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Cooking of meat and fish in Europe—results from the European Prospective Investigation into Cancer and Nutrition (EPIC)

Abstract

Objectives: There is epidemiologic evidence that the consumption of fried, grilled or barbecued meat and fish that are well-done or browned may be associated with an increased cancer risk. These high-temperature cooking methods are thought to be surrogates for mutagens and carcinogens produced in meat and fish, eg heterocyclic amines or polycyclic hydrocarbons. Since data on food cooking methods are scarce, the aim of this study was to describe the variation in meat and fish cooking methods in different parts of Europe.

Design: Using a standardized 24 h recall from a sub-sample of the EPIC cohort (35 644 persons, 35–75 y old), mean daily intake of meat and fish prepared by different cooking methods and the relative contribution of the cooking methods to the overall cooking of meat and fish was calculated.

Results: Whereas frying was more often noted in northern Europe, roasting and stir frying were more often used in the south. Concerning high-temperature cooking methods, their frequency of application varies between 15% in the EPIC cohort of North-Italy and 49% in the cohort of The Netherlands. Average consumption of fried, grilled and barbecued meat and fish ranges from a low of 12 g/day in the centres in southern Spain to a high of 91 g/day in northern Spain.

Conclusion: High variation in both the kind of meat/fish consumed as well as its cooking methods is observed within EPIC. In order to use this variation for the evaluation of the impact of cooking methods on cancer risk, a questionnaire on meat and fish cooking methods is being developed and could be applied in the whole EPIC cohort.

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References

  • Adamson RH, Thorgeirsson UP, Snyderwine EG, Thorgeirsson SS, Reeves J, Dalgard DW, Takayama S, Sugimura T . 1990 Carcinogenicity of 2-amino-3-methylimidazo[4,5-f]quinoline in non-human primates: induction of tumors in three macaques Jpn. J. Cancer Res. 81: 10–14

    CAS  Article  Google Scholar 

  • Ambrosone CB, Freudenheim JL, Sinha R, Graham S, Marshall JR, Vena JE, Laughon R, Nemoto R, Shields PG . 1998 Breast cancer risk, meat consumption and N-acetyltransferase (NAT2) genetic polymorphisms Int. J. Cancer 75: 825–839

    CAS  Article  Google Scholar 

  • Augustsson K, Lindblad J, Övervik E, Steineck G . 1999a A population-based dietary inventory of cooked meat and assessment of the daily intake of food mutagens Food Additives Contamin. 16: 215–225

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  • Deitz AC, Zheng W, Leff MA, Gross M, Wen W-Q, Doll MA, Xiao GH, Folsom AR, Hein DW . 2000 N-Acetyltransferase 2 genetic polymorphisms, well-done meat intake, and breast cancer risk among postmenopausal women Cancer Epidemiol. Biomark. Prev. 9: 905–910

    CAS  Google Scholar 

  • Delfino RJ, Sinha R, Smith C, West J, White E, Lin HJ, Liao S-Y, Gim JSY, Ma HL, Butler J, Anton-Culver H . 2000 Breast cancer, heterocyclic amines from meat and N-acetyltransferase 2 genotype Carcinogenesis 21: 607–615

    CAS  Article  Google Scholar 

  • De Stefani E, Doneo-Pellegrini H, Mendilaharsu M, Ronco A . 1997a Meat intake, heterocyclic amines and risk of colorectal cancer: a case-control study in Uruguay Int. J. Oncol. 10: 573–580

    CAS  Google Scholar 

  • De Stefani E, Ronco A, Mendilaharsu M, Guidobono M, Doneo-Pellegrini H . 1997b Meat intake, heterocyclic amines, and risk of breast cancer: a case–control study in Uruguay Cancer Epidemiol. Biomark. Prev. 6: 573–581

    CAS  Google Scholar 

  • De Stefani E, Boffetta P, Mendilaharsu M, Carzoglio J, Deneo-Pellegrini H . 1998a Dietary nitrosamines, heterocyclic amines, and risk of gastric cancer: a case–control study in Uruguay Nutr. Cancer 30: 158–162

