Epidemiology

Processed meat and risk of selected digestive tract and laryngeal cancers

Abstract

Background/objectives

To assess the association between processed meat and the risk of selected digestive tract and laryngeal cancers.

Subjects/methods

We conducted a series of case-control studies between 1985 and 2007 in Italy. The studies included a total of 1475 cases of cancer of the oral cavity and pharynx, 1077 of the larynx, 716 of the esophagus, 999 of the stomach, 684 of the liver, 159 of the biliary tract, 688 of the pancreas, and a total of 9720 controls. Odds ratios (ORs), and the corresponding 95% confidence intervals (CIs), were estimated by unconditional logistic regression models, including terms for socio-demographic factors, tobacco smoking, and alcohol intake.

Results

Compared to the lowest tertile of processed meat consumption, the ORs for subjects in the highest one were 1.18 (95% CI 0.98–1.43) for oral cavity and pharyngeal, 1.51 (95% CI 1.18–1.91) for esophageal, 1.19 (95% CI 0.96–1.47) for laryngeal, 0.98 (95% CI 0.81–1.18) for stomach, 0.85 (95% CI 0.51–1.40) for biliary tract, 1.20 (95% CI 0.94–1.54) for liver, and 1.46 (95% CI 1.15–1.85) for pancreatic cancers.

Conclusions

Our findings support the hypothesis that high processed meat consumption increases esophageal and pancreatic cancers risk. Residual confounding by socio-demographic factors, tobacco smoking, and alcohol intake may, partly or largely, account for these associations. We found no overall association with other digestive tract and laryngeal cancers.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Fig. 1

References

  1. 1.

    Bouvard V, Loomis D, Guyton KZ, Grosse Y, Ghissassi FE, Benbrahim-Tallaa L, et al. Carcinogenicity of consumption of red and processed meat. Lancet Oncol. 2015;16:1599–1600.

    Article  Google Scholar 

  2. 2.

    Lippi G, Mattiuzzi C, Cervellin G. Meat consumption and cancer risk: a critical review of published meta-analyses. Crit Rev Oncol Hematol. 2016;97:1–14.

    Article  Google Scholar 

  3. 3.

    Elmadfa I, Meyer A, Nowak V, Hasenegger V, Putz P, Verstraeten R, et al. European Nutrition and Health Report 2009. Forum Nutr. 2009;62:1–405.

    CAS  Article  Google Scholar 

  4. 4.

    Delgado CL. Rising consumption of meat and milk in developing countries has created a new food revolution. J Nutr. 2003;133 11Suppl 2:3907S–10S.

  5. 5.

    World Health Organization. Global and regional food consumption patterns and trends: availability and changes in consumption of animal products. 2016. http://www.who.int/nutrition/topics/3_foodconsumption/en/index4.html. Accessed May 2016.

  6. 6.

    Zhu H, Yang X, Zhang C, Zhu C, Tao G, Zhao L, et al. Red and processed meat intake is associated with higher gastric cancer risk: a meta-analysis of epidemiological observational studies. PLoS ONE. 2013;8:e70955.

    CAS  Article  Google Scholar 

  7. 7.

    Larsson SC, Wolk A. Red and processed meat consumption and risk of pancreatic cancer: meta-analysis of prospective studies. Br J Cancer. 2012;106:603–7.

    CAS  Article  Google Scholar 

  8. 8.

    Cross AJ, Leitzmann MF, Gail MH, Hollenbeck AR, Schatzkin A, Sinha R. A prospective study of red and processed meat intake in relation to cancer risk. PLoS Med. 2007;4:e325.

    Article  Google Scholar 

  9. 9.

    Gonzalez CA, Riboli E. Diet and cancer prevention: Contributions from the European Prospective Investigation into Cancer and Nutrition (EPIC) study. Eur J Cancer. 2010;46:2555–62.

    Article  Google Scholar 

  10. 10.

    Bravi F, Bosetti C, Filomeno M, Levi F, Garavello W, Galimberti S, et al. Foods, nutrients and the risk of oral and pharyngeal cancer. Br J Cancer. 2013;109:2904–10.

    CAS  Article  Google Scholar 

  11. 11.

    Tavani A, La Vecchia C, Gallus S, Lagiou P, Trichopoulos D, Levi F, et al. Red meat intake and cancer risk: a study in Italy. Int J Cancer. 2000;86:425–8.

    CAS  Article  Google Scholar 

  12. 12.

