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Open Access 01-12-2013 | Research article

Meat consumption and mortality - results from the European Prospective Investigation into Cancer and Nutrition

Authors: Sabine Rohrmann, Kim Overvad, H Bas Bueno-de-Mesquita, Marianne U Jakobsen, Rikke Egeberg, Anne Tjønneland, Laura Nailler, Marie-Christine Boutron-Ruault, Françoise Clavel-Chapelon, Vittorio Krogh, Domenico Palli, Salvatore Panico, Rosario Tumino, Fulvio Ricceri, Manuela M Bergmann, Heiner Boeing, Kuanrong Li, Rudolf Kaaks, Kay-Tee Khaw, Nicholas J Wareham, Francesca L Crowe, Timothy J Key, Androniki Naska, Antonia Trichopoulou, Dimitirios Trichopoulos, Max Leenders, Petra HM Peeters, Dagrun Engeset, Christine L Parr, Guri Skeie, Paula Jakszyn, María-José Sánchez, José M Huerta, M Luisa Redondo, Aurelio Barricarte, Pilar Amiano, Isabel Drake, Emily Sonestedt, Göran Hallmans, Ingegerd Johansson, Veronika Fedirko, Isabelle Romieux, Pietro Ferrari, Teresa Norat, Anne C Vergnaud, Elio Riboli, Jakob Linseisen

Published in: BMC Medicine | Issue 1/2013

Abstract

Background

Recently, some US cohorts have shown a moderate association between red and processed meat consumption and mortality supporting the results of previous studies among vegetarians. The aim of this study was to examine the association of red meat, processed meat, and poultry consumption with the risk of early death in the European Prospective Investigation into Cancer and Nutrition (EPIC).

Methods

Included in the analysis were 448,568 men and women without prevalent cancer, stroke, or myocardial infarction, and with complete information on diet, smoking, physical activity and body mass index, who were between 35 and 69 years old at baseline. Cox proportional hazards regression was used to examine the association of meat consumption with all-cause and cause-specific mortality.

Results

As of June 2009, 26,344 deaths were observed. After multivariate adjustment, a high consumption of red meat was related to higher all-cause mortality (hazard ratio (HR) = 1.14, 95% confidence interval (CI) 1.01 to 1.28, 160+ versus 10 to 19.9 g/day), and the association was stronger for processed meat (HR = 1.44, 95% CI 1.24 to 1.66, 160+ versus 10 to 19.9 g/day). After correction for measurement error, higher all-cause mortality remained significant only for processed meat (HR = 1.18, 95% CI 1.11 to 1.25, per 50 g/d). We estimated that 3.3% (95% CI 1.5% to 5.0%) of deaths could be prevented if all participants had a processed meat consumption of less than 20 g/day. Significant associations with processed meat intake were observed for cardiovascular diseases, cancer, and 'other causes of death'. The consumption of poultry was not related to all-cause mortality.

Conclusions

The results of our analysis support a moderate positive association between processed meat consumption and mortality, in particular due to cardiovascular diseases, but also to cancer.

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American Institute for Cancer Research/World Cancer Research Fund: Food, Nutrition, Physical Activity, and the Prevention of Cancer: a Global Perspective. 2007, Washington, DC: AICR

Mozaffarian D, Micha R, Wallace S: Effects on coronary heart disease of increasing polyunsaturated fat in place of saturated fat: a systematic review and meta-analysis of randomized controlled trials. PLoS Med. 2010, 7: e1000252-10.1371/journal.pmed.1000252.CrossRefPubMedPubMedCentral

Bingham SA, Hughes R, Cross AJ: Effect of white versus red meat on endogenous N-nitrosation in the human colon and further evidence of a dose response. J Nutr. 2002, 132: 3522S-3525S.PubMed

