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Meat intake, cooking methods and doneness and risk of colorectal tumours in the Spanish multicase-control study (MCC-Spain)

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Abstract

Purpose

Although there is convincing evidence that red and processed meat intake increases the risk of colorectal cancer (CRC), the potential role of meat cooking practices has not been established yet and could partly explain the current heterogeneity of results among studies. Therefore, we aimed to investigate the association between meat consumption and cooking practices and the risk of CRC in a population-based case–control study.

Methods

A total of 1671 CRC cases and 3095 controls recruited in Spain between September 2008 and December 2013 completing a food frequency questionnaire with a meat-specific module were included in the analyses. Odds ratios (OR) and confidence intervals (CI) were estimated by logistic regression models adjusted for known confounders.

Results

Total meat intake was associated with increased risk of CRC (OR T3–T1 1.41; 95% CI 1.19–1.67; p trend < 0.001), and similar associations were found for white, red and processed/cured/organ meat. Rare-cooked meat preference was associated with low risk of CRC in red meat (ORrare vs. medium 0.66; 95% CI 0.51–0.85) and total meat (ORrare vs. medium 0.56; 95% CI 0.37–0.86) consumers, these associations being stronger in women than in men. Griddle-grilled/barbecued meat was associated with an increased CRC risk (total meat: OR 1.45; 95% CI 1.13–1.87). Stewing (OR 1.25; 95% CI 1.04–1.51) and oven-baking (OR 1.18; 95% CI 1.00–1.40) were associated with increased CRC risk of white, but not red, meat.

Conclusions

Our study supports an association of white, red, processed/cured/organ and total meat intake with an increased risk of CRC. Moreover, our study showed that cooking practices can modulate such risk.

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References

  1. Ferlay J, Soerjomataram I, Ervik M, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D, Bray F (2013) GLOBOCAN 2012 v1.0, Cancer Incidence and Mortality Worldwide: IARC CancerBase No. 11. International Agency for Research on Cancer, Lyon. Available from: http://globocan.iarc.fr (last accessed May 6th 2015)

  2. Ferlay J, Steliarova-Foucher E, Lortet-Tieulent J, Rosso S, Coebergh JWW, Comber H, Forman D, Bray F (2013) Cancer incidence and mortality patterns in Europe: estimates for 40 countries in 2012. Eur J Cancer 49:1374–1403

    Article  CAS  Google Scholar 

  3. Spanish Interactive Epidemiological Information System (ARIADNA). http://ariadna.cne.isciii.es (last accessed January 27th 2016)

  4. World Cancer Research Fund/American Institute for Cancer Research (2011) Continuous Update Project Report Summary. Food, Nutrition, Physical Activity, and the prevention of Colorectal Cancer

  5. Carr PR, Walter V, Brenner H, Hoffmeister M (2016) Meat subtypes and their association with colorectal cancer: systematic review and meta-analysis. Int J Cancer 138:293–302

    Article  CAS  Google Scholar 

  6. Abid Z, Cross AJ, Sinha R (2014) Meat, dairy, and cancer. Am J Clin Nutr 100:386s–393s

    Article  CAS  Google Scholar 

  7. Chan DS, Lau R, Aune D, Vieira R, Greenwood DC, Kampman E, Norat T (2011) Red and processed meat and colorectal cancer incidence: meta-analysis of prospective studies. PLoS ONE 6:e20456

    Article  CAS  Google Scholar 

  8. Alexander DD, Weed DL, Cushing CA, Lowe KA (2011) Meta-analysis of prospective studies of red meat consumption and colorectal cancer. Eur J Cancer Prev 20:293–307

    Article  CAS  Google Scholar 

  9. Alexander DD, Miller AJ, Cushing CA, Lowe KA (2010) Processed meat and colorectal cancer: a quantitative review of prospective epidemiologic studies. Eur J Cancer Prev 19:328–341