    Bosetti C, La Vecchia C, Talamini R, Negri E, Levi F, Dal Maso L, et al. Food groups and laryngeal cancer risk: a case-control study from Italy and Switzerland. Int J Cancer. 2002;100:355–60.

    CAS  Article  Google Scholar 

  13. 13.

    Bosetti C, La Vecchia C, Talamini R, Simonato L, Zambon P, Negri E, et al. Food groups and risk of squamous cell esophageal cancer in northern Italy. Int J Cancer. 2000;87:289–94.

    CAS  Article  Google Scholar 

  14. 14.

    Tavani A, Negri E, Franceschi S, La Vecchia C. Risk factors for esophageal cancer in lifelong nonsmokers. Cancer Epidemiol Biomark Prev. 1994;3:387–92.

    CAS  Google Scholar 

  15. 15.

    Lucenteforte E, Scita V, Bosetti C, Bertuccio P, Negri E, La Vecchia C. Food groups and alcoholic beverages and the risk of stomach cancer: a case-control study in Italy. Nutr Cancer. 2008;60:577–84.

    Article  Google Scholar 

  16. 16.

    La Vecchia C, Negri E, Decarli A, D’Avanzo B, Franceschi S. A case-control study of diet and gastric cancer in northern Italy. Int J Cancer. 1987;40:484–9.

    Article  Google Scholar 

  17. 17.

    Talamini R, Polesel J, Montella M, Dal Maso L, Crispo A, Tommasi LG, et al. Food groups and risk of hepatocellular carcinoma: a multicenter case-control study in Italy. Int J Cancer. 2006;119:2916–21.

    CAS  Article  Google Scholar 

  18. 18.

    Rosato V, Bosetti C, Dal Maso L, Montella M, Serraino D, Negri E, et al. Medical conditions, family history of cancer, and the risk of biliary tract cancers. Tumori. 2016;2016:252–7.

    Article  Google Scholar 

  19. 19.

    Polesel J, Talamini R, Negri E, Bosetti C, Boz G, Lucenteforte E, et al. Dietary habits and risk of pancreatic cancer: an Italian case-control study. Cancer Causes Control. 2010;21:493–500.

    Article  Google Scholar 

  20. 20.

    Soler M, Chatenoud L, La Vecchia C, Franceschi S, Negri E. Diet, alcohol, coffee and pancreatic cancer: final results from an Italian study. Eur J Cancer Prev. 1998;7:455–60.

    CAS  Article  Google Scholar 

  21. 21.

    D’Avanzo B, La Vecchia C, Katsouyanni K, Negri E, Trichopoulos D. An assessment, and reproducibility of food frequency data provided by hospital controls. Eur J Cancer Prev. 1997;6:288–93.

    Article  Google Scholar 

  22. 22.

    Franceschi S, Barbone F, Negri E, Decarli A, Ferraroni M, Filiberti R, et al. Reproducibility of an Italian food frequency questionnaire for cancer studies. Results for specific nutrients. Ann Epidemiol. 1995;5:69–75.

    CAS  Article  Google Scholar 

  23. 23.

    Franceschi S, Negri E, Salvini S, Decarli A, Ferraroni M, Filiberti R, et al. Reproducibility of an Italian food frequency questionnaire for cancer studies: results for specific food items. Eur J Cancer. 1993;29A:2298–305.

    CAS  Article  Google Scholar 

  24. 24.

    Decarli A, Franceschi S, Ferraroni M, Gnagnarella P, Parpinel MT, La Vecchia C, et al. Validation of a food-frequency questionnaire to assess dietary intakes in cancer studies in Italy. Results for specific nutrients. Ann Epidemiol. 1996;6:110–8.

    CAS  Article  Google Scholar 

  25. 25.

    Ferraroni M, Decarli A, Franceschi S, La Vecchia C, Enard L, Negri E, et al. Validity and reproducibility of alcohol consumption in Italy. Int J Epidemiol. 1996;25:775–82.

    CAS  Article  Google Scholar 

  26. 26.

    Salvini S. Banca dati di composizione degli alimenti per studi epidemiologici in Italia. Italia: Istituito Europeo diOncologia; 1998.

    Google Scholar 

  27. 27.

    Breslow NE, Day NE. Statistical methods in cancer research. Vol. I. In: The analysis of case-control studies. IARC Sci Publ No. 32. Lyon, France: IARC; 1980.

    Google Scholar 

  28. 28.

