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Red and processed meat consumption and esophageal cancer risk: a systematic review and meta-analysis

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Abstract

Background

The associations between red and processed meat consumption and esophageal cancer risk remain inconclusive. We performed a systematic review and meta-analysis to analyze these associations.

Methods

We searched PubMed and EMBASE to identify studies published between the databases’ dates of inception and May 2019.

Results

We ultimately selected 33 eligible studies for analysis. We found that the summary relative risks for the associations between meat consumption and esophageal cancer risk were positive for the case–control studies (P < 0.05), but negative for the cohort studies included in the analysis (P > 0.05). Subtype analysis indicated that red and processed meat consumption was not associated with the risks of esophageal adenocarcinoma (P > 0.05) and esophageal squamous cell carcinoma (P > 0.05) in the cohort studies.

Conclusions

We found case–control but not cohort studies to associate consumption of red and processed meat with the risk of esophageal cancer. Further large prospective studies are needed to validate these findings.

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References

  1. Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68(6):394–424. https://doi.org/10.3322/caac.21492.

    Article  PubMed  Google Scholar 

  2. Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics, 2012. CA Cancer J Clin. 2015;65(2):87–108. https://doi.org/10.3322/caac.21262.

    Article  PubMed  Google Scholar 

  3. Islami F, Pourshams A, Nasrollahzadeh D, Kamangar F, Fahimi S, Shakeri R, et al. Tea drinking habits and oesophageal cancer in a high risk area in northern Iran: population based case-control study. BMJ. 2009;338:b929.

    Article  Google Scholar 

  4. Liu J, Wang J, Leng Y, Lv C. Intake of fruit and vegetables and risk of esophageal squamous cell carcinoma: a meta-analysis of observational studies. Int J Cancer. 2013;133(2):473–85. https://doi.org/10.1002/ijc.28024.

    Article  CAS  PubMed  Google Scholar 

  5. Li B, Jiang G, Zhang G, Xue Q, Zhang H, Wang C, et al. Intake of vegetables and fruit and risk of esophageal adenocarcinoma: a meta-analysis of observational studies. Eur J Nutr. 2014;53(7):1511–21. https://doi.org/10.1007/s00394-014-0656-5.

    Article  PubMed  Google Scholar 

  6. Jiang G, Li B, Liao X, Zhong C. Poultry and fish intake and risk of esophageal cancer: a meta-analysis of observational studies. Asia Pac J Clin Oncol. 2016;12(1):e82–91. https://doi.org/10.1111/ajco.12114.

    Article  PubMed  Google Scholar 

  7. Kaluza J, Harris H, Linden A, Wolk A. Long-term unprocessed and processed red meat consumption and risk of chronic obstructive pulmonary disease: a prospective cohort study of women. Eur J Nutr. 2018. https://doi.org/10.1007/s00394-018-1658-5.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Horikawa C, Kamada C, Tanaka S, Tanaka S, Araki A, Ito H, et al. Meat intake and incidence of cardiovascular disease in Japanese patients with type 2 diabetes: analysis of the Japan Diabetes Complications Study (JDCS). Eur J Nutr. 2017. https://doi.org/10.1007/s00394-017-1592-y.

    Article  PubMed  Google Scholar 

  9. de Batlle J, Gracia-Lavedan E, Romaguera D, Mendez M, Castano-Vinyals G, Martin V, et al. Meat intake, cooking methods and doneness and risk of colorectal tumours in the Spanish multicase-control study (MCC-Spain). Eur J Nutr. 2018;57(2):643–53. https://doi.org/10.1007/s00394-016-1350-6.

    Article  CAS  PubMed  Google Scholar 

  10. Lin S, Wang X, Huang C, Liu X, Zhao J, Yu IT, et al. Consumption of salted meat and its interactions with alcohol drinking and tobacco smoking on esophageal squamous-cell carcinoma. Int J Cancer. 2015;137(3):582–9. https://doi.org/10.1002/ijc.29406.

    Article  CAS  PubMed  Google Scholar 

  11. Zhu HC, Yang X, Xu LP, Zhao LJ, Tao GZ, Zhang C, et al. Meat consumption is associated with esophageal cancer risk in a meat- and cancer-histological-type dependent manner. Dig Dis Sci. 2014;59(3):664–73. https://doi.org/10.1007/s10620-013-2928-y.

    Article  CAS  PubMed  Google Scholar 

  12. O’Doherty MG, Cantwell MM, Murray LJ, Anderson LA, Abnet CC. Dietary fat and meat intakes and risk of reflux esophagitis, Barrett’s esophagus and esophageal adenocarcinoma. Int J Cancer. 2011;129(6):1493–502. https://doi.org/10.1002/ijc.26108.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. 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(2):134–8. https://doi.org/10.1097/CEJ.0b013e32834c9b6c.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol. 2010;25(9):603–5. https://doi.org/10.1007/s10654-010-9491-z.