    Article  Google Scholar 

  10. Bouvard V, Loomis D, Guyton KZ, Grosse Y, Ghissassi FE, Benbrahim-Tallaa L, Guha N, Mattock H, Straif K, International Agency for Research on Cancer Monograph Working Group (2015) Carcinogenicity of consumption of red and processed meat. Lancet Oncol 16:1599–1600

    Article  Google Scholar 

  11. Cross AJ, Sinha R (2004) Meat-related mutagens/carcinogens in the etiology of colorectal cancer. Environ Mol Mutagen 44:44–55

    Article  CAS  Google Scholar 

  12. Bastide NM, Pierre FH, Corpet DE (2011) Heme iron from meat and risk of colorectal cancer: a meta-analysis and a review of the mechanisms involved. Cancer Prev Res 4:177–184

    Article  CAS  Google Scholar 

  13. Joosen AM, Kuhnle GG, Aspinall SM, Barrow TM, Lecommandeur E, Azqueta A, Collins AR, Bingham SA (2009) Effect of processed and red meat on endogenous nitrosation and DNA damage. Carcinogenesis 30:1402–1407

    Article  CAS  Google Scholar 

  14. Jamin EL, Riu A, Douki T, Debrauwer L, Cravedi JP, Zalko D, Audebert M (2013) Combined genotoxic effects of a polycyclic aromatic hydrocarbon (B(a)P) and an heterocyclic amine (PhIP) in relation to colorectal carcinogenesis. PLoS ONE 8:e58591

    Article  CAS  Google Scholar 

  15. Di Maso M, Talamini R, Bosetti C, Montella M, Zucchetto A, Libra M, Negri E, Levi F, La Vecchia C, Franceschi S, Serraino D, Polesel J (2013) Red meat and cancer risk in a network of case-control studies focusing on cooking practices. Ann Oncol 24(12):3107–3112

    Article  Google Scholar 

  16. Parr CL, Hjartåker A, Lund E, Veierød MB (2013) Meat intake, cooking methods and risk of proximal colon, distal colon and rectal cancer: the Norwegian Women and Cancer (NOWAC) cohort study. Int J Cancer 133:1153–1163

    Article  CAS  Google Scholar 

  17. Miller PE, Lazarus P, Lesko SM, Cross AJ, Sinha R, Laio J, Zhu J, Harper G, Muscat JE, Hartman TJ (2013) Meat-related compounds and colorectal cancer risk by anatomical subsite. Nutr Cancer 65(2):202–226

    Article  CAS  Google Scholar 

  18. Tabatabaei SM, Fritschi L, Knuiman MW, Boyle T, Iacopetta BJ, Platell C, Heyworth JS (2011) Meat consumption and cooking practices and the risk of colorectal cancer. Eur J Clin Nutr 65:668–675

    Article  CAS  Google Scholar 

  19. Navarro A, Muñoz SE, Lantieri MJ, del Pilar Diaz M, Cristaldo PE, de Fabro SP, Eynard AR (2004) Meat cooking habits and risk of colorectal cancer in Córdoba, Argentina. Nutrition 20:873–877

    Article  Google Scholar 

  20. Murtaugh MA, Ma KN, Sweeney C, Caan BJ, Slattery ML (2004) Meat consumption patterns and preparation, genetic variants of metabolic enzymes, and their association with rectal cancer in men and women. J Nutr 134:776–784

    Article  CAS  Google Scholar 

  21. Muscat JE, Wynder EL (1994) The consumption of well-done red meat and the risk of colorectal cancer. Am J Public Health 84(5):856–858

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  23. Joshi AD, Kim A, Lewinger JP, Ulrich CM, Potter JD, Cotterchio M, Le Marchand L, Stern MC (2015) Meat intake, cooking methods, dietary carcinogens, and colorectal cancer risk: findings from the Colorectal Cancer Family Registry. Cancer Med 4(6):936–952

