Top

Published in:

Open Access 01-08-2021 | META-ANALYSIS

The association between meat and fish consumption and bladder cancer risk: a pooled analysis of 11 cohort studies

Authors: Mostafa Dianatinasab, Anke Wesselius, Tessa de Loeij, Amin Salehi-Abargouei, Evan Y. W. Yu, Mohammad Fararouei, Maree Brinkman, Piet van den Brandt, Emily White, Elisabete Weiderpass, Florence Le Calvez-Kelm, Marc J. Gunter, Inge Huybrechts, Fredrik Liedberg, Guri Skeie, Anne Tjonneland, Elio Riboli, Maurice P. Zeegers

Published in: European Journal of Epidemiology | Issue 8/2021

Abstract

Evidence on the effects of meat consumption from different sources on the risk of bladder cancer (BC) is limited and controversial. Therefore, this study aimed to evaluate the associations between meat consumption and BC risk using a pooled data approach. Individual data from 11 prospective cohorts comprising 2848 BC cases and 515,697 non-cases with a total of 5,498,025 person-years of follow-up was pooled and analysed to investigate the potential associations between total red meat and products, red meat, processed meat, poultry and total fish and BC risk. Hazard ratios (HRs), with corresponding 95% confidence intervals (CIs), were estimated using Cox regression models stratified on cohort. Overall, an increased BC risk was found for high intake of organ meat (HR comparing highest with lowest tertile: 1.18, 95% CI: 1.03, 1.36, p-trend = 0.03). On the contrary, a marginally inverse association was observed for total fish intake and BC risk among men (HR comparing highest with lowest tertile: 0.79, 95% CI 0.65, 0.97, p-trend = 0.04). No associations were observed for other meat sources. Results of this prospective study suggest that organ meat consumption may be associated with BC development. Replication in large-scale prospective studies and investigation of possible causal mechanisms is needed.

Available only for authorised users

Sung H, Ferlay J, Siegel RL, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021. https://doi.org/10.3322/caac.21660.CrossRef

Parkin DM. The global burden of urinary bladder cancer. Scand J Urol Nephrol Suppl. 2008;42(218):12–20. https://doi.org/10.1080/03008880802285032.CrossRef

Mossanen M, Gore JL. The burden of bladder cancer care: direct and indirect costs. Curr Opin Urol. 2014;24(5):487–91.CrossRef

Al-Zalabani AH, Stewart KF, Wesselius A, Schols AM, Zeegers MP. Modifiable risk factors for the prevention of bladder cancer: a systematic review of meta-analyses. Eur J Epidemiol. 2016;31(9):811–51. https://doi.org/10.1007/s10654-016-0138-6.CrossRefPubMedPubMedCentral

Janković S, Radosavljević V. Risk factors for bladder cancer. Tumori J. 2007;93(1):4–12.CrossRef

Clinton SK, Giovannucci EL, Hursting SD. The World Cancer Research Fund/American Institute for Cancer Research third expert report on diet, nutrition, physical activity, and cancer: impact and future directions. J Nutr. 2020;150(4):663–71.CrossRef

Bogovski P, Bogovski S. Special report animal species in which n-nitroso compounds induce cancer. Int J Cancer. 1981;27(4):471–4.CrossRef

Bryan GT. The pathogenesis of experimental bladder cancer. Cancer Res. 1977;37(8 Pt 2):2813–6.PubMed

Grosse Y, Baan R, Straif K, et al. Carcinogenicity of nitrate, nitrite, and cyanobacterial peptide toxins. Lancet Oncol. 2006;7(8):628–9. https://doi.org/10.1016/s1470-2045(06)70789-6.CrossRefPubMed

10.

Mirvish SS. Role of N-nitroso compounds (NOC) and N-nitrosation in etiology of gastric, esophageal, nasopharyngeal and bladder cancer and contribution to cancer of known exposures to NOC. Cancer Lett. 1995;93(1):17–48. https://doi.org/10.1016/0304-3835(95)03786-V.CrossRefPubMed

11.

