Abstract
Purpose
The association of red meat consumption with the risk of stomach cancer has been reported by many studies, with inconclusive results. We performed a meta-analysis of cohort and case–control studies to provide a quantitative assessment of this association.
Methods
Relevant studies were identified by searching PubMed and Embase before December 2013 without restrictions. A total of 18 studies involving 1,228,327 subjects were included in this meta-analysis. Summary relative risks were estimated using random effects models.
Results
The pooled relative risks of gastric cancer were 1.37 (95 % CI 1.18–1.59) for the highest versus lowest categories of red meat intake with significant heterogeneity among studies (P heterogeneity < 0.001, I 2 = 67.6 %). When stratified by the study design, the significant associations were observed in population-based case–control studies (RR 1.58; 95 % CI 1.22–2.06; P heterogeneity < 0.001, I 2 = 73.0 %) and hospital-based case–control studies (RR 1.63; 95 % CI 1.38–1.92; P heterogeneity = 0.284, I 2 = 19.1 %). However, no association was observed among cohort studies (RR 1.00; 95 % CI 0.83–1.20; P heterogeneity = 0.158, I 2 = 33.9 %). The significant association was also presented in the subgroup analysis by geographic area (Asia, Europe), publication year (≥2000), sample size (<1,000, ≥1,000) and quality score (<7 stars, ≥7 stars). The dose–response analysis associated every 100 g/day increment in red meat intake with a 17 % increased gastric cancer risk (RR 1.17; 95 % CI 1.05–1.32). A linear regression model further revealed that the risk of gastric cancer increased with increasing level of red meat consumption.
Conclusions
Increased intake of red meat might be a risk factor for stomach cancer. Further larger prospective studies are warranted to verify this association.
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References
Aune D, De Stefani E, Ronco A, Boffetta P, Deneo-Pellegrini H, Acosta G, Mendilaharsu M (2009) Meat consumption and cancer risk: a case-control study in Uruguay. Asian Pac J Cancer Prev 10(3):429–436
Aune D, Chan DS, Vieira AR, Navarro Rosenblatt DA, Vieira R, Greenwood DC, Kampman E, Norat T (2013) Red and processed meat intake and risk of colorectal adenomas: a systematic review and meta-analysis of epidemiological studies. Cancer Causes Control 24(4):611–627. doi:10.1007/s10552-012-0139-z
Compare D, Rocco A, Nardone G (2010) Risk factors in gastric cancer. Eur Rev Med Pharmacol Sci 14(4):302–308
Cross AJ, Pollock JR, Bingham SA (2003) Haem, not protein or inorganic iron, is responsible for endogenous intestinal N-nitrosation arising from red meat. Cancer Res 63(10):2358–2360
Cross AJ, Freedman ND, Ren J, Ward MH, Hollenbeck AR, Schatzkin A, Sinha R, Abnet CC (2011) Meat consumption and risk of esophageal and gastric cancer in a large prospective study. Am J Gastroenterol 106(3):432–442. doi:10.1038/ajg.2010.415
Daniel CR, Cross AJ, Koebnick C, Sinha R (2011) Trends in meat consumption in the USA. Public Health Nutr 14(4):575–583. doi:10.1017/s1368980010002077
De Stefani E, Correa P, Boffetta P, Deneo-Pellegrini H, Ronco AL, Mendilaharsu M (2004) Dietary patterns and risk of gastric cancer: a case-control study in Uruguay. Gastric Cancer 7(4):211–220. doi:10.1007/s10120-004-0295-2
DerSimonian R, Laird N (1986) Meta-analysis in clinical trials. Control Clin Trials 7(3):177–188
Duval S, Tweedie R (2000) Trim and fill: a simple funnel-plot-based method of testing and adjusting for publication bias in meta-analysis. Biometrics 56(2):455–463
Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM (2010) Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 127(12):2893–2917. doi:10.1002/ijc.25516
Fund WCR, Research AIfC (2007) Food, nutrition, physical activity, and the prevention of cancer: a global perspective. American Institute for Cancer Research
Gao Y, Hu N, Han XY, Ding T, Giffen C, Goldstein AM, Taylor PR (2011) Risk factors for esophageal and gastric cancers in Shanxi Province, China: a case–control study. Cancer Epidemiol 35(6):e91–e99. doi:10.1016/j.canep.2011.06.006