    Article  Google Scholar 

  15. Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ. 2003;327(7414):557–60. https://doi.org/10.1136/bmj.327.7414.557.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Egger M, Davey SG, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997;315(7109):629–34.

    Article  CAS  Google Scholar 

  17. Yu MC, Garabrant DH, Peters JM, Mack TM. Tobacco, alcohol, diet, occupation, and carcinoma of the esophagus. Cancer Res. 1988;48(13):3843–8.

    CAS  PubMed  Google Scholar 

  18. Rogers MA, Thomas DB, Davis S, Vaughan TL, Nevissi AE. A case-control study of element levels and cancer of the upper aerodigestive tract. Cancer Epidemiol Biomarkers Prev. 1993;2(4):305–12.

    CAS  PubMed  Google Scholar 

  19. Tavani A, Negri E, Franceschi S, La Vecchia C. Risk factors for esophageal cancer in lifelong nonsmokers. Cancer Epidemiol Biomarkers Prev. 1994;3(5):387–92.

    CAS  PubMed  Google Scholar 

  20. Castelletto R, Castellsague X, Munoz N, Iscovich J, Chopita N, Jmelnitsky A. Alcohol, tobacco, diet, mate drinking, and esophageal cancer in Argentina. Cancer Epidemiol Biomarkers Prev. 1994;3(7):557–64.

    CAS  PubMed  Google Scholar 

  21. Rolon PA, Castellsague X, Benz M, Munoz N. Hot and cold mate drinking and esophageal cancer in Paraguay. Cancer Epidemiol Biomarkers Prev. 1995;4(6):595–605.

    CAS  PubMed  Google Scholar 

  22. 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(2):289–94.

    Article  CAS  Google Scholar 

  23. Takezaki T, Shinoda M, Hatooka S, Hasegawa Y, Nakamura S, Hirose K, et al. Subsite-specific risk factors for hypopharyngeal and esophageal cancer (Japan). Cancer Causes Control. 2000;11(7):597–608.

    Article  CAS  Google Scholar 

  24. Takezaki T, Gao CM, Wu JZ, Ding JH, Liu YT, Zhang Y, 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(11):1157–65.

    Article  CAS  Google Scholar 

  25. Chen H, Ward MH, Graubard BI, Heineman EF, Markin RM, Potischman NA, et al. Dietary patterns and adenocarcinoma of the esophagus and distal stomach. Am J Clin Nutr. 2002;75(1):137–44.

    Article  CAS  Google Scholar 

  26. Li K, Yu P. Food groups and risk of esophageal cancer in Chaoshan region of China: a high-risk area of esophageal cancer. Cancer Invest. 2003;21(2):237–40.

    Article  Google Scholar 

  27. 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(2):346–9.

    Article  CAS  Google Scholar 

  28. Hung HC, Huang MC, Lee JM, Wu DC, Hsu HK, Wu MT. Association between diet and esophageal cancer in Taiwan. J Gastroenterol Hepatol. 2004;19(6):632–7. https://doi.org/10.1111/j.1440-1746.2004.03346.x.

    Article  PubMed  Google Scholar 

  29. Yang CX, Wang HY, Wang ZM, Du HZ, Tao DM, Mu XY, et al. Risk factors for esophageal cancer: a case-control study in South-western China. Asian Pac J Cancer Prev. 2005;6(1):48–53.

    PubMed  Google Scholar 

  30. Wu AH, Tseng CC, Hankin J, Bernstein L. Fiber intake and risk of adenocarcinomas of the esophagus and stomach. Cancer Causes Control. 2007;18(7):713–22. https://doi.org/10.1007/s10552-007-9014-8.

    Article  PubMed  Google Scholar 

  31. Wang JM, Xu B, Rao JY, Shen HB, Xue HC, Jiang QW. Diet habits, alcohol drinking, tobacco smoking, green tea drinking, and the risk of esophageal squamous cell carcinoma in the Chinese population. Eur J Gastroenterol Hepatol. 2007;19(2):171–6. https://doi.org/10.1097/MEG.0b013e32800ff77a.

    Article  CAS  PubMed  Google Scholar 

  32. 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(10):1161–70. https://doi.org/10.1007/s10552-008-9183-0.