    CAS  Article  Google Scholar 

  • De Stefani E, Ronco A, Mendilaharsu M, Doneo-Pellegrini H . 1998b Case–control study on the role of heterocyclic amines in the etiology of upper aerodigestive cancers in Uruguay Nutr. Cancer 32: 43–48

    CAS  Article  Google Scholar 

  • Doneo-Pellegrini H, De Stefani E, Ronco A, Mendilaharsu M, Carzoglio JC . 1996 Meat consumption and risk of lung cancer; a case-control study from Uruguay Lung Cancer 14: 195–205

    Article  Google Scholar 

  • Ferrari P, Slimani N, Ciampi A, Trichopoulos D, Naska A, Lauria C, Veglia F, Bueno-de-Mesquita HB, Ocké MC, Brustad M, Braaten T, Tormo MJ, Amiano P, Mattisson I, Johansson G, Welch A, Davey G, Overvad K, Tjønneland A, Clavel-Chapelon F, Thiebaut A, Linseisen J, Boeing H, Hemon B, Riboli E . 2002 Evaluation of misresporting in the 24-hour diet recalls in EPIC Pub. Health Nutr. (in press)

  • Gerhardsson de Verdier M, Hagman U, Peters UK, Steineck G, Övervik E . 1991 Meat, cooking methods and colorectal cancer: a case-referent study in Stockholm Int. J. Cancer 49: 520–525

    CAS  Article  Google Scholar 

  • Gertig DM, Hankinson SE, Hough H, Spiegelman D, Colditz GA, Willett WC, Kelsey KT, Hunter DJ . 1999 N-Acetyltransferase 2 genotypes, meat intake and breast cancer risk Int. J. Cancer 80: 13–17

    CAS  Article  Google Scholar 

  • Guillén MD, Sopelana P, Partearroyo . 1997 Food as a source of polycyclic aromatic carcinogens Rev. Environ. Health 13: 133–146

    Google Scholar 

  • Jägerstad M, Laser Reuterswärd A, Öste R, Dalquist A, Grivas S, Olsson K, Nyhammar T . 1983 Creatine and Maillard reaction products as precursors of mutagenic compounds formed in fried beef ACS Symp. Ser. 215: 507–519

    Article  Google Scholar 

  • Johansson MAE, Jägerstad M . 1994 Occurrence of mutagenic/carcinogenic heterocyclic amines in meat and fish products, including pan residues, prepared under domestic conditions Carcinogenesis 15: 1511–1518

    CAS  Article  Google Scholar 

  • Kampman E, Slattery ML, Bigler J, Leppert M, Samowitz W, Caan BJ, Potter JD . 1999 Meat consumption, genetic susceptibility, and colon cancer risk: a United States multicenter case–control study Cancer Epidemiol. Biomark. Prev. 8: 14–24

    Google Scholar 

  • Keating GA, Bogen KT . 2001 Methods to estimate heterocyclic aromatic amine concentrations in cooked meats in the US diet Food Chem. Toxicol. 11: 29–43

    Article  Google Scholar 

  • Knize MG, Sinha R, Salmon CP, Metha SS, Dewhirst KP, Felton JS . 1996 Formation of heterocyclic amine mutagens/carcinogens during home and commercial cooking of muscle food J. Muscle Foods 7: 271–279

    Article  Google Scholar 

  • Larsson BK, Sahlberg GP, Eriksson AT, Busk LÅ . 1983 Polycyclic aromatic hydrocarbons in grilled food J. Agric. Food Chem. 31: 867–873

    CAS  Article  Google Scholar 

  • Linseisen J, Kesse E, Slimani N, Bueno-de-Mesquita HB, Ocké MC, Skeie G, Kumle M, Iraeta MD, Gómez PM, Janzon L, Stattin P, Welch A, Spencer EA, Overvad K, Tjønneland A, Clavel-Clapelon F, Miller AB, Klipstein-Grobusch K, Lagiou P, Kalapothaki V, Masala G, Giurdanella MC, Norat T, Riboli E . 2002 Meat consumption in the EPIC cohorts—results from the 24-hour dietary recalls Pub. Health Nutr. (in press)