González CA, Jakszyn P, Pera G, Agudo A, Bingham S, Palli D, Ferrari P, Boeing H, del Giudice G, Plebani M, Carneiro F, Nesi G, Berrino F, Sacerdote C, Tumino R, Panico S, Berglund G, Simán H, Nyrén O, Hallmans G, Martinez C, Dorronsoro M, Barricarte A, Navarro C, Quirós JR, Allen N, Key TJ, Day NE, Linseisen J, Nagel G, Bergmann MM, Overvad K, Jensen MK, Tjonneland A, Olsen A, Bueno-de-Mesquita HB, Ocke M, Peeters PH, Numans ME, Clavel-Chapelon F, Boutron-Ruault MC, Trichopoulou A, Psaltopoulou T, Roukos D, Lund E, Hemon B, Kaaks R, Norat T, Riboli E (2006) Meat intake and risk of stomach and esophageal adenocarcinoma within the European Prospective Investigation Into Cancer and Nutrition (EPIC). J Natl Cancer Inst 98(5):345–354. doi:10.1093/jnci/djj071
Greenland S (1987) Quantitative methods in the review of epidemiologic literature. Epidemiol Rev 9:1–30
Greenland S, Longnecker MP (1992) Methods for trend estimation from summarized dose-response data, with applications to meta-analysis. Am J Epidemiol 135(11):1301–1309
Grulich AE, Vajdic CM, Falster MO, Kane E, Smedby KE, Bracci PM, de Sanjose S, Becker N, Turner J, Martinez-Maza O, Melbye M, Engels EA, Vineis P, Costantini AS, Holly EA, Spinelli JJ, La Vecchia C, Zheng T, Chiu BC, Franceschi S, Cocco P, Maynadie M, Foretova L, Staines A, Brennan P, Davis S, Severson RK, Cerhan JR, Breen EC, Birmann B, Cozen W (2010) Birth order and risk of non-hodgkin lymphoma–true association or bias? Am J Epidemiol 172(6):621–630. doi:10.1093/aje/kwq167
Hu J, La Vecchia C, DesMeules M, Negri E, Mery L (2008) Meat and fish consumption and cancer in Canada. Nutr Cancer 60(3):313–324. doi:10.1080/01635580701759724
Jakszyn P, Bingham S, Pera G, Agudo A, Luben R, Welch A, Boeing H, Del Giudice G, Palli D, Saieva C, Krogh V, Sacerdote C, Tumino R, Panico S, Berglund G, Siman H, Hallmans G, Sanchez MJ, Larranaga N, Barricarte A, Chirlaque MD, Quiros JR, Key TJ, Allen N, Lund E, Carneiro F, Linseisen J, Nagel G, Overvad K, Tjonneland A, Olsen A, Bueno-de-Mesquita HB, Ocke MO, Peeters PH, Numans ME, Clavel-Chapelon F, Trichopoulou A, Fenger C, Stenling R, Ferrari P, Jenab M, Norat T, Riboli E, Gonzalez CA (2006) Endogenous versus exogenous exposure to N-nitroso compounds and gastric cancer risk in the European Prospective Investigation into Cancer and Nutrition (EPIC-EURGAST) study. Carcinogenesis 27(7):1497–1501. doi:10.1093/carcin/bgl019
Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D (2011) Global cancer statistics. CA Cancer J Clin 61(2):69–90. doi:10.3322/caac.20107
Ji BT, Chow WH, Yang G, McLaughlin JK, Zheng W, Shu XO, Jin F, Gao RN, Gao YT, Fraumeni JF Jr (1998) Dietary habits and stomach cancer in Shanghai, China. Int J Cancer 76(5):659–664
Keszei AP, Schouten LJ, Goldbohm RA, van den Brandt PA (2012) Red and processed meat consumption and the risk of esophageal and gastric cancer subtypes in The Netherlands Cohort Study. Ann Oncol 23(9):2319–2326. doi:10.1093/annonc/mdr615
Kim HJ, Chang WK, Kim MK, Lee SS, Choi BY (2002) Dietary factors and gastric cancer in Korea: a case–control study. Int J Cancer 97(4):531–535
Larsson SC, Wolk A (2012) Red and processed meat consumption and risk of pancreatic cancer: meta-analysis of prospective studies. Br J Cancer 106(3):603–607. doi:10.1038/bjc.2011.585
Larsson SC, Bergkvist L, Wolk A (2006) Processed meat consumption, dietary nitrosamines and stomach cancer risk in a cohort of Swedish women. Int J Cancer 119(4):915–919. doi:10.1002/ijc.21925
Lewin MH, Bailey N, Bandaletova T, Bowman R, Cross AJ, Pollock J, Shuker DE, Bingham SA (2006) Red meat enhances the colonic formation of the DNA adduct O6-carboxymethyl guanine: implications for colorectal cancer risk. Cancer Res 66(3):1859–1865. doi:10.1158/0008-5472.can-05-2237
Lissowska J, Gail MH, Pee D, Groves FD, Sobin LH, Nasierowska-Guttmejer A, Sygnowska E, Zatonski W, Blot WJ, Chow WH (2004) Diet and stomach cancer risk in Warsaw, Poland. Nutr Cancer 48(2):149–159. doi:10.1207/s15327914nc4802_4
McNeill S, Van Elswyk ME (2012) Red meat in global nutrition. Meat Sci 92(3):166–173. doi:10.1016/j.meatsci.2012.03.014
Mirvish SS (1995) Role of N-nitroso compounds (NOC) and N-nitrosation in etiology of gastric, esophageal, nasopharyngeal and bladder cancer and contribution to cancer of known exposures to NOC. Cancer Lett 93(1):17–48. doi:10.1016/0304-3835(95)03786-v
Muñoz SE, Ferraroni M, La Vecchia C, Decarli A (1997) Gastric cancer risk factors in subjects with family history. Cancer Epidemiol Biomarkers Prev 6(2):137–140
