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The association between red, processed and white meat consumption and risk of pancreatic cancer: a meta-analysis of prospective cohort studies

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Abstract

Purpose

The association between meat consumption and the risk of pancreatic cancer has not been comprehensively investigated by different types of meat. The current study was conducted to evaluate this association.

Methods

PubMed and Web of Science databases were used to search for prospective cohort studies on meat consumption and pancreatic cancer risk through May 2022. A meta-analysis was performed using random-effects models to combine study-specific relative risks (RR). The quality of the included studies was evaluated using the Newcastle–Ottawa quality assessment scale.

Results

Twenty prospective cohort studies including 3,934,909 participants and 11,315 pancreatic cancer cases were identified. The pooled RR of pancreatic cancer for the highest versus lowest white meat intake category was 1.14 (95% CI: 1.03–1.27). There was no significant association between consumption of red meat and processed meat and pancreatic cancer risk in the highest versus lowest analysis. In dose–response analyses, pooled RRs were 1.14 (95% CI: 1.01–1.28) for an increase in red meat consumption of 120 g per day and 1.26 (95% CI: 1.08–1.47) for an increase in white meat consumption of 100 g per day, respectively. Processed meat consumption showed neither a linear nor a non-linear association with pancreatic cancer risk.

Conclusion

Findings from this meta-analysis suggested that high consumption of red meat and white meat is associated with an increased risk of pancreatic cancer. Future prospective studies are warranted to confirm the association between meat consumption and the risk of pancreatic cancer.

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References

  1. Sung H, Ferlay J, Siegel RL et al (2021) Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 71:209–249

    Article  PubMed  Google Scholar 

  2. Ward EM, Sherman RL, Henley SJ et al (2019) Annual report to the nation on the status of cancer, featuring cancer in men and women age 20–49 years. J Natl Cancer Inst 111:1279–1297

    Article  PubMed  PubMed Central  Google Scholar 

  3. WCRF/AICR. (2018) Diet, Nutrition, Physical Activity and cancer: a Global Perspective. Continous Update Project Expert Report 2018. World Cancer Research Fund/American Institute for Cancer Researsh.

  4. Siegel RL, Miller KD, Jemal A (2020) Cancer statistics, 2020. CA Cancer J Clin 70:7–30

    Article  PubMed  Google Scholar 

  5. Stolzenberg-Solomon RZ, Pietinen P, Taylor PR, Virtamo J, Albanes D (2002) Prospective study of diet and pancreatic cancer in male smokers. Am J Epidemiol 155:783–792

    Article  PubMed  Google Scholar 

  6. Michaud DS, Giovannucci E, Willett WC, Colditz GA, Fuchs CS (2003) Dietary meat, dairy products, fat, and cholesterol and pancreatic cancer risk in a prospective study. Am J Epidemiol 157:1115–1125

    Article  PubMed  Google Scholar 

  7. Nöthlings U, Wilkens LR, Murphy SP, Hankin JH, Henderson BE, Kolonel LN (2005) Meat and fat intake as risk factors for pancreatic cancer: the multiethnic cohort study. J Natl Cancer Inst 97:1458–1465

    Article  PubMed  Google Scholar 

  8. Lin Y, Kikuchi S, Tamakoshi A et al (2006) Dietary habits and pancreatic cancer risk in a cohort of middle-aged and elderly Japanese. Nutr Cancer 56:40–49

    Article  PubMed  Google Scholar 

  9. Heinen MM, Verhage BA, Goldbohm RA, van den Brandt PA (2009) Meat and fat intake and pancreatic cancer risk in the Netherlands cohort study. Int J Cancer 125:1118–1126

    Article  CAS  PubMed  Google Scholar 

  10. Inoue-Choi M, Flood A, Robien K, Anderson K (2011) Nutrients, food groups, dietary patterns, and risk of pancreatic cancer in postmenopausal women. Cancer Epidemiol Biomarkers Prev 20:711–714

    Article  PubMed  PubMed Central  Google Scholar 

  11. Anderson KE, Mongin SJ, Sinha R et al (2012) Pancreatic cancer risk: associations with meat-derived carcinogen intake in the Prostate, Lung, Colorectal, and Ovarian Cancer Screening Trial (PLCO) cohort. Mol Carcinog 51:128–137

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Ghorbani Z, Pourshams A, Fazeltabar Malekshah A, Sharafkhah M, Poustchi H, Hekmatdoost A (2016) Major dietary protein sources in relation to pancreatic cancer: a large prospective study. Arch Iran Med 19:248–256

    PubMed  Google Scholar 

  13. Taunk P, Hecht E, Stolzenberg-Solomon R (2016) Are meat and heme iron intake associated with pancreatic cancer? Results from the NIH-AARP diet and health cohort. Int J Cancer 138:2172–2189

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. McCullough ML, Jacobs EJ, Shah R et al (2018) Meat consumption and pancreatic cancer risk among men and women in the cancer prevention study-ii nutrition cohort. Cancer causes & control : CCC 29:125–133

    Article  PubMed  Google Scholar 

  15. Knuppel A, Papier K, Fensom GK et al (2020) Meat intake and cancer risk: prospective analyses in UK Biobank. Int J Epidemiol 49:1540–1552

    Article  PubMed  Google Scholar 

  16. Petrick JL, Castro-Webb N, Gerlovin H et al (2020) A prospective analysis of intake of red and processed meat in relation to pancreatic cancer among African American women. Cancer Epidemiol Biomarkers Prev 29:1775–1783