    Article  CAS  PubMed  Google Scholar 

  33. Chen YK, Lee CH, Wu IC, Liu JS, Wu DC, Lee JM, et al. Food intake and the occurrence of squamous cell carcinoma in different sections of the esophagus in Taiwanese men. Nutrition. 2009;25(7–8):753–61. https://doi.org/10.1016/j.nut.2009.02.002.

    Article  CAS  PubMed  Google Scholar 

  34. Aune D, De Stefani E, Ronco A, Boffetta P, Deneo-Pellegrini H, Acosta G, et al. Meat consumption and cancer risk: a case-control study in Uruguay. Asian Pac J Cancer Prev. 2009;10(3):429–36.

    PubMed  Google Scholar 

  35. Wu M, Zhang ZF, Kampman E, Zhou JY, Han RQ, Yang J, et al. Does family history of cancer modify the effects of lifestyle risk factors on esophageal cancer? A population-based case-control study in China. Int J Cancer. 2011;128(9):2147–57. https://doi.org/10.1002/ijc.25532.

    Article  CAS  PubMed  Google Scholar 

  36. Gao Y, Hu N, Han XY, Ding T, Giffen C, Goldstein AM, et al. Risk factors for esophageal and gastric cancers in Shanxi Province, China: a case-control study. Cancer Epidemiol. 2011;35(6):e91–9. https://doi.org/10.1016/j.canep.2011.06.006.

    Article  PubMed  PubMed Central  Google Scholar 

  37. 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(5):707–13. https://doi.org/10.1080/01635581.2011.563028.

    Article  CAS  PubMed  Google Scholar 

  38. O’Doherty MG, Cantwell MM, Murray LJ, Anderson LA, Abnet CC. Dietary fat and meat intakes and risk of reflux esophagitis, Barrett’s esophagus and esophageal adenocarcinoma. Int J Cancer. 2011;129(6):1493–502. https://doi.org/10.1002/ijc.26108.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. De Stefani E, Deneo-Pellegrini H, Ronco AL, Boffetta P, Correa P, Aune D, 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(2):294–9. https://doi.org/10.1080/01635581.2012.648299.

    Article  PubMed  Google Scholar 

  40. Song Q, Wang X, Yu IT, Huang C, Zhou X, Li J, et al. Processed food consumption and risk of esophageal squamous cell carcinoma: a case-control study in a high risk area. Cancer Sci. 2012;103(11):2007–11. https://doi.org/10.1111/j.1349-7006.2012.02387.x.

    Article  CAS  PubMed  Google Scholar 

  41. Di Maso M, Talamini R, Bosetti C, Montella M, Zucchetto A, Libra M, et al. Red meat and cancer risk in a network of case-control studies focusing on cooking practices. Ann Oncol. 2013;24(12):3107–12. https://doi.org/10.1093/annonc/mdt392.

    Article  PubMed  Google Scholar 

  42. De Stefani E, Boffetta P, Ronco AL, Deneo-Pellegrini H, Correa P, Acosta G, et al. Processed meat consumption and squamous cell carcinoma of the oesophagus in a large case-control study in Uruguay. Asian Pac J Cancer Prev. 2014;15(14):5829–33.

    Article  Google Scholar 

  43. Golozar A, Etemadi A, Kamangar F, Fazeltabar MA, Islami F, Nasrollahzadeh D, et al. Food preparation methods, drinking water source, and esophageal squamous cell carcinoma in the high-risk area of Golestan, Northeast Iran. Eur J Cancer Prev. 2016;25(2):123–9. https://doi.org/10.1097/CEJ.0000000000000156.

    Article  PubMed  PubMed Central  Google Scholar 

  44. Rosato V, Kawakita D, Negri E, Serraino D, Garavello W, Montella M, et al. Processed meat and risk of selected digestive tract and laryngeal cancers. Eur J Clin Nutr. 2019;73(1):141–9. https://doi.org/10.1038/s41430-018-0153-7.

    Article  PubMed  Google Scholar 

  45. Yu Y, Taylor PR, Li JY, Dawsey SM, Wang GQ, Guo WD, et al. Retrospective cohort study of risk-factors for esophageal cancer in Linxian, People’s Republic of China. Cancer Causes Control. 1993;4(3):195–202.

    PubMed  Google Scholar 

  46. Cross AJ, Freedman ND, Ren J, Ward MH, Hollenbeck AR, Schatzkin A, et al. Meat consumption and risk of esophageal and gastric cancer in a large prospective study. Am J Gastroenterol. 2011;106(3):432–42. https://doi.org/10.1038/ajg.2010.415.

    Article  CAS  PubMed  Google Scholar 

  47. 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(9):2319–26. https://doi.org/10.1093/annonc/mdr615.

