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Meat intake and bladder cancer in a prospective study: a role for heterocyclic aromatic amines?

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An Erratum to this article was published on 26 April 2008

Abstract

Background

The suspect carcinogens, heterocyclic amines (HAAs), found in well-done meat require host-mediated metabolic activation before inducing DNA mutations. The role of SULT1A1 and of NAT2 on the activation of HAAs suggests that NAT2 rapid acetylator genotype and SULT1A1 allele variants can have an effect on HAA carcinogenicity.

Methods

Data were collected as part of a case–control study nested within the EPIC cohort, the Gen Air investigation. EPIC is a prospective study designed to investigate the relationship between nutrition and cancer. Information was collected through a non-dietary questionnaire on lifestyle variables and through a dietary questionnaire. The subjects were restricted to non-smokers. We calculated the matched odds ratio for bladder cancer risk using logistic regression, controlling for potential confounders.

Results

There were 227 bladder cases and 612 controls matched 1:3. Meat intake and NAT2 genotype were not independently associated with bladder cancer risk. A significant relationship was observed between bladder cancer risk and consumption of meat only among subjects with the rapid NAT2 genotype (odds ratios [OR] 2.9, 95% CI 1.0–7.9 for the 2nd quartile of meat intake; 3.6, 95% CI 1.3–9.7 for the 3rd quartile; and 3.5, 95% CI 1.2–9.7 for the 4th quartile), and was not present among subjects with the slow genotype. An interaction between NAT2 and meat intake was found in logistic regression (P = 0.034). No association was observed for SULT1A *1/2 genotype (1.0; 95% CI 0.7–1.5) and for SULT1A1 *2/2 genotype (0.9; 95% CI 0.5–1.7).

Conclusions

These results are suggestive of a role of meat intake and NAT2 on bladder cancer risk. They support the hypothesis that among subjects with the rapid NAT2 acetylation genotype higher levels of HAAs exposure are a bladder cancer risk factor. We did not observe an effect of SULT1A1 allele variants on this cancer. The present study adds new information on the possible long-term adverse effects of diets with high meat intake.

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References

  1. World Health Organization. The world health report. Geneva, Switzerland: World Health Organization, 2003

  2. Vineis P, Simonato L (1991) Proportion of lung and bladder cancers in males resulting from occupation: a systematic approach. Arch Environ Health 46:6–15

    Article  PubMed  CAS  Google Scholar 

  3. Vineis P, Talaska G, Malaveille C et al (1996) DNA adducts in urothelial cells: relationship with biomarkers of exposure to arylamines and polycyclic aromatic hydrocarbons from tobacco smoke. Int J Cancer 65:314–316

    Article  PubMed  CAS  Google Scholar 

  4. Steinmaus CM, Nunez S, Smith AH (2000) Diet and bladder cancer: a meta-analysis of six dietary variables. Am J Epidemiol 151:693–702

    PubMed  CAS  Google Scholar 

  5. Chyou PH, Nomura AM, Stemmermann GN (1993) A prospective study of diet, smoking, and lower urinary tract cancer. Ann Epidemiol 3:211–216

    PubMed  CAS  Google Scholar 

  6. Riboli E, Gonzalez CA, Lopez-Abente G et al (1991) Diet and bladder cancer in Spain: a multi-centre case–control study. Int J Cancer 49:214–219

    Article  PubMed  CAS  Google Scholar 

  7. Gross GA, Gruter A (1992) Quantitation of mutagenic/carcinogenic heterocyclic aromatic amines in food products. J Chromatogr 592:271–278

    Article  PubMed  CAS  Google Scholar 

  8. Boobis AR, Lynch AM, Murray S et al (1994) CYP1A2-catalyzed conversion of dietary heterocyclic amines to their major route of metabolism in humans. Cancer Res 54:89–94

    PubMed  CAS  Google Scholar 

  9. Minchin RF, Reeves PT, Teitel CH et al (1992) N-and O-acetylation of aromatic and heterocyclic amine carcinogens by human monomorphic and polymorphic acetyltransferases expressed in COS-1 cells. Biochem Biophys Res Commun 185:839–844

    Article  PubMed  CAS  Google Scholar 

  10. Hein DW, Doll MA, Fretland AJ et al (2000) Molecular genetics and epidemiology of the NAT1 and NAT2 acetylation polymorphisms. Cancer Epidemiol Biomarkers Prev 9:29–42

    PubMed  CAS  Google Scholar 

  11. Berlau J, Glei M, Pool-Zobel BL (2004) Colon cancer risk factors from nutrition. Anal Bioanal Chem 378:737–743

    Article  PubMed  CAS  Google Scholar 

  12. Butler LM, Sinha R, Millikan RC et al (2003) Heterocyclic amines, meat intake, and association with colon cancer in a population-based study. Am J Epidemiol 157:434–445