  • Lyon JL, Mahoney AW . 1988 Fried foods and the risk of colon cancer Am. J. Epidemiol. 128: 1000–1006

    CAS  Article  Google Scholar 

  • Muscat JE, Wynder EL . 1994 The consumption of well-done red meat and the risk of colorectal cancer Am. J. Public Health 84: 856–858

    CAS  Article  Google Scholar 

  • Norrish AE, Ferguson LR, Knize MG, Felton JS, Sharpe SJ, Jackson RT . 1999 Heterocyclic amine content of cooked meat and risk of prostate cancer J. Natl Cancer Inst. 91: 2038–2044

    CAS  Article  Google Scholar 

  • Parkin DM, Whelan SL, Ferlay J, Raymond L, Young J . 1997 Cancer Incidence in Five Continents Vol. VII. IARC Scientific Publications no. 143 Lyon: International Agency for Research on Cancer

    Google Scholar 

  • Probst-Hensch NM, Sinha R, Longnecker MP, Witte JS, Ingles SA, Frankl HD, Lee ER, Haile RW . 1997 Meat preparation and colorectal adenomas in a large sigmoidoscopy-based case–control study in California (United States) Cancer Causes Control 8: 175–183

    CAS  Article  Google Scholar 

  • Riboli E . 1992 Nutrition and cancer: background and rationale of the European Prospective Investigation into Cancer and Nutrition (EPIC) Ann. Oncol. 3: 783–791

    CAS  Article  Google Scholar 

  • Riboli E, Kaaks R . 1997 The EPIC Project: rationale and study design Int. J. Epidemiol. 26: (Suppl 1) S6–S14

    Article  Google Scholar 

  • Rothman N, Correa-Villasenor A, Ford DP, Poirier MC, Haas R, Hansen JA, O'Toole T, Strickland PT . 1993 Contribution of occupation and diet to white blood cell polycyclic aromatic hydrocarbon–DNA adducts in Wildland firefighters Cancer Epidemiol. Biomark. Prev. 2: 341–347

    CAS  Google Scholar 

  • Schiffman MH, Felton JS . 1990 Re: ‘Fried foods and the risk of colon cancer’ Am. J. Epidemiol. 131: 376–378

    CAS  Article  Google Scholar 

  • Shirai T, Tamano S, Sano M, Masui T, Hasegawa R, Ito N . 1995 Carcinogenicity of 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP) in rats: dose–response studies Princess Takamatsu Symposia 23: 232–239

    CAS  PubMed  Google Scholar 

  • Sinha R, Rothman N . 1999 Role of well-done, grilled red meat, heterocyclic amines (HCAs) in the etiology of human cancer Cancer Lett. 143: 189–194

    CAS  Article  Google Scholar 

  • Sinha R, Kulldorff M, Curtin J, Brown CC, Alavanja MCR, Swanson CA . 1998 Fried, well-done red meat and risk of lung cancer in women (United States) Cancer Causes Control 9: 621–630

    CAS  Article  Google Scholar 

  • Sinha R, Chow WH, Kulldorff M, Denobile J, Butler J, Garcia-Closas M, Weil R, Hoover RN, Rothman N . 1999 Well-done, grilled red meat increases the risk of colorectal adenomas Cancer Res. 59: 4320–4324

    CAS  PubMed  Google Scholar 

  • Sinha R, Gustafson DR, Kulldorf M, Wen W-Q, Cerhan JR, Zheng W . 2000a 2-Amino-1-methyl-6-phenylimidazo[4,5-b]pyridine, a carcinogen in high-temperature-cooked meat, and breast cancer risk J. Natl Cancer Inst. 92: 1352–1354

    CAS  Article  Google Scholar 

  • Sinha R, Kulldorff M, Swanson CA, Curtin J, Brownson RC, Alavanja MCR . 2000b Dietary heterocyclic amines and the risk of lung cancer among Missouri women Cancer Res. 60: 3753–3757

