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Meat Consumption Is Associated with Esophageal Cancer Risk in a Meat- and Cancer-Histological-Type Dependent Manner

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Abstract

Background

We conducted a systematic review and meta-analysis of meat intake and esophageal cancer risk, with subgroup analyses based on meat type and histological type of cancer.

Aims

The purpose of this study was to investigate the association between meat intake and risk of esophageal cancer.

Methods

We searched MEDLINE, EMBASE and Cochrane Library (April 2013) for cohort and case–control studies that assessed meat intake and esophageal cancer risk. Random-effect or fixed-effect models were used to pool relative risks (RRs) from individual studies with heterogeneity and publication bias analyses carried out. Seven cohort and 28 case–control studies were included.

Results

The summary RRs for esophageal cancer for the highest versus lowest consumption categories were 1.19 (95 % confidence interval [CI] 0.98–1.46) for total meat, 1.55 (95 % CI 1.22–1.96) for red meat, 1.33 (95 % CI 1.04–1.69) for processed meat, 0.72 (95 % CI 0.60–0.86) for white meat, 0.83 (95 % CI 0.72–0.96) for poultry, and 0.95 (95 % CI 0.76–1.19) for fish. When striated by histological subtype, positive associations were seen among esophageal squamous cell carcinoma and red meat, white meat and poultry, and esophageal adenocarcinoma with total meat and processed meat.

Conclusions

Meat consumption is associated with esophageal cancer risk, which depends on meat type and histological type of esophageal cancer. High intake of red meat and low intake of poultry are associated with an increased risk of esophageal squamous cell carcinoma. High meat intake, especially processed meat, is likely to increase esophageal adenocarcinoma risk. And fish consumption may not be associated with incidence of esophageal cancer.

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References

  1. Abnet CC, Lai B, Qiao YL, et al. Zinc concentration in esophageal biopsy specimens measured by x-ray fluorescence and esophageal cancer risk. J Natl Cancer Inst. 2005;97:301–306.

    Article  CAS  PubMed  Google Scholar 

  2. Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics. 1994;50:1088–1101.

    Article  CAS  PubMed  Google Scholar 

  3. Bosetti C, La Vecchia C, Talamini R, et al. Food groups and risk of squamous cell esophageal cancer in northern Italy. Int J Cancer. 2000;87:289–294.

    Google Scholar 

  4. Brown LM, Blot WJ, Schuman SH, et al. Environmental factors and high risk of esophageal cancer among men in coastal South Carolina. J Natl Cancer Inst. 1988;80:1620–1625.

    Article  CAS  PubMed  Google Scholar 

  5. Chen H, Ward MH, Graubard BI, et al. Dietary patterns and adenocarcinoma of the esophagus and distal stomach. Am J Clin Nutr. 2002;75:137–144.

    CAS  PubMed  Google Scholar 

  6. Choi Y, Song S, Song Y, Lee JE. Consumption of red and processed meat and esophageal cancer risk: meta-analysis. World J Gastroenterol. 2013;19:1020–1029.

    Article  PubMed  Google Scholar 

  7. Cook-Mozaffari PJ, Azordegan F, Day NE, Ressicaud A, Sabai C, Aramesh B. Oesophageal cancer studies in the Caspian Littoral of Iran: results of a case–control study. Br J Cancer. 1979;39:293–309.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  8. Cross AJ, Freedman ND, Ren J, et al. Meat consumption and risk of esophageal and gastric cancer in a large prospective study. Am J Gastroenterol. 2011;106:432–442.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  9. Daniel CR, Cross AJ, Graubard BI, Hollenbeck AR, Park Y, Sinha R. Prospective investigation of poultry and fish intake in relation to cancer risk. Cancer Prev Res (Phila). 2011;4:1903–1911.

    Article  Google Scholar 

  10. DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986;7:177–188.

    Article  CAS  PubMed  Google Scholar 

  11. De Stefani E, Deneo-Pellegrini H, Boffetta P, Mendilaharsu M. Meat intake and risk of squamous cell esophageal cancer: a case–control study in Uruguay. Int J Cancer. 1999;82:33–37.

    Article  PubMed  Google Scholar 

  12. De Stefani E, Deneo-Pellegrini H, Ronco AL, et al. Meat consumption, cooking methods, mutagens, and risk of squamous cell carcinoma of the esophagus: a case–control study in Uruguay. Nutr Cancer. 2012;64:294–299.