Dianatinasab M, Wesselius A, Salehi-Abargouei A, et al. Adherence to a Western dietary pattern and risk of bladder cancer: a pooled analysis of 13 cohort studies of the Bladder Cancer Epidemiology and Nutritional Determinants international study. Int J Cancer. 2020. https://doi.org/10.1002/ijc.33173.CrossRefPubMedPubMedCentral

12.

Larsson SC, Johansson JE, Andersson SO, Wolk A. Meat intake and bladder cancer risk in a Swedish prospective cohort. Cancer Causes Control. 2009;20(1):35–40. https://doi.org/10.1007/s10552-008-9214-x.CrossRefPubMed

13.

Ferrucci LM, Sinha R, Ward MH, et al. Meat and components of meat and the risk of bladder cancer in the NIH-AARP Diet and Health Study. Cancer. 2010;116(18):4345–53. https://doi.org/10.1002/cncr.25463.CrossRefPubMed

14.

Xu X. Processed meat intake and bladder cancer risk in the prostate, lung, colorectal, and ovarian (PLCO) cohort. Cancer Epidemiol Biomarkers Prev. 2019;28(12):1993–7. https://doi.org/10.1158/1055-9965.EPI-19-0604.CrossRefPubMed

15.

Crippa A, Larsson SC, Discacciati A, Wolk A, Orsini N. Red and processed meat consumption and risk of bladder cancer: a dose–response meta-analysis of epidemiological studies. Eur J Nutr. 2018;57(2):689–701.CrossRef

16.

Li F, An S, Hou L, Chen P, Lei C, Tan W. Red and processed meat intake and risk of bladder cancer: a meta-analysis. Int J Clin Exp Med. 2014;7(8):2100–10.PubMedPubMedCentral

17.

Goossens ME, Isa F, Brinkman M, et al. International pooled study on diet and bladder cancer: the bladder cancer, epidemiology and nutritional determinants (BLEND) study: design and baseline characteristics. Arch Public Health. 2016;74:30. https://doi.org/10.1186/s13690-016-0140-1.CrossRefPubMedPubMedCentral

18.

Riboli E, Kaaks R. The EPIC Project: rationale and study design. European Prospective Investigation into Cancer and Nutrition. Int J Epidemiol. 1997;26(Suppl 1):S6–14. https://doi.org/10.1093/ije/26.suppl_1.s6.CrossRefPubMed

19.

Tjonneland A, Olsen A, Boll K, 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(4):432–41. https://doi.org/10.1080/14034940601047986.CrossRefPubMed

20.

Clavel-Chapelon F, van Liere MJ, Giubout C, et al. E3N, a French cohort study on cancer risk factors. E3N Group. Etude Epidemiologique aupres de femmes de l’Education Nationale. Eur J Cancer Prev. 1997;6(5):473–8. https://doi.org/10.1097/00008469-199710000-00007.CrossRefPubMed

21.

Boeing H, Korfmann A, Bergmann MM. Recruitment procedures of EPIC-Germany. European Investigation into Cancer and Nutrition. Ann Nutr Metab. 1999;43(4):205–15. https://doi.org/10.1159/000012787.CrossRefPubMed

22.

Panico S, Dello Iacovo R, Celentano E, et al. Progetto ATENA, a study on the etiology of major chronic diseases in women: design, rationale and objectives. Eur J Epidemiol. 1992;8(4):601–8. https://doi.org/10.1007/BF00146383.CrossRefPubMed

23.

Beulens JW, Monninkhof EM, Verschuren WM, et al. Cohort profile: the EPIC-NL study. Int J Epidemiol. 2010;39(5):1170–8. https://doi.org/10.1093/ije/dyp217.CrossRefPubMed

24.

Lund E, Dumeaux V, Braaten T, et al. Cohort profile: the Norwegian Women and Cancer Study–NOWAC–Kvinner og kreft. Int J Epidemiol. 2008;37(1):36–41. https://doi.org/10.1093/ije/dym137.CrossRefPubMed

25.

Riboli E, Hunt KJ, Slimani N, et al. European Prospective Investigation into Cancer and Nutrition (EPIC): study populations and data collection. Public Health Nutr. 2002;5(6B):1113–24. https://doi.org/10.1079/PHN2002394.CrossRefPubMed

26.