    Article  CAS  PubMed  Google Scholar 

  48. 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(11):2744–50. https://doi.org/10.1002/ijc.28291.

    Article  CAS  PubMed  Google Scholar 

  49. 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(5):257–67. https://doi.org/10.1111/nure.12028.

    Article  PubMed  Google Scholar 

  50. Qu X, Ben Q, Jiang Y. Consumption of red and processed meat and risk for esophageal squamous cell carcinoma based on a meta-analysis. Ann Epidemiol. 2013;23(12):762–70. https://doi.org/10.1016/j.annepidem.2013.09.003.

    Article  PubMed  Google Scholar 

  51. 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(7):1020–9. https://doi.org/10.3748/wjg.v19.i7.1020.

    Article  PubMed  PubMed Central  Google Scholar 

  52. Samraj AN, Pearce OM, Laubli H, Crittenden AN, Bergfeld AK, Banda K, et al. A red meat-derived glycan promotes inflammation and cancer progression. Proc Natl Acad Sci USA. 2015;112(2):542–7. https://doi.org/10.1073/pnas.1417508112.

    Article  CAS  PubMed  Google Scholar 

  53. Bastide NM, Chenni F, Audebert M, Santarelli RL, Tache S, Naud N, et al. A central role for heme iron in colon carcinogenesis associated with red meat intake. Cancer Res. 2015;75(5):870–9. https://doi.org/10.1158/0008-5472.CAN-14-2554.

    Article  CAS  PubMed  Google Scholar 

  54. Xie FJ, Zhang YP, Zheng QQ, Jin HC, Wang FL, Chen M, et al. Helicobacter pylori infection and esophageal cancer risk: an updated meta-analysis. World J Gastroenterol. 2013;19(36):6098–107. https://doi.org/10.3748/wjg.v19.i36.6098.

    Article  PubMed  PubMed Central  Google Scholar 

  55. Petrick JL, Wyss AB, Butler AM, Cummings C, Sun X, Poole C, et al. Prevalence of human papillomavirus among oesophageal squamous cell carcinoma cases: systematic review and meta-analysis. Br J Cancer. 2014;110(9):2369–77. https://doi.org/10.1038/bjc.2014.96.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Flood A, Velie EM, Sinha R, Chaterjee N, Lacey JJ, Schairer C, et al. Meat, fat, and their subtypes as risk factors for colorectal cancer in a prospective cohort of women. Am J Epidemiol. 2003;158(1):59–68.

    Article  Google Scholar 

  57. Li WQ, Park Y, Wu JW, Ren JS, Goldstein AM, Taylor PR, et al. Index-based dietary patterns and risk of esophageal and gastric cancer in a large cohort study. Clin Gastroenterol Hepatol. 2013;11(9):1130–6. https://doi.org/10.1016/j.cgh.2013.03.023.

    Article  PubMed  PubMed Central  Google Scholar 

  58. Jung KW, Talley NJ, Romero Y, Katzka DA, Schleck CD, Zinsmeister AR, et al. Epidemiology and natural history of intestinal metaplasia of the gastroesophageal junction and Barrett’s esophagus: a population-based study. Am J Gastroenterol. 2011;106(8):1447–55. https://doi.org/10.1038/ajg.2011.130.

    Article  PubMed  PubMed Central  Google Scholar 

  59. Zhao Z, Pu Z, Yin Z, Yu P, Hao Y, Wang Q, et al. Dietary fruit, vegetable, fat, and red and processed meat intakes and Barrett’s esophagus risk: a systematic review and meta-analysis. Sci Rep. 2016;6:27334. https://doi.org/10.1038/srep27334.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Funding

This work was supported by the funds of the Innovation Funds of Navy General Hospital (CXPY201801) and the Bethune Charitable Foundation HZB-20181119-71.

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Contributions

Zhanwei Zhao, and Fei Wang wrote the main manuscript text, participated in the design of the work. Di Chen participated in the analysis of the data and prepared figures. Chaojun Zhang carried out the study design, the analysis and interpretation of the data and drafted the manuscript. All authors have reviewed the manuscript. Zhanwei Zhao, Fei Wang and Di Chen contributed equally to this work.

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Correspondence to C. Zhang.

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This work described was original research that has not been published previously, and not under consideration for publication elsewhere, in whole or in part. All the authors listed have approved the manuscript that is enclosed. Our meta-analysis did not involve human participants and animals.

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Zhao, Z., Wang, F., Chen, D. et al. Red and processed meat consumption and esophageal cancer risk: a systematic review and meta-analysis. Clin Transl Oncol 22, 532–545 (2020). https://doi.org/10.1007/s12094-019-02157-0

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