    Article  PubMed  Google Scholar 

  13. De Stefani E, Muñoz N, Estève J, Vasallo A, Victora CG, Teuchmann S. Mate drinking, alcohol, tobacco, diet, and esophageal cancer in Uruguay. Cancer Res. 1990;50:426–431.

    PubMed  Google Scholar 

  14. Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997;315:629–634.

    Article  CAS  PubMed  Google Scholar 

  15. Fan Y, Yuan JM, Wang R, Gao YT, Yu MC. Alcohol, tobacco, and diet in relation to esophageal cancer: the Shanghai Cohort Study. Nutr Cancer. 2008;60:354–363.

    Article  PubMed Central  PubMed  Google Scholar 

  16. Fernandez E, Chatenoud L, La Vecchia C, Negri E, Franceschi S. Fish consumption and cancer risk. Am J Clin Nutr. 1999;70:85–90.

    CAS  PubMed  Google Scholar 

  17. Flood A, Rastogi T, Wirfält E, et al. Dietary patterns as identified by factor analysis and colorectal cancer among middle-aged Americans. Am J Clin Nutr. 2008;88:176–184.

    CAS  PubMed Central  PubMed  Google Scholar 

  18. Ganesh B, Talole SD, Dikshit R. Tobacco, alcohol and tea drinking as risk factors for esophageal cancer: a case–control study from Mumbai, India. Cancer Epidemiol. 2009;33:431–434.

    Article  CAS  PubMed  Google Scholar 

  19. Gao Y, Hu N, Han XY, et al. Risk factors for esophageal and gastric cancers in Shanxi Province, China: a case–control study. Cancer Epidemiol. 2011;35:e91–e99.

    Article  PubMed Central  PubMed  Google Scholar 

  20. González CA, Jakszyn P, Pera 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.

    Article  PubMed  Google Scholar 

  21. Hajizadeh B, Jessri M, Moasheri SM, Rad AH, Rashidkhani B. Fruits and vegetables consumption and esophageal squamous cell carcinoma: a case–control study. Nutr Cancer. 2011;63:707–713.

    Article  CAS  PubMed  Google Scholar 

  22. Han YJ, Li J, Huang W, Fang Y, Xiao LN, Liao ZE. Fish consumption and risk of esophageal cancer and its subtypes: a systematic review and meta-analysis of observational studies. Eur J Clin Nutr. 2013;67:147–154.

    Article  CAS  PubMed  Google Scholar 

  23. Huang W, Han Y, Xu J, Zhu W, Li Z. Red and processed meat intake and risk of esophageal adenocarcinoma: a meta-analysis of observational studies. Cancer Causes Control. 2013;24(1):193–201.

    PubMed  Google Scholar 

  24. Huang X. Iron overload and its association with cancer risk in humans: evidence for iron as a carcinogenic metal. Mutat Res. 2003;533:153–171.

    Article  CAS  PubMed  Google Scholar 

  25. Ibiebele TI, Hughes MC, Whiteman DC, Webb PM, Australian Cancer Study. Dietary patterns and risk of oesophageal cancers: a population-based case–control study. Br J Nutr. 2012;107:1207–1216.

    Google Scholar 

  26. Jemal A, Center MM, DeSantis C, Ward EM. Global patterns of cancer incidence and mortality rates and trends. Cancer Epidemiol Biomarkers Prev. 2012;19:1893–1907.

    Article  Google Scholar 

  27. Kamangar F, Dores GM, Anderson WF. Patterns of cancer incidence, mortality, and prevalence across five continents: defining priorities to reduce cancer disparities in different geographic regions of the world. J Clin Oncol. 2006;24:2137–2150.

    Article  PubMed  Google Scholar 

  28. Ke L, Yu P, Zhang ZX. Novel epidemiologic evidence for the association between fermented fish sauce and esophageal cancer in South China. Int J Cancer. 2002;99:424–426.

    Article  CAS  PubMed  Google Scholar 

  29. Keszei AP, Schouten LJ, Goldbohm RA, van den Brandt PA. Red and processed meat consumption and the risk of esophageal and gastric cancer subtypes in The Netherlands Cohort Study. Ann Oncol. 2012;23:2319–2326.

