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Published in: Cancer Causes & Control 4/2013

01-04-2013 | Review article

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

Authors: Dagfinn Aune, Doris S. M. Chan, Ana Rita Vieira, Deborah A. Navarro Rosenblatt, Rui Vieira, Darren C. Greenwood, Ellen Kampman, Teresa Norat

Published in: Cancer Causes & Control | Issue 4/2013

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Abstract

Background

Current evidence indicates that red and processed meat intake increases the risk of colorectal cancer; however, the association with colorectal adenomas is unclear.

Objective

To conduct a systematic review and meta-analysis of epidemiological studies of red and processed meat intake and risk of colorectal adenomas as part of the Continuous Update Project of the World Cancer Research Fund.

Design

PubMed and several other databases were searched for relevant studies from their inception up to 31 December 2011. Summary relative risks (RRs) were estimated using a random effects model.

Results

Nineteen case–control studies and seven prospective studies were included in the analyses. The summary RR per 100 g/day of red meat was 1.27 (95 % CI 1.16–1.40, I 2 = 5 %, n = 16) for all studies combined, 1.20 (95 % CI 1.06–1.36, I 2 = 0 %, n = 6) for prospective studies, and 1.34 (95 % CI 1.12–1.59, I 2 = 31 %, n = 10) for case–control studies. The summary RR per 50 g/day of processed meat intake was 1.29 (95 % CI 1.10–1.53, I 2 = 27 %, n = 10) for all studies combined, 1.45 (95 % CI 1.10–1.90, I 2 = 0 %, n = 2) for prospective studies, and 1.23 (95 % CI 0.99–1.52, I 2 = 37 %, n = 8) for case–control studies. There was evidence of a nonlinear association between red meat (p nonlinearity < 0.001) and processed meat (p nonlinearity = 0.01) intake and colorectal adenoma risk.

