from broiled sardine, cooked beef and beef extract. Carcinogenesis 5:921–924
  Article PubMed CAS Google Scholar
• Dashwood RH, Suzui M, Nakagama H, Sugimura T, Nagao M (1998) High frequency of beta-catenin (ctnnb1) mutations in the colon tumors induced by two heterocyclic amines in the F344 rat. Cancer Res 58:1127–1129
  PubMed CAS Google Scholar
• Tappel A (2007) Heme of consumed red meat can act as a catalyst of oxidative damage and could initiate colon, breast and prostate cancers, heart disease and other diseases. Med Hypotheses 68:562–564
  Article PubMed CAS Google Scholar
• Cross AJ, Pollock JR, Bingham SA (2003) Haem, not protein or inorganic iron, is responsible for endogenous intestinal N-nitrosation arising from red meat. Cancer Res 63:2358–2360
  PubMed CAS Google Scholar
• Lijinsky W (1987) Carcinogenicity and mutagenicity of N-nitroso compounds. Mol Toxicol 1:107–119
  PubMed CAS Google Scholar