    Article  CAS  PubMed  Google Scholar 

  30. Kinjo Y, Cui Y, Akiba S, et al. Mortality risks of oesophageal cancer associated with hot tea, alcohol, tobacco and diet in Japan. J Epidemiol. 1998;8:235–243.

    Article  CAS  PubMed  Google Scholar 

  31. Kolahdooz F, van der Pols JC, Bain CJ, et al. Meat, fish, and ovarian cancer risk: results from 2 Australian case-control studies, a systematic review, and meta-analysis. Am J Clin Nutr. 2010;91:1752–1763.

    Google Scholar 

  32. Lagergren J, Bergstrom R, Lindgren A, Nyren O. Symptomatic gastroesophageal reflux as a risk factor for esophageal adenocarcinoma. N Engl J Med. 1999;340:825–831.

    Article  CAS  PubMed  Google Scholar 

  33. Larsson SC, Wolk A. Red and processed meat consumption and risk of pancreatic cancer: meta-analysis of prospective studies. Br J Cancer. 2012;106:603–607.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  34. Launoy G, Milan C, Day NE, Pienkowski MP, Gignoux M, Faivre J. Diet and squamous-cell cancer of the oesophagus: a French multicentre case–control study. Int J Cancer. 1998;76:7–12.

    Article  CAS  PubMed  Google Scholar 

  35. Lepage C, Rachet B, Jooste V, Faivre J, Coleman MP. Continuing rapid increase in esophageal adenocarcinoma in England and Wales. Am J Gastroenterol. 2008;103:2694–2699.

    Article  PubMed  Google Scholar 

  36. Levi F, Pasche C, Lucchini F, et al. Food groups and oesophageal cancer risk in Vaud, Switzerland. Eur J Cancer Prev. 2000;9:257–263.

    Article  CAS  PubMed  Google Scholar 

  37. Lucenteforte E, Garavello W, Bosetti C, et al. Diet diversity and the risk of squamous cell esophageal cancer. Int J Cancer. 2008;123:2397–2400.

    Article  CAS  PubMed  Google Scholar 

  38. Navarro Silvera SA, Mayne ST, Risch HA, et al. Principal component analysis of dietary and lifestyle patterns in relation to risk of subtypes of esophageal and gastric cancer. Ann Epidemiol. 2011;21:543–550.

    Article  PubMed  Google Scholar 

  39. Notani PN, Jayant K. Role of diet in upper aerodigestive tract cancers. Nutr Cancer. 1987;10:103–113.

    Article  CAS  PubMed  Google Scholar 

  40. O’Doherty MG, Cantwell MM, Murray LJ, Anderson LA, Abnet CC, FINBAR Study Group. Dietary fat and meat intakes and risk of reflux esophagitis, Barrett’s esophagus and esophageal adenocarcinoma. Int J Cancer. 2011;129:1493–1502.

    Google Scholar 

  41. Pan G, Takahashi K, Feng Y, et al. Nested case–control study of esophageal cancer in relation to occupational exposure to silica and other dusts. Am J Ind Med. 1999;35:272–280.

    Article  CAS  PubMed  Google Scholar 

  42. Phukan RK, Chetia CK, Ali MS, Mahanta J. Role of dietary habits in the development of esophageal cancer in Assam, the north-eastern region of India. Nutr Cancer. 2001;39:204–209.

    Article  CAS  PubMed  Google Scholar 

  43. Pennathur A, Gibson MK, Jobe BA, Luketich JD. Oesophageal carcinoma. Lancet. 2013;381:400–412.

    Article  PubMed  Google Scholar 

  44. Rolón PA, Castellsagué X, Benz M, Muñoz N. Hot and cold mate drinking and esophageal cancer in Paraguay. Cancer Epidemiol Biomarkers Prev. 1995;4:595–605.

    PubMed  Google Scholar 

  45. Salehi M, Moradi-Lakeh M, Salehi MH, Nojomi M, Kolahdooz F. Meat, fish, and esophageal cancer risk: a systematic review and dose-response meta-analysis. Nutr Rev. 2013;71:257–267.