Joosen AMCP, Kuhnle GGC, Aspinall SM, Barrow TM, Lecommandeur E, Azqueta A, Collins AR, Bingham SA: Effect of processed and red meat on endogenous nitrosation and DNA damage. Carcinogenesis. 2009, 30: 1402-1407. 10.1093/carcin/bgp130.CrossRefPubMedPubMedCentral

Hebels DG, Sveje KM, de Kok MC, van Herwijnen MH, Kuhnle GG, Engels LG, Vleugels-Simon CB, Mares WG, Pierik M, Masclee AA, Kleinjans JC, de Kok TM: N-nitroso compound exposure-associated transcriptomic profiles are indicative of an increased risk for colorectal cancer. Cancer Lett. 2011, 309: 1-10. 10.1016/j.canlet.2011.05.007.CrossRefPubMed

Pan A, Sun Q, Bernstein AM, Schulze MB, Manson JE, Stampfer MJ, Willett WC, Hu FB: Red meat consumption and mortality: results from 2 prospective cohort studies. Arch Intern Med. 2012, 172: 555-563. 10.1001/archinternmed.2011.2287.CrossRefPubMedPubMedCentral

Nagao M, Iso H, Yamagishi K, Date C, Tamakoshi A: Meat consumption in relation to mortality from cardiovascular disease among Japanese men and women. Eur J Clin Nutr. 2012, 66: 687-693. 10.1038/ejcn.2012.6.CrossRefPubMed

Sinha R, Cross AJ, Graubard BI, Leitzmann MF, Schatzkin A: Meat intake and mortality: a prospective study of over half a million people. Arch Intern Med. 2009, 169: 562-571. 10.1001/archinternmed.2009.6.CrossRefPubMedPubMedCentral

Key TJ, Appleby PN, Spencer EA, Travis RC, Roddam AW, Allen NE: Mortality in British vegetarians: results from the European Prospective Investigation into Cancer and Nutrition (EPIC-Oxford). Am J Clin Nutr. 2009, 89: 1613S-1619S. 10.3945/ajcn.2009.26736L.CrossRefPubMed

10.

Trichopoulou A, Bamia C, Trichopoulos D: Anatomy of health effects of Mediterranean diet: Greek EPIC prospective cohort study. BMJ. 2009, 338: b2337-10.1136/bmj.b2337.CrossRefPubMedPubMedCentral

11.

Chang-Claude J, Hermann S, Eilber U, Steindorf K: Lifestyle determinants and mortality in German vegetarians and health-conscious persons: results of a 21-year follow-up. Cancer Epidemiol Biomarkers Prev. 2005, 14: 963-968. 10.1158/1055-9965.EPI-04-0696.CrossRefPubMed

12.

Kelemen LE, Kushi LH, Jacobs DR, Cerhan JR: Associations of dietary protein with disease and mortality in a prospective study of postmenopausal women. Am J Epidemiol. 2005, 161: 239-249. 10.1093/aje/kwi038.CrossRefPubMed

13.

Appleby PN, Key TJ, Thorogood M, Burr ML, Mann J: Mortality in British vegetarians. Public Health Nutr. 2002, 5: 29-36.PubMed

14.

Fortes C, Forastiere F, Farchi S, Rapiti E, Pastori G, Perucci CA: Diet and overall survival in a cohort of very elderly people. Epidemiology. 2000, 11: 440-445. 10.1097/00001648-200007000-00013.CrossRefPubMed

15.

Whiteman D, Muir J, Jones L, Murphy M, Key T: Dietary questions as determinants of mortality: the OXCHECK experience. Public Health Nutr. 1999, 2: 477-487.CrossRefPubMed

16.

Fraser GE: Associations between diet and cancer, ischemic heart disease, and all-cause mortality in non-Hispanic white California Seventh-day Adventists. Am J Clin Nutr. 1999, 70: 532S-538S.PubMed

17.

Kahn HA, Phillips RL, Snowdon DA, Choi W: Association between reported diet and all-cause mortality. Twenty-one-year follow-up on 27,530 adult Seventh-Day Adventists. Am J Epidemiol. 1984, 119: 775-787.PubMed

18.