Manjer J, Carlsson S, Elmstahl S, et al. The Malmo Diet and Cancer Study: representativity, cancer incidence and mortality in participants and non-participants. Eur J Cancer Prev. 2001;10(6):489–99. https://doi.org/10.1097/00008469-200112000-00003.CrossRefPubMed

27.

Hallmans G, Agren A, Johansson G, et al. Cardiovascular disease and diabetes in the Northern Sweden Health and Disease Study Cohort—evaluation of risk factors and their interactions. Scand J Public Health Suppl. 2003;61:18–24. https://doi.org/10.1080/14034950310001432.CrossRefPubMed

28.

Davey GK, Spencer EA, Appleby PN, Allen NE, Knox KH, Key TJ. EPIC-Oxford: lifestyle characteristics and nutrient intakes in a cohort of 33 883 meat-eaters and 31 546 non meat-eaters in the UK. Public Health Nutr. 2003;6(3):259–69. https://doi.org/10.1079/PHN2002430.CrossRefPubMed

29.

Day N, Oakes S, Luben R, et al. EPIC-Norfolk: study design and characteristics of the cohort. European Prospective Investigation of Cancer. Br J Cancer. 1999;80(Suppl 1):95–103.PubMed

30.

van den Brandt PA, Goldbohm RA, van’t Veer P, Volovics A, Hermus RJ, Sturmans F. A large-scale prospective cohort study on diet and cancer in The Netherlands. J Clin Epidemiol. 1990;43(3):285–95. https://doi.org/10.1016/0895-4356(90)90009-e.CrossRefPubMed

31.

White E, Patterson RE, Kristal AR, et al. VITamins And Lifestyle cohort study: study design and characteristics of supplement users. Am J Epidemiol. 2004;159(1):83–93. https://doi.org/10.1093/aje/kwh010.CrossRefPubMed

32.

Percy C, Holten VV, Muir CS, Organization WH. International classification of diseases for oncology; 1990.

33.

Percy C, Holten Vv, Muir CS, World Health O. In: Percy C, Van Holten V, Muir C, editors. International classification of diseases for oncology. 2nd ed. Geneva: World Health Organization; 1990.

34.

Kaaks R, Riboli E. Validation and calibration of dietary intake measurements in the EPIC project: methodological considerations. European Prospective Investigation into Cancer and Nutrition. Int J Epidemiol. 1997;26(Suppl 1):S15–25. https://doi.org/10.1093/ije/26.suppl_1.s15.CrossRefPubMed

35.

Zeegers MP, Goldbohm RA, van den Brandt PA. Are retinol, vitamin C, vitamin E, folate and carotenoids intake associated with bladder cancer risk? Results from the Netherlands Cohort Study. Br J Cancer. 2001;85(7):977–83. https://doi.org/10.1054/bjoc.2001.1968.CrossRefPubMedPubMedCentral

36.

Ferrari P, Slimani N, Ciampi A, et al. Evaluation of under- and overreporting of energy intake in the 24-hour diet recalls in the European Prospective Investigation into Cancer and Nutrition (EPIC). Public Health Nutr. 2002;5(6b):1329–45. https://doi.org/10.1079/phn2002409.CrossRefPubMed

37.

Poortvliet E, Klensin J, Kohlmeier L. Rationale document for the Eurocode 2 food coding system (version 91/2). Eur J Clin Nutr. 1992;46(Suppl 5):S9–24.PubMed

38.

Daniel CR, Cross AJ, Graubard BI, Hollenbeck AR, Park Y, Sinha R. Prospective investigation of poultry and fish intake in relation to cancer risk. Cancer Prev Res. 2011;4(11):1903–11.CrossRef

39.

Willett WC, Howe GR, Kushi LH. Adjustment for total energy intake in epidemiologic studies. Am J Clin Nutr. 1997;65(4):1220S-S1228.CrossRef

40.

Joshi AD, Kim A, Lewinger JP, et al. Meat intake, cooking methods, dietary carcinogens, and colorectal cancer risk: findings from the Colorectal Cancer Family Registry. Cancer Med. 2015;4(6):936–52. https://doi.org/10.1002/cam4.461.CrossRefPubMedPubMedCentral

41.