    Article  PubMed  Google Scholar 

  46. Sapkota A, Hsu CC, Zaridze D, et al. Dietary risk factors for squamous cell carcinoma of the upper aerodigestive tract in central and eastern Europe. Cancer Causes Control. 2008;19:1161–1170.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  48. Takezaki T, Gao CM, Wu JZ, et al. Dietary protective and risk factors for esophageal and stomach cancers in a low-epidemic area for stomach cancer in Jiangsu Province, China: comparison with those in a high-epidemic area. Jpn J Cancer Res. 2001;92:1157–1165.

    Article  CAS  PubMed  Google Scholar 

  49. Tavani A, Negri E, Franceschi S, La Vecchia C. Risk factors for esophageal cancer in lifelong nonsmokers. Cancer Epidemiol Biomarkers Prev. 1994;3:387–392.

    CAS  PubMed  Google Scholar 

  50. Terry PD, Lagergren J, Wolk A, Steineck G, Nyren O. Dietary intake of heterocyclic amines and cancers of the esophagus and gastric cardia. Cancer Epidemiol Biomarkers Prev. 2003;12:940–944.

    CAS  PubMed  Google Scholar 

  51. Tran GD, Sun XD, Abnet CC, et al. Prospective study of risk factors for esophageal and gastric cancers in the Linxian general population trial cohort in China. Int J Cancer. 2005;113:456–463.

    Article  CAS  PubMed  Google Scholar 

  52. Wang C, Jiang H. Meat intake and risk of bladder cancer: a meta-analysis. Med Oncol. 2012;29:848–855.

    Article  PubMed  Google Scholar 

  53. Ward MH, Cross AJ, Abnet CC, Sinha R, Markin RS, Weisenburger DD. Heme iron from meat and risk of adenocarcinoma of the esophagus and stomach. Eur J Cancer Prev. 2012;21:134–138.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  54. Ward MH, Sinha R, Heineman EF, et al. Risk of adenocarcinoma of the stomach and esophagus with meat cooking method and doneness preference. Int J Cancer. 1997;71:14–19.

    Article  CAS  PubMed  Google Scholar 

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

  56. Wu AH, Tseng CC, Hankin J, Bernstein L. Fiber intake and risk of adenocarcinomas of the esophagus and stomach. Cancer Causes Control. 2007;18:713–722.

    Article  PubMed  Google Scholar 

  57. Wu M, Zhao JK, Hu XS, et al. Association of smoking, alcohol drinking and dietary factors with esophageal cancer in high- and low-risk areas of Jiangsu Province, China. World J Gastroenterol. 2006;12:1686–1693.

    PubMed  Google Scholar 

  58. Xu X, Yu E, Gao X, et al. Red and processed meat intake and risk of colorectal adenomas: a meta-analysis of observational studies. Int J Cancer. 2013;132:437–448.

    Article  CAS  PubMed  Google Scholar 

  59. Yang WS, Va P, Wong MY, Zhang HL, Xiang YB. Soy intake is associated with lower lung cancer risk: results from a meta-analysis of epidemiologic studies. Am J Clin Nutr. 2011;94:1575–1583.

    Article  CAS  PubMed  Google Scholar 

  60. Yang WS, Wong MY, Vogtmann E, et al. Meat consumption and risk of lung cancer: evidence from observational studies. Ann Oncol. 2012;23:3163–3170.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by the Natural Science Foundation of China (No. 81272504), Innovation Team [No. LJ201123 (EH11)], Jiangsu Provincial Science and Technology Projects [BK2011854 (DA11)], research grants from the Chinese Society of Clinical Oncology [T-H2010-033 (KA10)], the introduction of talent of Jiangsu Province Hospital [NA11(2011)], A Project Funded by the Prority Academic Program Development of Jiangsu Higher Education Institutions (PAPD) (JX10231801), and grants from Key Academic Discipline of Jiangsu Province “Medical Aspects of Specific Environments”.

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Correspondence to Hong-Yan Cheng or Xin-Chen Sun.

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Hong-Cheng Zhu and Xi Yang contributed equally to this work.

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Zhu, HC., Yang, X., Xu, LP. et al. Meat Consumption Is Associated with Esophageal Cancer Risk in a Meat- and Cancer-Histological-Type Dependent Manner. Dig Dis Sci 59, 664–673 (2014). https://doi.org/10.1007/s10620-013-2928-y

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