Conclusion

These results indicate an elevated risk of colorectal adenomas with intake of red and processed meat, but further prospective studies are warranted.
Appendix
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Literature
1.
go back to reference 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 127:2893–2917PubMedCrossRef 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 127:2893–2917PubMedCrossRef
2.
go back to reference Leslie A, Carey FA, Pratt NR, Steele RJ (2002) The colorectal adenoma-carcinoma sequence. Br J Surg 89:845–860PubMedCrossRef Leslie A, Carey FA, Pratt NR, Steele RJ (2002) The colorectal adenoma-carcinoma sequence. Br J Surg 89:845–860PubMedCrossRef
3.
go back to reference Atkin WS, Morson BC, Cuzick J (1992) Long-term risk of colorectal cancer after excision of rectosigmoid adenomas. N Engl J Med 326:658–662PubMedCrossRef Atkin WS, Morson BC, Cuzick J (1992) Long-term risk of colorectal cancer after excision of rectosigmoid adenomas. N Engl J Med 326:658–662PubMedCrossRef
4.
go back to reference 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 375:1624–1633PubMedCrossRef 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 375:1624–1633PubMedCrossRef
5.
go back to reference 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 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
6.
go back to reference 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:d6617PubMedCrossRef 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:d6617PubMedCrossRef
7.
go back to reference 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 141:106–118PubMedCrossRef 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 141:106–118PubMedCrossRef
8.
go back to reference 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 23:37–45PubMedCrossRef 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 23:37–45PubMedCrossRef
9.
go back to reference 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:e20456PubMedCrossRef 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:e20456PubMedCrossRef
10.
go back to reference 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 28:2289–2295PubMed 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 28:2289–2295PubMed
11.
go back to reference Ferrucci LM, Sinha R, Graubard BI et al (2009) Dietary meat intake in relation to colorectal adenoma in asymptomatic women. Am J Gastroenterol 104:1231–1240PubMedCrossRef Ferrucci LM, Sinha R, Graubard BI et al (2009) Dietary meat intake in relation to colorectal adenoma in asymptomatic women. Am J Gastroenterol 104:1231–1240PubMedCrossRef
12.
go back to reference 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 32:203–209PubMedCrossRef 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 32:203–209PubMedCrossRef
13.
go back to reference Northwood EL, Elliott F, Forman D et al (2010) Polymorphisms in xenobiotic metabolizing enzymes and diet influence colorectal adenoma risk. Pharmacogenet Genomics 20:315–326PubMedCrossRef Northwood EL, Elliott F, Forman D et al (2010) Polymorphisms in xenobiotic metabolizing enzymes and diet influence colorectal adenoma risk. Pharmacogenet Genomics 20:315–326PubMedCrossRef
14.
go back to reference Ramadas A, Kandiah M (2009) Food intake and colorectal adenomas: a case-control study in Malaysia. Asian Pac J Cancer Prev 10:925–932PubMed Ramadas A, Kandiah M (2009) Food intake and colorectal adenomas: a case-control study in Malaysia. Asian Pac J Cancer Prev 10:925–932PubMed
15.
go back to reference 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 63:583–592PubMedCrossRef 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 63:583–592PubMedCrossRef
16.
go back to reference 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) 4:1686–1697CrossRef 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) 4:1686–1697CrossRef
17.
go back to reference 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 15:1120–1125PubMedCrossRef 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 15:1120–1125PubMedCrossRef
18.
go back to reference 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 99:1224–1231PubMedCrossRef 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 99:1224–1231PubMedCrossRef
19.
go back to reference 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 89:1418–1424PubMedCrossRef 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 89:1418–1424PubMedCrossRef
20.
go back to reference 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 63:565–572PubMedCrossRef 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 63:565–572PubMedCrossRef
21.
go back to reference 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) 4:1465–1475CrossRef 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) 4:1465–1475CrossRef
22.
go back to reference Ferrucci LM, Sinha R, Huang WY et al (2012) Meat consumption and the risk of incident distal colon and rectal adenoma. Br J Cancer 106:608–616PubMedCrossRef Ferrucci LM, Sinha R, Huang WY et al (2012) Meat consumption and the risk of incident distal colon and rectal adenoma. Br J Cancer 106:608–616PubMedCrossRef
23.
go back to reference 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 9:151–164PubMedCrossRef 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 9:151–164PubMedCrossRef
24.
go back to reference 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 132:437–448PubMedCrossRef 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 132:437–448PubMedCrossRef
25.
go back to reference 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 283:2008–2012PubMedCrossRef 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 283:2008–2012PubMedCrossRef
26.
go back to reference 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 73:497–502PubMedCrossRef 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 73:497–502PubMedCrossRef
27.
go back to reference Sinha R, Chow WH, Kulldorff M et al (1999) Well-done, grilled red meat increases the risk of colorectal adenomas. Cancer Res 59:4320–4324PubMed Sinha R, Chow WH, Kulldorff M et al (1999) Well-done, grilled red meat increases the risk of colorectal adenomas. Cancer Res 59:4320–4324PubMed
28.
go back to reference 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 38:2300–2308PubMedCrossRef 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 38:2300–2308PubMedCrossRef
29.
go back to reference 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 15:225–236PubMedCrossRef 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 15:225–236PubMedCrossRef