Bagnardi V, Zambon A, Quatto P, Corrao G. Flexible meta-regression functions for modeling aggregate dose–response data, with an application to alcohol and mortality. Am J Epidemiol. 2004;159(11):1077–86. https://doi.org/10.1093/aje/kwh142.CrossRefPubMed

42.

Isa F, Xie LP, Hu Z, et al. Dietary consumption and diet diversity and risk of developing bladder cancer: results from the South and East China case-control study. Cancer Causes Control. 2013;24(5):885–95. https://doi.org/10.1007/s10552-013-0165-5.CrossRefPubMed

43.

Steinmaus CM, Nunez S, Smith AH. Diet and bladder cancer: a meta-analysis of six dietary variables. Am J Epidemiol. 2000;151(7):693–702. https://doi.org/10.1093/oxfordjournals.aje.a010264.CrossRefPubMed

44.

Brinkman M, Zeegers MP. Nutrition, total fluid and bladder cancer. Scand J Urol Nephrol Suppl. 2008;42(218):25–36. https://doi.org/10.1080/03008880802285073.CrossRef

45.

Lin J, Forman MR, Wang J, et al. Intake of red meat and heterocyclic amines, metabolic pathway genes and bladder cancer risk. Int J Cancer. 2012;131(8):1892–903. https://doi.org/10.1002/ijc.27437.CrossRefPubMedPubMedCentral

46.

Chiang VS-C, Quek S-Y. The relationship of red meat with cancer: Effects of thermal processing and related physiological mechanisms. Crit Rev Food Sci Nutr. 2017;57(6):1153–73.CrossRef

47.

Knize M, Andresen B, Healy S, et al. Effects of temperature, patty thickness and fat content on the production of mutagens in fried ground beef. Food Chem Toxicol. 1985;23(12):1035–40.CrossRef

48.

Di Maso M, Turati F, Bosetti C, et al. Food consumption, meat cooking methods and diet diversity and the risk of bladder cancer. Cancer Epidemiol. 2019;63:101595. https://doi.org/10.1016/j.canep.2019.101595.CrossRefPubMed

49.

Hopkins HT, Murphy EW, Smith DP. Minerals and proximate composition of organ meats. J Am Diet Assoc. 1961;38:344–9.PubMed

50.

Anderson-Otunu O, Akhtar S. Chronic infections of the urinary tract and bladder cancer risk: a systematic review. Asian Pac J Cancer Prev. 2016;17(8):3805–7.PubMed

51.

Vermeulen SH, Hanum N, Grotenhuis AJ, et al. Recurrent urinary tract infection and risk of bladder cancer in the Nijmegen bladder cancer study. Br J Cancer. 2015;112(3):594–600. https://doi.org/10.1038/bjc.2014.601.CrossRefPubMed

52.

Kjaer SK, Knudsen JB, Sorensen BL, Moller JO. The Copenhagen case-control study of bladder cancer. V. Review of the role of urinary-tract infection. Acta Oncol. 1989;28(5):631–6. https://doi.org/10.3109/02841868909092283.CrossRefPubMed

53.

Hoffmann D, Rivenson A, Abbi R, Wynder EL. A study of tobacco carcinogenesis: effect of the fat content of the diet on the carcinogenic activity of 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone in F344 rats. Can Res. 1993;53(12):2758–61.

54.

Hebert JR, Kabat GC. Distribution of smoking and its association with lung cancer: implications for studies on the association of fat with cancer. J Natl Cancer Inst. 1991;83(12):872–5.CrossRef

55.

Taioli E, Nicolosi A, Wynder E. Possible role of diet as a host factor in the aetiology of tobacco-induced lung cancer: an ecological study in southern and northern Italy. Int J Epidemiol. 1991;20(3):611.CrossRef

56.

Hoffmann D, Adams J, Piade J, Hecht S. Chemical studies on tobacco smoke LXVIII. Analysis of volatile and tobacco-specific nitrosamines in tobacco products. IARC Sci Publ. 1980;31:507.

57.

Wang C, Jiang H. Meat intake and risk of bladder cancer: a meta-analysis. Med Oncol. 2012;29(2):848–55. https://doi.org/10.1007/s12032-011-9985-x.CrossRefPubMed

58.