    Article  CAS  Google Scholar 

  24. Castaño-Vinyals G, Aragonés N, Pérez-Gómez B, Martín V, Llorca J, Moreno V, Altzibar JM, Ardanaz E, de Sanjosé S, Jiménez-Moleón JJ, Tardón A, Alguacil J, Peiró R, Marcos-Gragera R, Navarro C, Pollán M, Kogevinas M, MCC-Spain Study Group (2015) Population-based multicase-control study in common tumors in Spain (MCC-Spain): rationale and study design. Gac Sanit 29(4):308–315

    Article  Google Scholar 

  25. García-Closas R, García-Closas M, Kogevinas M, Malats N, Silverman D, Serra C, Tardón A, Carrato A, Castaño-Vinyals G, Dosemeci M, Moore L, Rothman N, Sinha R (2007) Food, nutrient and heterocyclic amine intake and the risk of bladder cancer. Eur J Cancer 43:1731–1740

    Article  Google Scholar 

  26. CESNID (2008) Tablas de composición de alimentos CESNID. Taules de composició dels aliments CESNID. Ediciones de la Universitat de Barcelona, McGraw Hill-Interamericana de España SA, Barcelona

  27. Calvert C, Cade J, Barrett JH, Woodhouse A, UKWCS Steering Group (1997) Using crosscheck questions to address the problem of mis-reporting of specific food groups on Food Frequency Questionnaires. Eur J Clin Nutr 51:708–712

    Article  CAS  Google Scholar 

  28. Nothlings U, Hoffmann K, Boeing H (2002) Do cross-check questions improve food frequency questionnaire data?. IARC Scientific Publications, IARC Press, Lyon

    Google Scholar 

  29. Mendez MA, Popkin BM, Buckland G, Schroder H, Amiano P, Barricarte A, Huerta JM, Quirós JR, Sánchez MJ, González CA (2011) Alternative methods of accounting for underreporting and overreporting when measuring dietary intake-obesity relations. Am J Epidemiol 173:448–458

    Article  Google Scholar 

  30. Hosmer DW, Lemeshow S (1989) Applied logistic regression. Wiley, New York

    Google Scholar 

  31. Ollberding NJ, Wilkens LR, Henderson BE, Kolonel LN, Le Marchand L (2012) Meat consumption, heterocyclic amines and colorectal cancer risk: the Multiethnic Cohort Study. Int J Cancer 131(7):e1125–e1133

    Article  CAS  Google Scholar 

  32. Larsson SC, Wolk A (2006) Meat consumption and risk of colorectal cancer: a meta-analysis of prospective studies. Int J Cancer 119(11):2657–2664

    Article  CAS  Google Scholar 

  33. Shi Y, Yu PW, Zeng DZ (2015) Dose-response meta-analysis of poultry intake and colorectal cancer incidence and mortality. Eur J Nutr 54(2):243–250

    Article  CAS  Google Scholar 

  34. Wang J, Joshi AD, Corral R, Siegmund KD, Marchand LL, Martinez ME, Haile RW, Ahnen DJ, Sandler RS, Lance P, Stern MC (2012) Carcinogen metabolism genes, red meat and poultry intake, and colorectal cancer risk. Int J Cancer 130(8):1898–1907

    Article  CAS  Google Scholar 

  35. Guallar-Castillón P, Rodríguez-Artalejo F, Lopez-Garcia E, León-Muñoz LM, Amiano P, Ardanaz E, Arriola L, Barricarte A, Buckland G, Chirlaque MD, Dorronsoro M, Huerta JM, Larrañaga N, Marin P, Martínez C, Molina E, Navarro C, Quirós JR, Rodríguez L, Sanchez MJ, González CA, Moreno-Iribas C (2012) Consumption of fried foods and risk of coronary heart disease: Spanish cohort of the European Prospective Investigation into Cancer and Nutrition study. BMJ 344:e363

    Article  Google Scholar 

  36. Bastide NM, Chenni F, Audebert M, Santarelli RL, Taché S, Naud N, Baradat M, Jouanin I, Surya R, Hobbs DA, Kuhnle GG, Raymond-Letron I, Gueraud F, Corpet DE, Pierre FH (2015) A central role for heme iron in colon carcinogenesis associated with red meat intake. Cancer Res 75(5):870–879