30.
go back to reference 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 26:637–642PubMedCrossRef 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 26:637–642PubMedCrossRef
31.
go back to reference 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 121:136–142PubMedCrossRef 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 121:136–142PubMedCrossRef
32.
go back to reference Kahn HS, Tatham LM, Thun MJ, Heath CW Jr (1998) Risk factors for self-reported colon polyps. J Gen Intern Med 13:303–310PubMedCrossRef Kahn HS, Tatham LM, Thun MJ, Heath CW Jr (1998) Risk factors for self-reported colon polyps. J Gen Intern Med 13:303–310PubMedCrossRef
33.
go back to reference 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 44:105–111PubMedCrossRef 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 44:105–111PubMedCrossRef
34.
go back to reference 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 97:917–926PubMedCrossRef 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 97:917–926PubMedCrossRef
35.
go back to reference Benito E, Cabeza E, Moreno V, Obrador A, Bosch FX (1993) Diet and colorectal adenomas: a case-control study in Majorca. Int J Cancer 55:213–219PubMedCrossRef Benito E, Cabeza E, Moreno V, Obrador A, Bosch FX (1993) Diet and colorectal adenomas: a case-control study in Majorca. Int J Cancer 55:213–219PubMedCrossRef
36.
go back to reference 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 40:179–188PubMedCrossRef 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 40:179–188PubMedCrossRef
37.
go back to reference 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 41:35–43PubMedCrossRef 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 41:35–43PubMedCrossRef
38.
go back to reference 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 44:7–15PubMedCrossRef 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 44:7–15PubMedCrossRef
39.
go back to reference Ward MH, Cross AJ, Divan H et al (2007) Processed meat intake, CYP2A6 activity and risk of colorectal adenoma. Carcinogenesis 28:1210–1216PubMedCrossRef Ward MH, Cross AJ, Divan H et al (2007) Processed meat intake, CYP2A6 activity and risk of colorectal adenoma. Carcinogenesis 28:1210–1216PubMedCrossRef
40.
go back to reference 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 16:25–30PubMedCrossRef 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 16:25–30PubMedCrossRef
41.
go back to reference 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 85:884–891PubMedCrossRef 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 85:884–891PubMedCrossRef
42.
go back to reference 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 6:79–85PubMed 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 6:79–85PubMed
43.
go back to reference 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 46:86–95PubMedCrossRef 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 46:86–95PubMedCrossRef
44.
go back to reference Chiu BC, Gapstur SM (2004) Changes in diet during adult life and risk of colorectal adenomas. Nutr Cancer 49:49–58PubMedCrossRef Chiu BC, Gapstur SM (2004) Changes in diet during adult life and risk of colorectal adenomas. Nutr Cancer 49:49–58PubMedCrossRef
45.
go back to reference 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 8:175–183PubMedCrossRef 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 8:175–183PubMedCrossRef
46.
go back to reference 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 17:320–329PubMedCrossRef 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 17:320–329PubMedCrossRef
47.
go back to reference 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 84:91–98PubMedCrossRef 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 84:91–98PubMedCrossRef
48.
go back to reference Lieberman DA, Prindiville S, Weiss DG, Willett W (2003) Risk factors for advanced colonic neoplasia and hyperplastic polyps in asymptomatic individuals. JAMA 290:2959–2967PubMedCrossRef Lieberman DA, Prindiville S, Weiss DG, Willett W (2003) Risk factors for advanced colonic neoplasia and hyperplastic polyps in asymptomatic individuals. JAMA 290:2959–2967PubMedCrossRef
49.
go back to reference 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 15:853–862PubMedCrossRef 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 15:853–862PubMedCrossRef
50.
go back to reference Sinha R, Peters U, Cross AJ et al (2005) Meat, meat cooking methods and preservation, and risk for colorectal adenoma. Cancer Res 65:8034–8041PubMedCrossRef Sinha R, Peters U, Cross AJ et al (2005) Meat, meat cooking methods and preservation, and risk for colorectal adenoma. Cancer Res 65:8034–8041PubMedCrossRef
51.
go back to reference 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 14:2030–2034PubMedCrossRef 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 14:2030–2034PubMedCrossRef
52.
go back to reference 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 10:559–562PubMed 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 10:559–562PubMed
53.
go back to reference Diergaarde B, Tiemersma EW, Braam H et al (2005) Dietary factors and truncating APC mutations in sporadic colorectal adenomas. Int J Cancer 113:126–132PubMedCrossRef Diergaarde B, Tiemersma EW, Braam H et al (2005) Dietary factors and truncating APC mutations in sporadic colorectal adenomas. Int J Cancer 113:126–132PubMedCrossRef
54.
go back to reference 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 10:395–406PubMedCrossRef 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 10:395–406PubMedCrossRef
55.
go back to reference 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 49:131–138PubMedCrossRef 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 49:131–138PubMedCrossRef
56.
go back to reference 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 119:398–405PubMedCrossRef 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 119:398–405PubMedCrossRef
57.
go back to reference 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 101:34–45PubMedCrossRef 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 101:34–45PubMedCrossRef
58.
go back to reference 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 81:1101–1108PubMedCrossRef 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 81:1101–1108PubMedCrossRef
59.
go back to reference 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 44:1255–1261PubMedCrossRef 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 44:1255–1261PubMedCrossRef