    Article  PubMed  CAS  Google Scholar 

  13. Webster DJ, Flook D, Jenkins J, Hutchings A, Routledge PA (1992) Drug acetylation in breast cancer. Br J Cancer 60:236–237

    Google Scholar 

  14. Ilett KF, Detchon P, Ingram DM, Castleden WM (1990) Acetylation phenotype is not associated with breast cancer. Cancer Res 50:6649–6651

    PubMed  CAS  Google Scholar 

  15. Sardas S, Cok I, Sardas OS, Ilhan O, Karakaya AE (1990) Polymorphic N-acetylation capacity in breast cancer patients. Int J Cancer 46:1138–1139

    Article  PubMed  CAS  Google Scholar 

  16. Ward MH, Sinha R, Heineman EF, Rothman N, Markin R, Weisenburger DD et al (1997) Risk of adenocarcinoma of the stomach and esophagus with meat cooking method and doneness preference. Int J Cancer 71:14–19

    Article  PubMed  CAS  Google Scholar 

  17. Zheng L, Wang Y, Schabath MB, Grossman HB, Wu X (2003) Sulfotransferase 1A1 (SULT1A1) polymorphism and bladder cancer risk: a case–control study. Cancer Lett 202:61–69

    Article  PubMed  CAS  Google Scholar 

  18. Nowell S, Coles B, Sinha R et al (2002) Analysis of total meat intake and exposure to individual heterocyclic amines in a case–control study of colorectal cancer: contribution of metabolic variation to risk. Mutat Res 506–507:175–185

    PubMed  Google Scholar 

  19. Wong CF, Liyou N, Leggett B, Young J, Johnson A, McManus ME (2002) Association of the SULT1A1 R213H polymorphism with colorectal cancer. Clin Exp Pharmacol Physiol 29:754–758

    Article  PubMed  CAS  Google Scholar 

  20. Sachse C, Smith G, Wilkie MJ et al Colorectal Cancer Study Group (2002) A pharmacogenetic study to investigate the role of dietary carcinogens in the etiology of colorectal cancer. Carcinogenesis 23:1839–1849

    Article  PubMed  CAS  Google Scholar 

  21. Riboli E, Hunt KJ, Slimani N et al (2002) European prospective investigation into cancer and nutrition (EPIC): study populations and data collection. Public Health Nutr 5:1113–1124

    Article  PubMed  CAS  Google Scholar 

  22. Margetts BM, Pietinen P (1997) European prospective investigation into cancer and nutrition: validity studies on dietary assessment methods. Int J Epidemiol 26 Suppl 1:S1–S5

    Article  Google Scholar 

  23. Rosner B, Gore R (2001) Measurement error correction in nutritional epidemiology based on individual foods, with application to the relation of diet to breast cancer. Am J Epidemiol 154:827–835

    Article  PubMed  CAS  Google Scholar 

  24. Linseisen J, Kesse E, Slimani N et al (2002) Meat consumption in the European prospective investigation into cancer and nutrition (EPIC) cohorts: results from 24-hour dietary recalls. Public Health Nutr 5:1243–1258

    Article  PubMed  CAS  Google Scholar 

  25. Peluso M, Hainaut P, Airoldi L et al EPIC investigators (2005) Methodology of laboratory measurements in prospective studies on gene-environment interactions: the experience of GenAir. Mutat Res 574:92–104

    PubMed  CAS  Google Scholar 

  26. Manuguerra M, Matullo G, Veglia F et al (2007) Multi-factor dimensionality reduction applied to a large prospective investigation on gene-gene and gene-environment interactions. Carcinogenesis 28:414–422

    Article  PubMed  CAS  Google Scholar 

  27. Reis IM, Hirji KF, Afifi AA (1999) Exact and asymptotic tests for homogeneity in several 2 x 2 tables. Stat Med 18:893–906

    Article  PubMed  CAS  Google Scholar 

  28. Vineis P, Veglia F, Garte S, Malaveille C, Matullo G, Dunning A et al (2007) Genetic susceptibility according to three metabolic pathways in cancers of the lung and bladder and in myeloid leukemias in nonsmokers. Ann Oncol 18:1230–1242

    Article  PubMed  CAS  Google Scholar 

  29. Chou HC, Ozawa S, Fu PP, Lang NP, Kadlubar FF (1998) Metabolic activation of methyl-hydroxylated derivatives of 7,12-dimethylbenz[a]anthracene by human liver dehydroepiandrosterone-steroid sulfotransferase. Carcinogenesis 19:1071–1076

    Article  PubMed  CAS  Google Scholar 

  30. Sandhu MS, White IR, McPherson K (2001) Systematic review of the prospective cohort studies on meat consumption and colorectal cancer risk: a meta-analytical approach. Cancer Epidemiol Biomarkers Prev 10:439–446