Riboli E, Hunt KJ, Slimani N, Ferrari P, Norat T, Fahey M, Charrondière UR, Hémon B, Casagrande C, Vignat J, Overvad K, Tjønneland A, Clavel-Chapelon F, Thiébaut A, Wahrendorf J, Boeing H, Trichopoulos D, Trichopoulou A, Vineis P, Palli D, Bueno-De-Mesquita HB, Peeters PH, Lund E, Engeset D, González CA, Barricarte A, Berglund G, Hallmans G, Day NE, Key TJ, Kaaks R, Saracci R: European Prospective Investigation into Cancer and Nutrition (EPIC): study populations and data collection. Public Health Nutr. 2002, 5: 1113-1124. 10.1079/PHN2002394.CrossRefPubMed

19.

Haftenberger M, Lahmann PH, Panico S, Gonzalez CA, Seidell JC, Boeing H, Giurdanella MC, Krogh V, Bueno-de-Mesquita HB, Peeters PH, Skeie G, Hjartåker A, Rodriguez M, Quirós JR, Berglund G, Janlert U, Khaw KT, Spencer EA, Overvad K, Tjønneland A, Clavel-Chapelon F, Tehard B, Miller AB, Klipstein-Grobusch K, Benetou V, Kiriazi G, Riboli E, Slimani N: Overweight, obesity and fat distribution in 50- to 64-year-old participants in the European Prospective Investigation into Cancer and Nutrition (EPIC). Public Health Nutr. 2002, 5: 1147-1162. 10.1079/PHN2002396.CrossRefPubMed

20.

Heinzl H, Kaider A: Gaining more flexibility in Cox proportional hazards regression models with cubic spline functions. Comput Methods Programs Biomed. 1997, 54: 201-208. 10.1016/S0169-2607(97)00043-6.CrossRefPubMed

21.

Steenland K, Deddens JA: A practical guide to dose-response analyses and risk assessment in occupational epidemiology. Epidemiology. 2004, 15: 63-70. 10.1097/01.ede.0000100287.45004.e7.CrossRefPubMed

22.

Linseisen J, Rohrmann S, Miller AB, Bueno-de-Mesquita HB, Büchner FL, Vineis P, Agudo A, Gram IT, Janson L, Krogh V, Overvad K, Rasmuson T, Schulz M, Pischon T, Kaaks R, Nieters A, Allen NE, Key TJ, Bingham S, Khaw KT, Amiano P, Barricarte A, Martinez C, Navarro C, Quirós R, Clavel-Chapelon F, Boutron-Ruault MC, Touvier M, Peeters PH, Berglund G, et al: Fruit and vegetable consumption and lung cancer risk: updated information from the European Prospective Investigation into Cancer and Nutrition (EPIC). Int J Cancer. 2007, 121: 1103-1114. 10.1002/ijc.22807.CrossRefPubMed

23.

Wareham NJ, Jakes RW, Rennie KL, Schuit J, Mitchell J, Hennings S, Day NE: Validity and repeatability of a simple index derived from the short physical activity questionnaire used in the European Prospective Investigation into Cancer and Nutrition (EPIC) study. Public Health Nutr. 2003, 6: 407-413.CrossRefPubMed

24.

Slimani N, Kaaks R, Ferrari P, Casagrande C, Clavel-Chapelon F, Lotze G, Kroke A, Trichopoulos D, Trichopoulou A, Lauria C, Bellegotti M, Ocké MC, Peeters PH, Engeset D, Lund E, Agudo A, Larrañaga N, Mattisson I, Andren C, Johansson I, Davey G, Welch AA, Overvad K, Tjønneland A, Van Staveren WA, Saracci R, Riboli E: European Prospective Investigation into Cancer and Nutrition (EPIC) calibration study: rationale, design and population characteristics. Public Health Nutr. 2002, 5: 1125-1145. 10.1079/PHN2002395.CrossRefPubMed

25.