    Xu J, Yang XX, Wu YG, Li XY, Bai B. Meat consumption and risk of oral cavity and oropharynx cancer: a meta-analysis of observational studies. PLoS ONE. 2014;9:e95048.

    Article  Google Scholar 

  29. 29.

    Steffen A, Bergmann MM, Sanchez MJ, Chirlaque MD, Jakszyn P, Amiano P, et al. Meat and heme iron intake and risk of squamous cell carcinoma of the upper aero-digestive tract in the European Prospective Investigation into Cancer and Nutrition (EPIC). Cancer Epidemiol Biomark Prev. 2012;21:2138–48.

    CAS  Article  Google Scholar 

  30. 30.

    Chuang SC, Jenab M, Heck JE, Bosetti C, Talamini R, Matsuo K, et al. Diet and the risk of head and neck cancer: a pooled analysis in the INHANCE consortium. Cancer Causes Control. 2012;23:69–88.

    Article  Google Scholar 

  31. 31.

    Levi F, Pasche C, Lucchini F, Bosetti C, La Vecchia C. Processed meat and the risk of selected digestive tract and laryngeal neoplasms in Switzerland. Ann Oncol. 2004;15:346–9.

    CAS  Article  Google Scholar 

  32. 32.

    De Stefani E, Boffetta P, Ronco AL, Deneo-Pellegrini H, Correa P, Acosta G, et al. Processed meat consumption and risk of cancer: a multisite case-control study in Uruguay. Br J Cancer. 2012;107:1584–8.

    Article  Google Scholar 

  33. 33.

    Oreggia F, De Stefani E, Boffetta P, Brennan P, Deneo-Pellegrini H, Ronco AL. Meat, fat and risk of laryngeal cancer: a case-control study in Uruguay. Oral Oncol. 2001;37:141–5.

    CAS  Article  Google Scholar 

  34. 34.

    Sapkota A, Hsu CC, Zaridze D, Shangina O, Szeszenia-Dabrowska N, Mates D, et al. Dietary risk factors for squamous cell carcinoma of the upper aerodigestive tract in central and eastern Europe. Cancer Causes Control. 2008;19:1161–70.

    CAS  Article  Google Scholar 

  35. 35.

    Choi Y, Song S, Song Y, Lee JE. Consumption of red and processed meat and esophageal cancer risk: meta-analysis. World J Gastroenterol. 2013;19:1020–9.

    Article  Google Scholar 

  36. 36.

    Jakszyn P, Lujan-Barroso L, Agudo A, Bueno-de-Mesquita HB, Molina E, Sanchez MJ, et al. Meat and heme iron intake and esophageal adenocarcinoma in the European Prospective Investigation into Cancer and Nutrition study. Int J Cancer. 2013;133:2744–50.

    CAS  PubMed  Google Scholar 

  37. 37.

    Fang X, Wei J, He X, An P, Wang H, Jiang L, et al. Landscape of dietary factors associated with risk of gastric cancer: A systematic review and dose-response meta-analysis of prospective cohort studies. Eur J Cancer. 2015;51:2820–32.

    Article  Google Scholar 

  38. 38.

    World Cancer Research Fund International/American Institute for Cancer Research. Continuous Update Project Report: Diet, Nutrition, Physical Activity and Stomach Cancer. 2016. wcrf.org/stomach-cancer-2016.

  39. 39.

    Fedirko V, Trichopolou A, Bamia C, Duarte-Salles T, Trepo E, Aleksandrova K, et al. Consumption of fish and meats and risk of hepatocellular carcinoma: the European Prospective Investigation into Cancer and Nutrition (EPIC). Ann Oncol. 2013;24:2166–73.

    CAS  Article  Google Scholar 

  40. 40.

    Kanazir M, Boricic I, Delic D, Tepavcevic DK, Knezevic A, Jovanovic T, et al. Risk factors for hepatocellular carcinoma: a case-control study in Belgrade (Serbia). Tumori. 2010;96:911–7.

    Article  Google Scholar 

  41. 41.

    Tominaga S, Kuroishi T, Ogawa H, Shimizu H. Epidemiologic aspects of biliary tract cancer in Japan. Natl Cancer Inst Monogr. 1979;25–34.

  42. 42.

    Moerman CJ, Bueno de Mesquita HB, Smeets FW, Runia S. Consumption of foods and micronutrients and the risk of cancer of the biliary tract. Prev Med. 1995;24:591–602.

    CAS  Article  Google Scholar 

  43. 43.