    PubMed  CAS  Google Scholar 

  31. Norat T, Riboli E (2001) Meat consumption and colorectal cancer: a review of epidemiologic evidence. Nutr Rev 59:37–47

    Article  PubMed  CAS  Google Scholar 

  32. 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 

  33. Augustsson K, Skog K, Jägerstad M, Dickman PW, Steineck G (1999) Dietary heterocyclic amines and cancer of the colon, rectum, bladder, and kidney: a population-based study. Lancet 353:703–707

    Article  PubMed  CAS  Google Scholar 

  34. Dolara P, Commoner B, Vithayathil A et al (1979) The effect of temperature on the formation of mutagens in heated beef stock and cooked ground beef. Mutat Res 60:231–237

    PubMed  CAS  Google Scholar 

  35. Baker R, Arlauskas A, Bonin A, Angus D (1982) Detection of mutagenic activity in human urine following fried pork or bacon meals. Cancer Lett 16:81–89

    Article  PubMed  CAS  Google Scholar 

  36. Murray S, Lake BG, Gray S et al (2001) Effect of cruciferous vegetable consumption on heterocyclic aromatic amine metabolism in man. Carcinogenesis 22:1413–1420

    Article  PubMed  CAS  Google Scholar 

  37. Pavanello S, Simioli P, Mastrangelo G et al (2002) Role of metabolic polymorphisms NAT2 and CYP1A2 on urinary mutagenicity after a pan-fried hamburger meal. Food Chem Toxicol 40:1139–1144

    Article  PubMed  CAS  Google Scholar 

  38. Michaud DS, Holick CN, Giovannucci E, Stampfer MJ (2006) Meat intake and bladder cancer risk in 2 prospective cohort studies. Am J Clin Nutr 84:1177–1183

    PubMed  CAS  Google Scholar 

  39. Garcia-Closas M, Malats N, Silverman D et al (2005) NAT2 slow acetylation, GSTM1 null genotype, and risk of bladder cancer: results from the Spanish bladder cancer study and meta-analyses. Lancet 366:649–659

    Article  PubMed  CAS  Google Scholar 

  40. Lower GM Jr, Nilsson T, Nelson CE, Wolf H, Gamsky TE, Bryan GT (1979) N-Acetyltransferase phenotype and risk in urinary bladder cancer: approaches in molecular epidemiology. Preliminary results in Sweden and Denmark. Environ Health Perspect 29:71–79

    Article  PubMed  CAS  Google Scholar 

  41. Glatt H, Boeing H, Engelke CE et al (2001) Human cytosolic sulphotransferases: genetics, characteristics, toxicological aspects. Mutat Res 482:27–40

    PubMed  CAS  Google Scholar 

  42. Day N, McKeown N, Wong M, Welch A, Bingham S (2001) Epidemiological assessment of diet: a comparison of a 7-day diary with a food frequency questionnaire using urinary markers of nitrogen, potassium and sodium. Int J Epidemiol 30:309–317

    Article  PubMed  CAS  Google Scholar 

  43. Skog KI, Johansson MA, Jagerstad MI (1998) Carcinogenic heterocyclic amines in model systems and cooked foods: a review on formation, occurrence and intake. Food Chem Toxicol 36:879–896

    Article  PubMed  CAS  Google Scholar 

  44. Rohrmann S, Linseisen J, Becker N, Sinha R EPIC Working Group on Dietary Patterns (2002) Use of high-temperature cooking methods in preparation of meat and fish in European countries. IARC Sci Publ 156:219–220

    PubMed  CAS  Google Scholar 

  45. Vineis P, Pirastu R (1997) Aromatic amines and cancer. Cancer Causes Control 8:346–355

    Article  PubMed  CAS  Google Scholar 

  46. Vineis P, Marinelli D, Autrup H et al (2001) Current smoking, occupation, N-acetyltransferase-2 and bladder cancer: a pooled analysis of genotype-based studies. Cancer Epidemiol Biomarkers Prev 10:1249–1252

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This paper was made possible by a grant of the European Community (5th Framework Program) to PV (GENAIR investigation, grant QLK4-CT-1999–00927) and a grant of the Compagnia di San Paolo to the ISI Foundation. All authors are independent from funders.

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Correspondence to P. Vineis.

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An erratum to this article can be found at http://dx.doi.org/10.1007/s10552-008-9157-2

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Lumbreras, B., Garte, S., Overvad, K. et al. Meat intake and bladder cancer in a prospective study: a role for heterocyclic aromatic amines?. Cancer Causes Control 19, 649–656 (2008). https://doi.org/10.1007/s10552-008-9121-1

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