    CAS  PubMed  Google Scholar 

  • Sinha R, Kulldorff M, Chow W-H, Denobile J, Rothman N . 2001 Dietary intake of heterocyclic amines, meat-derived mutagenic activity, and risk of colorectal adenomas Cancer Epidemiol. Biomark. Prev. 10: 559–562

    CAS  Google Scholar 

  • Skog K, Steineck G, Augustsson K, Jägerstad M . 1995 Effect of cooking temperature on the formation of heterocyclic amines in fried meat products and pan residues Carcinogenesis 16: 861–867

    CAS  Article  Google Scholar 

  • Skog KI, Johansson MAE, Jägerstad MI . 1998 Carcinogenic heterocyclic amines in model systems and cooked foods: a review on formation, occurrence and intake Food Chem. Toxicol. 36: 879–896

    CAS  Article  Google Scholar 

  • Slimani N, Deharveng G, Charrondière RU, van Kappel AL, Ocké MC, Welch A, Lagiou A, van Liere M, Agudo A, Pala V, Brandstetter B, Andren C, Stripp C, van Staveren WA, Riboli E . 1999 Structure of the standardised computeried 24-h recall interview used as reference method in the 22 centers participating in the EPIC project Comp. Meth. Progr. Biomed. 58: 251–266

    CAS  Article  Google Scholar 

  • Slimani N, Ferrari P, Ocké MC, Welch A, Boeing H, van Liere A, Pala V, Amiano P, Lagiou A, Mattisson I, Stripp C, Engset D, Charrondière R, Buzzard M, van Staveren W, Riboli E . 2000 Standardization of the 24-hour diet recall calibration method used in the European Prospective Investigation into Cancer and Nutrition (EPIC): general concepts and preliminary results Eur. J. Clin. Nutr. 54: 900–917

    CAS  Article  Google Scholar 

  • Steineck G, Hagman U, Gerhardsson de Verdier M, Norell SE . 1990 Vitamin A supplements, fried foods, fat and urothelial cancer. A case-referent study in Stockholm in 1985–87 Int. J. Cancer 45: 1006–1011

    CAS  Article  Google Scholar 

  • Tavani A, La Vecchia C, Gallus S, Lagiou P, Trichopoulos D, Levi F, Negri E . 2000 Red meat intake and cancer risk Int. J. Cancer 86: 425–429

    CAS  Article  Google Scholar 

  • Ward MH, Sinha R, Heineman EF, Rothman N, Markin R, Weisenburger DD, Correa P, Zahm SH . 1997 Risk of adenocarcinoma of the stomach and esophagus with meat cooking method and doneness preference Int. J. Cancer 71: 14–19

    CAS  Article  Google Scholar 

  • World Cancer Research Fund. 1997 Food, nutrition and the prevention of cancer: a global perspective Washington, DC: American Institute for Cancer Research

  • Zheng W, Gustafson DR, Sinha R, Cerhan JR, Moore D, Hong C-P, Anderson KE, Kushi LH, Sellers TA, Folsom AR . 1998 Well-done meat intake and the risk of breast cancer J. Natl Cancer Inst. 90: 1724–1729

    CAS  Article  Google Scholar 

  • Zheng W, Deitz AC, Campbell DR, Wen W-Q, Cerhan JR, Sellers TA, Folsom AR, Hein DW . 1999 N-Acetyltransferase 1 genetic polymorphism, cigarette smoking, well-done meat intake, and breast cancer risk Cancer Epidemol. Biomark. Prev. 8: 233–239

    CAS  Google Scholar 

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Acknowledgements

This work is part of the EPIC project supported by the ‘Europe Against Cancer’ Programme of the European Commission.

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Correspondence to S Rohrmann.

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Rohrmann, S., Linseisen, J., Becker, N. et al. Cooking of meat and fish in Europe—results from the European Prospective Investigation into Cancer and Nutrition (EPIC). Eur J Clin Nutr 56, 1216–1230 (2002). https://doi.org/10.1038/sj.ejcn.1601494

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Keywords

  • EPIC
  • meat
  • fish
  • cooking methods
  • 24 h recall

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