    Article  CAS  Google Scholar 

  37. Humphreys KJ, Conlon MA, Young GP, Topping DL, Hu Y, Winter JM, Bird AR, Cobiac L, Kennedy NA, Michael MZ, Le Leu RK (2014) Dietary manipulation of oncogenic microRNA expression in human rectal mucosa: a randomized trial. Cancer Prev Res 7(8):786–795

    Article  CAS  Google Scholar 

  38. Zur Hausen H (2012) Red meat consumption and cancer: reasons to suspect involvement of bovine infectious factors in colorectal cancer. Int J Cancer 130:2475–2483

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The study was partially funded by the “Accion Transversal del Cancer”, approved on the Spanish Ministry Council on 11 October 2007, by the Instituto de Salud Carlos III-FEDER (PI08/1770, PI08/0533, PI08/1359, PS09/00773, PS09/01286, PS09/01903, PS09/02078, PS09/01662, PI11/01403, PI11/01889, PI11/00226, PI11/01810, PI11/02213, PI12/00488, PI12/00265, PI12/01270, PI12/00715, PI12/00150), by the Fundación Marqués de Valdecilla (API 10/09), by the ICGC International Cancer Genome Consortium CLL, by the Junta de Castilla y León (LE22A10-2), by the Consejería de Salud of the Junta de Andalucía (PI-0571), by the Conselleria de Sanitat of the Generalitat Valenciana (AP 061/10), by the Recercaixa (2010ACUP 00310), by the Regional Government of the Basque Country, by European Commission grants FOOD-CT-2006-036224-HIWATE, by the Spanish Association Against Cancer (AECC) Scientific Foundation, by the Catalan Government DURSI grant 2009SGR1489. Jordi de Batlle acknowledges the support of the European Commission FP7 Marie Curie Actions-People, Cofunding of regional, national, and international programs (COFUND).

Author information

Authors and Affiliations

  1. International Agency for Research on Cancer (IARC), Lyon, France

    Jordi de Batlle

  2. ISGlobal, Centre for Research in Environmental Epidemiology (CREAL), Barcelona, Spain

    Esther Gracia-Lavedan, Dora Romaguera, Gemma Castaño-Vinyals & Manolis Kogevinas

  3. CIBER Epidemiología y Salud Pública (CIBERESP), Madrid, Spain

    Esther Gracia-Lavedan, Gemma Castaño-Vinyals, Vicente Martín, Núria Aragonés, Inés Gómez-Acebo, Rocío Olmedo-Requena, José Juan Jimenez-Moleon, Marcela Guevara, Guillermo Fernandez-Tardon, Victor Moreno, Elena Boldo, Beatriz Pérez-Gómez, Jesús Castilla, Trinidad Dierssen, Jone M. Altzibar, Manolis Kogevinas, Marina Pollán & Pilar Amiano

  4. Universitat Pompeu Fabra (UPF), Barcelona, Spain

    Esther Gracia-Lavedan, Gemma Castaño-Vinyals & Manolis Kogevinas

  5. Instituto de Investigación Sanitaria de Palma (IdISPa), Hospital Universitario Son Espases, Unidad de Investigación, I-1. Carretera de Valldemossa, 79, 07120, Palma de Mallorca, Spain