Slimani N, Ferrari P, Ocké M, Welch A, Boeing H, Liere M, Pala V, Amiano P, Lagiou A, Mattisson I, Stripp C, Engeset D, Charrondière R, Buzzard M, Staveren W, Riboli E: 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. 2000, 54: 900-917. 10.1038/sj.ejcn.1601107.CrossRefPubMed

26.

Ferrari P, Day NE, Boshuizen HC, Roddam A, Hoffmann K, Thiébaut A, Pera G, Overvad K, Lund E, Trichopoulou A, Tumino R, Gullberg B, Norat T, Slimani N, Kaaks R, Riboli E: The evaluation of the diet/disease relation in the EPIC study: considerations for the calibration and the disease models. Int J Epidemiol. 2008, 37: 368-378. 10.1093/ije/dym242.CrossRefPubMed

27.

Rosthoj S, Andersen PK, Abildstrom SZ: SAS macros for estimation of the cumulative incidence functions based on a Cox regression model for competing risks survival data. Comput Methods Programs Biomed. 2004, 74: 69-75. 10.1016/S0169-2607(03)00069-5.CrossRefPubMed

28.

Spiegelman D, Hertzmark E, Wand HC: Point and interval estimates of partial population attributable risks in cohort studies: examples and software. Cancer Causes Control. 2007, 18: 571-579. 10.1007/s10552-006-0090-y.CrossRefPubMed

29.

Norat T, Bingham S, Ferrari P, Slimani N, Jenab M, Mazuir M, Overvad K, Olsen A, Tjønneland A, Clavel F, Boutron-Ruault MC, Kesse E, Boeing H, Bergmann MM, Nieters A, Linseisen J, Trichopoulou A, Trichopoulos D, Tountas Y, Berrino F, Palli D, Panico S, Tumino R, Vineis P, Bueno-de-Mesquita HB, Peeters PH, Engeset D, Lund E, Skeie G, Ardanaz E, et al: Meat, fish, and colorectal cancer risk: the European Prospective Investigation into Cancer and Nutrition. J Natl Cancer Inst. 2005, 97: 906-916. 10.1093/jnci/dji164.CrossRefPubMedPubMedCentral

30.

González CA, Jakszyn P, Pera G, Agudo A, Bingham S, Palli D, Ferrari P, Boeing H, del Giudice G, Plebani M, Carneiro F, Nesi G, Berrino F, Sacerdote C, Tumino R, Panico S, Berglund G, Simán H, Nyrén O, Hallmans G, Martinez C, Dorronsoro M, Barricarte A, Navarro C, Quirós JR, Allen N, Key TJ, Day NE, Linseisen J, Nagel G, et al: Meat intake and risk of stomach and esophageal adenocarcinoma within the European Prospective Investigation Into Cancer and Nutrition (EPIC). J Natl Cancer Inst. 2006, 98: 345-354. 10.1093/jnci/djj071.CrossRefPubMed

31.

Kaaks R, Slimani N, Riboli E: Pilot phase studies on the accuracy of dietary intake measurements in the EPIC project: overall evaluation of results. European Prospective Investigation into Cancer and Nutrition. Int J Epidemiol. 1997, 26: S26-36. 10.1093/ije/26.suppl_1.S26.CrossRefPubMed

32.

Ferrari P, Kaaks R, Fahey MT, Slimani N, Day NE, Pera G, Boshuizen HC, Roddam A, Boeing H, Nagel G, Thiebaut A, Orfanos P, Krogh V, Braaten T, Riboli E, European Prospective Investigation into Cancer and Nutrition study: Within- and between-cohort variation in measured macronutrient intakes, taking account of measurement errors, in the European Prospective Investigation into Cancer and Nutrition Study. Am J Epidemiol. 2004, 160: 814-822. 10.1093/aje/kwh280.CrossRefPubMed

33.