    Kato K, Akai S, Tominaga S, Kato I. A case-control study of biliary tract cancer in Niigata Prefecture, Japan. Jpn J Cancer Res. 1989;80:932–8.

    CAS  Article  Google Scholar 

  44. 44.

    Hsing AW, Rashid A, Devesa SS, Fraumeni JFJ. Biliary tract cancer. IN: Schottenfeld D, Fraumeni JF, editors. Cancer epidemiology and prevention. New York: Oxford University Press; 2006. p. 787–800.

  45. 45.

    Rohrmann S, Linseisen J, Nothlings U, Overvad K, Egeberg R, Tjonneland A, et al. Meat and fish consumption and risk of pancreatic cancer: results from the European Prospective Investigation into Cancer and Nutrition. Int J Cancer. 2013;132:617–24.

    CAS  Article  Google Scholar 

  46. 46.

    Taunk P, Hecht E, Stolzenberg-Solomon R. Are meat and heme iron intake associated with pancreatic cancer? Results from the NIH-AARP diet and health cohort. Int J Cancer. 2016;138:2172–89.

    CAS  Article  Google Scholar 

  47. 47.

    McCullough ML, Jacobs EJ, Shah R, Campbell PT, Wang Y, Hartman TJ, et al. Meat consumption and pancreatic cancer risk among men and women in the Cancer Prevention Study-II Nutrition Cohort. Cancer Causes Control. 2017;29:125–33.

    Article  Google Scholar 

  48. 48.

    Battaglia Richi E, Baumer B, Conrad B, Darioli R, Schmid A, Keller U. Health risks associated with meat consumption: a review of epidemiological studies. Int J Vitam Nutr Res. 2015;85:70–78.

    Article  Google Scholar 

  49. 49.

    Norat T, Scoccianti C, Boutron-Ruault MC, Anderson A, Berrino F, Cecchini M, et al. European Code against Cancer 4th Edition: Diet and cancer. Cancer Epidemiol. 2015;39 Suppl 1:S56–66.

    Article  Google Scholar 

  50. 50.

    Santarelli RL, Pierre F, Corpet DE. Processed meat and colorectal cancer: a review of epidemiologic and experimental evidence. Nutr Cancer. 2008;60:131–44.

    CAS  Article  Google Scholar 

  51. 51.

    Keszei AP, Goldbohm RA, Schouten LJ, Jakszyn P, van den Brandt PA. Dietary N-nitroso compounds, endogenous nitrosation, and the risk of esophageal and gastric cancer subtypes in the Netherlands Cohort Study. Am J Clin Nutr. 2013;97:135–46.

    CAS  Article  Google Scholar 

  52. 52.

    Coss A, Cantor KP, Reif JS, Lynch CF, Ward MH. Pancreatic cancer and drinking water and dietary sources of nitrate and nitrite. Am J Epidemiol. 2004;159:693–701.

    Article  Google Scholar 

  53. 53.

    Risch HA. Etiology of pancreatic cancer, with a hypothesis concerning the role of N-nitroso compounds and excess gastric acidity. J Natl Cancer Inst. 2003;95:948–60.

    CAS  Article  Google Scholar 

  54. 54.

    Orlich MJ, Jaceldo-Siegl K, Sabate J, Fan J, Singh PN, Fraser GE. Patterns of food consumption among vegetarians and non-vegetarians. Br J Nutr. 2014;112:1644–53.

    CAS  Article  Google Scholar 

  55. 55.

    La Vecchia C, Negri E, Franceschi S, Parazzini F, Decarli A. Differences in dietary intake with smoking, alcohol, and education. Nutr Cancer. 1992;17:297–304.

    Article  Google Scholar 

Download references

Acknowledgements

This work was conducted within a grant by the Italian Foundation for Cancer Research (FIRC) and received unconditional support by ASSICA. Funders had no role in study design, data collection, analysis or interpretation, manuscript preparation, or the decision to publish. VR was supported by a fellowship from the Italian Foundation for Cancer Research (FIRC No. 18107). In addition, DK was supported by JSPS Grant-in-Aid for Young Scientists (B) (No. 15K21283).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Monica Ferraroni.

Ethics declarations

Conflict of interest

Partially supported by unconditional grant to the Department of Clinical Sciences and Community Health, University of Milan, by ASSICA.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Rosato, V., Kawakita, D., Negri, E. et al. Processed meat and risk of selected digestive tract and laryngeal cancers. Eur J Clin Nutr 73, 141–149 (2019). https://doi.org/10.1038/s41430-018-0153-7

Download citation

Further reading