    Dora Romaguera

  6. CIBER Fisiopatología de la Obesidad y la Nutrición (CIBER-OBN), Madrid, Spain

    Dora Romaguera

  7. Department of Nutrition, Gillings School of Global Public Health, University of North Carolina, Chapel Hill, NC, USA

    Michelle Mendez

  8. Carolina Population Center and Lineberger Cancer Center, University of North Carolina, Chapel Hill, NC, USA

    Michelle Mendez

  9. IMIM (Hospital del Mar Medical Research Institute), Barcelona, Spain

    Gemma Castaño-Vinyals & Manolis Kogevinas

  10. Grupo de Investigación en Interacciones gen-ambiente y salud, Universidad de León, León, Spain

    Vicente Martín, Tania Fernández-Villa & Juan Pablo Barrio

  11. Instituto de Salud Carlos III, Madrid, Spain

    Núria Aragonés, Elena Boldo, Beatriz Pérez-Gómez & Marina Pollán

  12. Cancer Epidemiology Unit, National Center for Epidemiology, Instituto de Salud Carlos III, Madrid, Spain

    Núria Aragonés, Elena Boldo, Beatriz Pérez-Gómez & Marina Pollán

  13. Cancer Epidemiology Research Group, Oncology and Hematology Area, IIS Puerta de Hierro (IDIPHIM), Majadahonda, Madrid, Spain

    Núria Aragonés, Elena Boldo, Beatriz Pérez-Gómez & Marina Pollán

  14. Universidad de Cantabria – IDIVAL, Santander, Spain

    Inés Gómez-Acebo & Trinidad Dierssen

  15. Department of Preventive Medicine and Public Health, University of Granada, Granada, Spain

    Rocío Olmedo-Requena & José Juan Jimenez-Moleon

  16. Instituto de Investigación Biosanitaria de Granada (ibs.GRANADA), Complejo Hospitales Universitarios de Granada, Universidad de Granada, Granada, Spain

    Rocío Olmedo-Requena & José Juan Jimenez-Moleon

  17. Instituto de Salud Pública de Navarra, IdiSNA, Pamplona, Spain

    Marcela Guevara & Jesús Castilla

  18. Public Health Division of Gipuzkoa, BioDonostia Research Institute, Government of the Basque Country, San Sebastian, Spain

    Mikel Azpiri, Jone M. Altzibar & Pilar Amiano

  19. Centro de Salud Pública de Dénia, Consellería de Sanidad Universal y Salud Pública, Generalitat Valenciana, Fundación para el Fomento de la Investigación Sanitaria y Biomédica de la Comunidad Valenciana (FISABIO), València, Spain

    Cristóbal Llorens-Ivorra

  20. IUOPA, Preventive Medicine Department, University of Oviedo, Oviedo, Spain

    Guillermo Fernandez-Tardon

  21. Centro de Investigación en Salud y Medio Ambiente (CYSMA), Universidad de Huelva, Huelva, Spain

    Jose Andrés Lorca

  22. Department of Epidemiology, Murcia Regional Health Council, IMIB-Arrixaca, Murcia, Spain

    José María Huerta

  23. IDIBELL-Catalan Institute of Oncology, L’Hospitalet de Llobregat, Spain

    Victor Moreno

  24. Department of Clinical Sciences, Faculty of Medicine, University of Barcelona, Campus de Bellvitge, L’Hospitalet del Llobregat, Barcelona, Spain

    Victor Moreno

  25. Department of Gastroenterology, Hospital del Mar, IMIM (Hospital del Mar Medical Research Institute), Pompeu Fabra University, Barcelona, Spain

    Montserrat Andreu

  26. Gastroenterology Department, Hospital Clínic, IDIBAPS, CIBERehd, University of Barcelona, Barcelona, Catalonia, Spain

    Antoni Castells

Authors
  1. Jordi de Batlle
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  2. Esther Gracia-Lavedan
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  3. Dora Romaguera
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  13. Cristóbal Llorens-Ivorra
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  17. Victor Moreno
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  18. Elena Boldo
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  25. Trinidad Dierssen
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  26. Jone M. Altzibar
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  27. Manolis Kogevinas
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  28. Marina Pollán
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  29. Pilar Amiano
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Corresponding author

Correspondence to Dora Romaguera.

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The authors declare that they have no conflict of interest.

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All participants signed an informed consent prior to their inclusion in the study. The study has been approved by the ethics committees of all participating centres and has therefore been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments.

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de Batlle, J., Gracia-Lavedan, E., Romaguera, D. et al. Meat intake, cooking methods and doneness and risk of colorectal tumours in the Spanish multicase-control study (MCC-Spain). Eur J Nutr 57, 643–653 (2018). https://doi.org/10.1007/s00394-016-1350-6

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