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: S15-25. 10.1093/ije/26.suppl_1.S15.CrossRefPubMed

34.

Day N, McKeown N, Wong M, Welch A, Bingham S: 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. 2001, 30: 309-317. 10.1093/ije/30.2.309.CrossRefPubMed

35.

Kipnis V, Midthune D, Freedman LS, Bingham S, Schatzkin A, Subar A, Carroll RJ: Empirical evidence of correlated biases in dietary assessment instruments and its implications. Am J Epidemiol. 2001, 153: 394-403. 10.1093/aje/153.4.394.CrossRefPubMed

36.

Linseisen J, Kesse E, Slimani N, Bueno-De-Mesquita HB, Ocké MC, Skeie G, Kumle M, Dorronsoro Iraeta M, Morote Gómez P, Janzon L, Stattin P, Welch AA, Spencer EA, Overvad K, Tjønneland A, Clavel-Chapelon F, Miller AB, Klipstein-Grobusch K, Lagiou P, Kalapothaki V, Masala G, Giurdanella MC, Norat T, Riboli E: Meat consumption in the European Prospective Investigation into Cancer and Nutrition (EPIC) cohorts: results from 24-hour dietary recalls. Public Health Nutr. 2002, 5: 1243-1258. 10.1079/PHN2002402.CrossRefPubMed

37.

Lloyd-Jones DM, Martin DO, Larson MG, Levy D: Accuracy of death certificates for coding coronary heart disease as the cause of death. Ann Intern Med. 1998, 129: 1020-1026.CrossRefPubMed

38.

Modelmog D, Rahlenbeck S, Trichopoulos D: Accuracy of death certificates: a population-based, complete-coverage, one-year autopsy study in East Germany. Cancer Causes Control. 1992, 3: 541-546. 10.1007/BF00052751.CrossRefPubMed

39.

Smith Sehdev AE, Hutchins GM: Problems with proper completion and accuracy of the cause-of-death statement. Arch Intern Med. 2001, 161: 277-284. 10.1001/archinte.161.2.277.CrossRefPubMed

The pre-publication history for this paper can be accessed here:http://www.biomedcentral.com/1741-7015/11/63/prepub

Title: Meat consumption and mortality - results from the European Prospective Investigation into Cancer and Nutrition
Authors: Sabine Rohrmann
Kim Overvad
H Bas Bueno-de-Mesquita
Marianne U Jakobsen
Rikke Egeberg
Anne Tjønneland
Laura Nailler
Marie-Christine Boutron-Ruault
Françoise Clavel-Chapelon
Vittorio Krogh
Domenico Palli
Salvatore Panico
Rosario Tumino
Fulvio Ricceri
Manuela M Bergmann
Heiner Boeing
Kuanrong Li
Rudolf Kaaks
Kay-Tee Khaw
Nicholas J Wareham
Francesca L Crowe
Timothy J Key
Androniki Naska
Antonia Trichopoulou
Dimitirios Trichopoulos
Max Leenders
Petra HM Peeters
Dagrun Engeset
Christine L Parr
Guri Skeie
Paula Jakszyn
María-José Sánchez
José M Huerta
M Luisa Redondo
Aurelio Barricarte
Pilar Amiano
Isabel Drake
Emily Sonestedt
Göran Hallmans
Ingegerd Johansson
Veronika Fedirko
Isabelle Romieux
Pietro Ferrari
Teresa Norat
Anne C Vergnaud
Elio Riboli
Jakob Linseisen
Publication date: 01-12-2013
Publisher: BioMed Central
Published in: BMC Medicine / Issue 1/2013
Electronic ISSN: 1741-7015
DOI: https://doi.org/10.1186/1741-7015-11-63

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Meat consumption and mortality - results from the European Prospective Investigation into Cancer and Nutrition

Abstract

Background

Methods

Results

Conclusions

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

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