Tappel A. 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. 2007;68(3):562–4.CrossRef

59.

Baena AV, Allam MF, Del Castillo AS, et al. Urinary bladder cancer risk factors in men: a Spanish case-control study. Eur J Cancer Prev. 2006;15(6):498–503. https://doi.org/10.1097/01.cej.0000215618.05757.04.CrossRefPubMed

60.

Larsson SC, Kumlin M, Ingelman-Sundberg M, Wolk A. Dietary long-chain n-3 fatty acids for the prevention of cancer: a review of potential mechanisms. Am J Clin Nutr. 2004;79(6):935–45. https://doi.org/10.1093/ajcn/79.6.935.CrossRefPubMed

61.

Holick CN, Giovannucci EL, Stampfer MJ, Michaud DS. A prospective study of fish, marine fatty acids, and bladder cancer risk among men and women (United States). Cancer Causes Control. 2006;17(9):1163–73. https://doi.org/10.1007/s10552-006-0059-x.CrossRefPubMed

62.

Li Z, Yu J, Miao Q, et al. The association of fish consumption with bladder cancer risk: a meta-analysis. World J Surg Oncol. 2011;9(1):107. https://doi.org/10.1186/1477-7819-9-107.CrossRefPubMedPubMedCentral

63.

This part: World Cancer Research Fund/American Institute for Cancer Research. Continuous Update Project Expert Report 2018. Meat fadpatrocAa.dietandcancerreport.org.

64.

Michaud DS, Holick CN, Giovannucci E, Stampfer MJ. Meat intake and bladder cancer risk in 2 prospective cohort studies. Am J Clin Nutr. 2006;84(5):1177–83. https://doi.org/10.1093/ajcn/84.5.1177.CrossRefPubMed

65.

Flood A, Rastogi T, Wirfält E, et al. Dietary patterns as identified by factor analysis and colorectal cancer among middle-aged Americans. Am J Clin Nutr. 2008;88(1):176–84.CrossRef

66.

Koebnick C, Michaud D, Moore SC, et al. Body mass index, physical activity, and bladder cancer in a large prospective study. Cancer Epidemiol Biomarkers Prev. 2008;17(5):1214–21. https://doi.org/10.1158/1055-9965.EPI-08-0026.CrossRefPubMed

67.

Margetts B, Vorster H, Venter C. Evidence-based nutrition—the impact of information and selection bias on the interpretation of individual studies. South Afr J Clin Nutr. 2003;16:79.

Title: The association between meat and fish consumption and bladder cancer risk: a pooled analysis of 11 cohort studies
Authors: Mostafa Dianatinasab
Anke Wesselius
Tessa de Loeij
Amin Salehi-Abargouei
Evan Y. W. Yu
Mohammad Fararouei
Maree Brinkman
Piet van den Brandt
Emily White
Elisabete Weiderpass
Florence Le Calvez-Kelm
Marc J. Gunter
Inge Huybrechts
Fredrik Liedberg
Guri Skeie
Anne Tjonneland
Elio Riboli
Maurice P. Zeegers
Publication date: 01-08-2021
Publisher: Springer Netherlands
Published in: European Journal of Epidemiology / Issue 8/2021
Print ISSN: 0393-2990
Electronic ISSN: 1573-7284
DOI: https://doi.org/10.1007/s10654-021-00762-4

At a glance: The STEP trials

Springer Medicine

The association between meat and fish consumption and bladder cancer risk: a pooled analysis of 11 cohort studies

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 8/2021

Oral contraceptive use by formulation and endometrial cancer risk among women born in 1947–1964: The Nurses’ Health Study II, a prospective cohort study

Modern Epidemiology, 4th edition. TL Lash, TJ VanderWeele, S Haneuse, KJ Rothman. Wolters Kluwer, 2021

Maternal exposure to airborne polychlorinated biphenyls (PCBs) and risk of adverse birth outcomes

Sedentary behaviour in relation to ovarian cancer risk: a systematic review and meta-analysis

The origin of Modern Epidemiology, the book

Comparative effectiveness and safety of direct acting oral anticoagulants in nonvalvular atrial fibrillation for stroke prevention: a systematic review and meta-analysis