Palli D, Russo A, Ottini L, Masala G, Saieva C, Amorosi A, Cama A, D’Amico C, Falchetti M, Palmirotta R, Decarli A, Mariani Costantini R, Fraumeni JF Jr (2001) Red meat, family history, and increased risk of gastric cancer with microsatellite instability. Cancer Res 61(14):5415–5419
Perez-Perez GI, Israel DA (2000) Role of iron in Helicobacter pylori: its influence in outer membrane protein expression and in pathogenicity. Eur J Gastroenterol Hepatol 12(12):1263–1265
Pourfarzi F, Whelan A, Kaldor J, Malekzadeh R (2009) The role of diet and other environmental factors in the causation of gastric cancer in Iran–a population based study. Int J Cancer 125(8):1953–1960. doi:10.1002/ijc.24499
Royston P (2000) A strategy for modelling the effect of a continuous covariate in medicine and epidemiology. Stat Med 19(14):1831–1847
Santarelli RL, Pierre F, Corpet DE (2008) Processed meat and colorectal cancer: a review of epidemiologic and experimental evidence. Nutr Cancer 60(2):131–144. doi:10.1080/01635580701684872
Skog KI, Johansson MA, Jagerstad MI (1998) Carcinogenic heterocyclic amines in model systems and cooked foods: a review on formation, occurrence and intake. Food Chem Toxicol 36(9–10):879–896
Stang A (2010) Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol 25(9):603–605. doi:10.1007/s10654-010-9491-z
Suzuki H, Iwasaki E, Hibi T (2009) Helicobacter pylori and gastric cancer. Gastric Cancer 12(2):79–87. doi:10.1007/s10120-009-0507-x
Tavani A, La Vecchia C, Gallus S, Lagiou P, Trichopoulos D, Levi F, Negri E (2000) Red meat intake and cancer risk: a study in Italy. Int J Cancer 86(3):425–428
Ward MH, Sinha R, Heineman EF, Rothman N, Markin R, Weisenburger DD, Correa P, Zahm SH (1997) Risk of adenocarcinoma of the stomach and esophagus with meat cooking method and doneness preference. Int J Cancer 71(1):14–19
Wu AH, Tseng CC, Hankin J, Bernstein L (2007) Fiber intake and risk of adenocarcinomas of the esophagus and stomach. Cancer Causes Control 18(7):713–722. doi:10.1007/s10552-007-9014-8
Xu X, Yu E, Gao X, Song N, Liu L, Wei X, Zhang W, Fu C (2013) Red and processed meat intake and risk of colorectal adenomas: a meta-analysis of observational studies. Int J Cancer 132(2):437–448. doi:10.1002/ijc.27625
Zamani N, Hajifaraji M, Fazel-tabar Malekshah A, Keshtkar AA, Esmaillzadeh A, Malekzadeh R (2013) A case–control study of the relationship between gastric cancer and meat consumption in Iran. Arch Iran Med 16(6):324–329. doi:http://www.ncbi.nlm.nih.gov/pubmed/23725064
Zhang ZF, Kurtz RC, Yu GP, Sun M, Gargon N, Karpeh M Jr, Fein JS, Harlap S (1997) Adenocarcinomas of the esophagus and gastric cardia: the role of diet. Nutr Cancer 27(3):298–309. doi:10.1080/01635589709514541
Zhou Y, Du WD, Chen G, Ruan J, Xu S, Zhou FS, Zuo XB, Lv ZJ, Zhang XJ (2012) Association analysis of genetic variants in microRNA networks and gastric cancer risk in a Chinese Han population. J Cancer Res Clin Oncol 138(6):939–945. doi:10.1007/s00432-012-1164-8
Zhu H, Yang X, Zhang C, Zhu C, Tao G, Zhao L, Tang S, Shu Z, Cai J, Dai S, Qin Q, Xu L, Cheng H, Sun X (2013) Red and processed meat intake is associated with higher gastric cancer risk: a meta-analysis of epidemiological observational studies. PLoS ONE 8(8):e70955. doi:10.1371/journal.pone.0070955
Acknowledgments
P. S. and Q. Z. designed research; P. S. and M. L. performed research; P. S., Q. Z., Q. Y., L. W. analyzed data; P. S., Q. Z., L. W., D. Z., B. F., B. W. wrote the draft; all authors read, reviewed and approved the final manuscript. Q. Z. had primary responsibility for final content. We thank Zhizhong Zhang (Department of Neurology, Jinling Hospital, Nanjing University School of Medicine, Jiangsu Province, China) for critical reviewing and language editing the manuscript.
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The authors have declared that no competing interests exist.
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Peng Song, Ming Lu, Qin Yin have contributed equally to this work.
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Song, P., Lu, M., Yin, Q. et al. Red meat consumption and stomach cancer risk: a meta-analysis. J Cancer Res Clin Oncol 140, 979–992 (2014). https://doi.org/10.1007/s00432-014-1637-z
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DOI: https://doi.org/10.1007/s00432-014-1637-z