60.
go back to reference 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 84:13–19PubMedCrossRef 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 84:13–19PubMedCrossRef
61.
go back to reference Todoroki I, Kono S, Shinchi K et al (1995) Relationship of cigarette smoking, alcohol use, and dietary habits with sigmoid colon adenomas. Ann Epidemiol 5:478–483PubMedCrossRef Todoroki I, Kono S, Shinchi K et al (1995) Relationship of cigarette smoking, alcohol use, and dietary habits with sigmoid colon adenomas. Ann Epidemiol 5:478–483PubMedCrossRef
62.
go back to reference 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 118:91–95PubMed 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 118:91–95PubMed
63.
go back to reference 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 6:127–131PubMed 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 6:127–131PubMed
64.
go back to reference 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 1:139–146PubMed 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 1:139–146PubMed
65.
go back to reference Skjelbred CF, Saebø M, Hjartaker A et al (2007) Meat, vegetables and genetic polymorphisms and the risk of colorectal carcinomas and adenomas. BMC Cancer 7:228PubMedCrossRef Skjelbred CF, Saebø M, Hjartaker A et al (2007) Meat, vegetables and genetic polymorphisms and the risk of colorectal carcinomas and adenomas. BMC Cancer 7:228PubMedCrossRef
66.
go back to reference 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 18:2310–2317PubMedCrossRef 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 18:2310–2317PubMedCrossRef
67.
go back to reference Robertson DJ, Sandler RS, Haile R et al (2005) Fat, fiber, meat and the risk of colorectal adenomas. Am J Gastroenterol 100:2789–2795PubMedCrossRef Robertson DJ, Sandler RS, Haile R et al (2005) Fat, fiber, meat and the risk of colorectal adenomas. Am J Gastroenterol 100:2789–2795PubMedCrossRef
68.
go back to reference Tseng M, Sandler RS, Greenberg ER, Mandel JS, Haile RW, Baron JA (1997) Dietary iron and recurrence of colorectal adenomas. Cancer Epidemiol Biomarkers Prev 6:1029–1032PubMed Tseng M, Sandler RS, Greenberg ER, Mandel JS, Haile RW, Baron JA (1997) Dietary iron and recurrence of colorectal adenomas. Cancer Epidemiol Biomarkers Prev 6:1029–1032PubMed
69.
go back to reference Mathew A, Sinha R, Burt R et al (2004) Meat intake and the recurrence of colorectal adenomas. Eur J Cancer Prev 13:159–164PubMedCrossRef Mathew A, Sinha R, Burt R et al (2004) Meat intake and the recurrence of colorectal adenomas. Eur J Cancer Prev 13:159–164PubMedCrossRef
70.
go back to reference DerSimonian R, Kacker R (2007) Random-effects model for meta-analysis of clinical trials: an update. Contemp Clin Trials 28:105–114PubMedCrossRef DerSimonian R, Kacker R (2007) Random-effects model for meta-analysis of clinical trials: an update. Contemp Clin Trials 28:105–114PubMedCrossRef
71.
go back to reference Greenland S, Longnecker MP (1992) Methods for trend estimation from summarized dose-response data, with applications to meta-analysis. Am J Epidemiol 135:1301–1309PubMed Greenland S, Longnecker MP (1992) Methods for trend estimation from summarized dose-response data, with applications to meta-analysis. Am J Epidemiol 135:1301–1309PubMed
72.
go back to reference 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 98:241–256PubMedCrossRef 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 98:241–256PubMedCrossRef
73.
go back to reference Royston P (2000) A strategy for modelling the effect of a continuous covariate in medicine and epidemiology. Stat Med 19:1831–1847PubMedCrossRef Royston P (2000) A strategy for modelling the effect of a continuous covariate in medicine and epidemiology. Stat Med 19:1831–1847PubMedCrossRef
74.
go back to reference Higgins JP, Thompson SG (2002) Quantifying heterogeneity in a meta-analysis. Stat Med 21:1539–1558PubMedCrossRef Higgins JP, Thompson SG (2002) Quantifying heterogeneity in a meta-analysis. Stat Med 21:1539–1558PubMedCrossRef
75.
go back to reference Egger M, Davey SG, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315:629–634PubMedCrossRef Egger M, Davey SG, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315:629–634PubMedCrossRef
76.
go back to reference Begg CB, Mazumdar M (1994) Operating characteristics of a rank correlation test for publication bias. Biometrics 50:1088–1101PubMedCrossRef Begg CB, Mazumdar M (1994) Operating characteristics of a rank correlation test for publication bias. Biometrics 50:1088–1101PubMedCrossRef
77.
go back to reference Martinez ME, Jacobs ET, Ashbeck EL et al (2007) Meat intake, preparation methods, mutagens and colorectal adenoma recurrence. Carcinogenesis 28:2019–2027PubMedCrossRef Martinez ME, Jacobs ET, Ashbeck EL et al (2007) Meat intake, preparation methods, mutagens and colorectal adenoma recurrence. Carcinogenesis 28:2019–2027PubMedCrossRef
78.
go back to reference 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 5:921–924PubMedCrossRef 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 5:921–924PubMedCrossRef
79.
go back to reference 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 58:1127–1129PubMed 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 58:1127–1129PubMed
80.
go back to reference 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 68:562–564PubMedCrossRef 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 68:562–564PubMedCrossRef
81.
go back to reference 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 63:2358–2360PubMed 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 63:2358–2360PubMed
82.
go back to reference Lijinsky W (1987) Carcinogenicity and mutagenicity of N-nitroso compounds. Mol Toxicol 1:107–119PubMed Lijinsky W (1987) Carcinogenicity and mutagenicity of N-nitroso compounds. Mol Toxicol 1:107–119PubMed
Metadata
Title
Red and processed meat intake and risk of colorectal adenomas: a systematic review and meta-analysis of epidemiological studies
Authors
Dagfinn Aune
Doris S. M. Chan
Ana Rita Vieira
Deborah A. Navarro Rosenblatt
Rui Vieira
Darren C. Greenwood
Ellen Kampman
Teresa Norat
Publication date
01-04-2013
Publisher
Springer Netherlands
Published in
Cancer Causes & Control / Issue 4/2013
Print ISSN: 0957-5243
Electronic ISSN: 1573-7225
DOI
https://doi.org/10.1007/s10552-012-0139-z

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