Skip to main content
Top
Published in: Digestive Diseases and Sciences 3/2014

01-03-2014 | Original Article

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

Authors: Hong-Cheng Zhu, Xi Yang, Li-Ping Xu, Lian-Jun Zhao, Guang-Zhou Tao, Chi Zhang, Qin Qin, Jing Cai, Jian-Xin Ma, Wei-Dong Mao, Xi-Zhi Zhang, Hong-Yan Cheng, Xin-Chen Sun

Published in: Digestive Diseases and Sciences | Issue 3/2014

Login to get access

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.
Appendix
Available only for authorised users
Literature
1.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
2.
go back to reference Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics. 1994;50:1088–1101.PubMedCrossRef Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics. 1994;50:1088–1101.PubMedCrossRef
3.
go back to reference 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. 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.
4.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
5.
go back to reference 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.PubMed 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.PubMed
6.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
7.
go back to reference 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.PubMedCentralPubMedCrossRef 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.PubMedCentralPubMedCrossRef
8.
go back to reference 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.PubMedCentralPubMedCrossRef 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.PubMedCentralPubMedCrossRef
9.
go back to reference 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.CrossRef 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.CrossRef
10.
11.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
12.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
13.
go back to reference 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 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
14.
go back to reference Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997;315:629–634.PubMedCrossRef Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997;315:629–634.PubMedCrossRef
15.
go back to reference 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.PubMedCentralPubMedCrossRef 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.PubMedCentralPubMedCrossRef
16.
go back to reference Fernandez E, Chatenoud L, La Vecchia C, Negri E, Franceschi S. Fish consumption and cancer risk. Am J Clin Nutr. 1999;70:85–90.PubMed Fernandez E, Chatenoud L, La Vecchia C, Negri E, Franceschi S. Fish consumption and cancer risk. Am J Clin Nutr. 1999;70:85–90.PubMed
17.
go back to reference 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.PubMedCentralPubMed 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.PubMedCentralPubMed
18.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
19.
go back to reference 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.PubMedCentralPubMedCrossRef 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.PubMedCentralPubMedCrossRef
20.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
21.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
22.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
23.
go back to reference 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 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
24.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
25.
go back to reference 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. 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.
26.
go back to reference 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.CrossRef 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.CrossRef
27.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
28.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
29.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
30.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
31.
go back to reference 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. 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.
32.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
33.
go back to reference 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.PubMedCentralPubMedCrossRef 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.PubMedCentralPubMedCrossRef
34.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
35.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
36.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
37.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
38.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
39.
go back to reference Notani PN, Jayant K. Role of diet in upper aerodigestive tract cancers. Nutr Cancer. 1987;10:103–113.PubMedCrossRef Notani PN, Jayant K. Role of diet in upper aerodigestive tract cancers. Nutr Cancer. 1987;10:103–113.PubMedCrossRef
40.
go back to reference 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. 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.
41.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
42.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
43.
44.
go back to reference 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 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
45.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
46.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
47.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
48.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
49.
go back to reference 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.PubMed 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.PubMed
50.
go back to reference 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.PubMed 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.PubMed
51.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
52.
go back to reference Wang C, Jiang H. Meat intake and risk of bladder cancer: a meta-analysis. Med Oncol. 2012;29:848–855.PubMedCrossRef Wang C, Jiang H. Meat intake and risk of bladder cancer: a meta-analysis. Med Oncol. 2012;29:848–855.PubMedCrossRef
53.
go back to reference 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.PubMedCentralPubMedCrossRef 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.PubMedCentralPubMedCrossRef
54.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
55.
go back to reference 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. 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.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
57.
go back to reference 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 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
58.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
59.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
60.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
Metadata
Title
Meat Consumption Is Associated with Esophageal Cancer Risk in a Meat- and Cancer-Histological-Type Dependent Manner
Authors
Hong-Cheng Zhu
Xi Yang
Li-Ping Xu
Lian-Jun Zhao
Guang-Zhou Tao
Chi Zhang
Qin Qin
Jing Cai
Jian-Xin Ma
Wei-Dong Mao
Xi-Zhi Zhang
Hong-Yan Cheng
Xin-Chen Sun
Publication date
01-03-2014
Publisher
Springer US
Published in
Digestive Diseases and Sciences / Issue 3/2014
Print ISSN: 0163-2116
Electronic ISSN: 1573-2568
DOI
https://doi.org/10.1007/s10620-013-2928-y

Other articles of this Issue 3/2014

Digestive Diseases and Sciences 3/2014 Go to the issue

UNM Clinical Case Conferences

The Clinical Course of Acute Hepatitis C