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Zheng W, McLaughlin JK, Gridley G et al (1993) A cohort study of smoking, alcohol consumption, and dietary factors for pancreatic cancer (United States). Cancer causes & control 4:477–482

    Article  CAS  Google Scholar 

  18. Coughlin SS, Calle EE, Patel AV, Thun MJ (2000) Predictors of pancreatic cancer mortality among a large cohort of United States adults. Cancer causes & control 11:915–923

    Article  CAS  Google Scholar 

  19. Isaksson B, Jonsson F, Pedersen NL, Larsson J, Feychting M, Permert J (2002) Lifestyle factors and pancreatic cancer risk: a cohort study from the Swedish Twin Registry. Int J Cancer 98:480–482

    Article  CAS  PubMed  Google Scholar 

  20. Khan MM, Goto R, Kobayashi K et al (2004) Dietary habits and cancer mortality among middle aged and older Japanese living in hokkaido, Japan by cancer site and sex. Asian Pacific J cancer prevent 5:58–65

    CAS  Google Scholar 

  21. Huang BZ, Wang SR, Bogumil D et al (2021) Red meat consumption, cooking mutagens, NAT1/2 genotypes and pancreatic cancer risk in two ethnically diverse prospective cohorts. Int J Cancer 149:811–819

    Article  CAS  Google Scholar 

  22. Pang YJ, Holmes MV, Guo Y et al (2018) Smoking, alcohol, and diet in relation to risk of pancreatic cancer in China: a prospective study of 0.5 million people. Cancer Med 7:229–239

    Article  PubMed  Google Scholar 

  23. Rohrmann S, Linseisen J, Nöthlings U et al (2013) Meat and fish consumption and risk of pancreatic cancer: results from the European prospective investigation into cancer and nutrition. Int J Cancer 132:617–624

    Article  CAS  PubMed  Google Scholar 

  24. Larsson SC, Håkanson N, Permert J, Wolk A (2006) Meat, fish, poultry and egg consumption in relation to risk of pancreatic cancer: a prospective study. Int J Cancer 118:2866–2870

    Article  CAS  PubMed  Google Scholar 

  25. Larsson SC, Hakanson N, Permert J, Wolk A (2006) Meat, fish, poultry and egg consumption in relation to risk of pancreatic cancer: a prospective study. Int J Cancer 118:2866–2870

    Article  CAS  PubMed  Google Scholar 

  26. Rohrmann S, Linseisen J, Nothlings U et al (2013) Meat and fish consumption and risk of pancreatic cancer: results from the European prospective investigation into cancer and nutrition. Int J Cancer 132:617–624

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Zhao Z, Yin Z, Pu Z, Zhao Q (2017) Association between consumption of red and processed meat and pancreatic cancer risk: a systematic review and meta-analysis. Clin Gastroenterol Hepatol 15:486-493.e410

    Article  PubMed  Google Scholar 

  29. Gao Y, Ma Y, Yu M et al (2021) Poultry and fish intake and pancreatic cancer risk: a systematic review and meta-analysis. Nutr Cancer 74:1–13

    Google Scholar 

  30. Zhao ZW, Yin ZF, Pu ZS, Zhao QC (2017) Association between consumption of red and processed meat and pancreatic cancer risk: a systematic review and meta-analysis. Clin Gastroenterol Hepatol 15:486

    Article  PubMed  Google Scholar 

  31. Moher D, Liberati A, Tetzlaff J, Altman DG, Group P (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS med 6:e1000097

    Article  PubMed  PubMed Central  Google Scholar 

  32. Wells GA SB, O’Connell D. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomized studies in meta-analysis. http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp.

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

    Article  CAS  PubMed  Google Scholar 

  34. Greenland S, Longnecker MP (1992) Methods for trend estimation from summarized dose-response data, with applications to meta-analysis. Am J Epidemiol 135:1301–1309

    Article  CAS  PubMed  Google Scholar 

  35. Berlin JA, Longnecker MP, Greenland S (1993) Meta-analysis of epidemiologic dose-response data. Epidemiology 4:218–228

    Article  CAS  PubMed  Google Scholar 

  36. Orsini N, Bellocco R, Greenland S (2006) Generalized least squares for trend estimation of summarized dose-response data. Stata J 6:40–57

    Article  Google Scholar 

  37. Norat T, Lukanova A, Ferrari P, Riboli E (2002) Meat consumption and colorectal cancer risk: an estimate of attributable and preventable fractions. IARC Sci Publ 156:223–225

    CAS  PubMed  Google Scholar 

  38. Shi Y, Yu PW, Zeng DZ (2015) Dose-response meta-analysis of poultry intake and colorectal cancer incidence and mortality. Eur J Nutr 54:243–250

    Article  CAS  PubMed  Google Scholar 

  39. Orsini N, Li R, Wolk A, Khudyakov P, Spiegelman D (2012) Meta-analysis for linear and nonlinear dose-response relations: examples, an evaluation of approximations, and software. Am J Epidemiol 175:66–73

    Article  PubMed  Google Scholar 

  40. Cochran WG (1954) The combination of estimates from different experiments. Biometrics 10:101–129

    Article  Google Scholar 

  41. Higgins JP, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analyses. BMJ 327:557–560

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Farvid MS, Sidahmed E, Spence ND, Mante Angua K, Rosner BA, Barnett JB (2021) Consumption of red meat and processed meat and cancer incidence: a systematic review and meta-analysis of prospective studies. Eur J Epidemiol 36:937–951

    Article  PubMed  Google Scholar 

  45. Bouvard V, Loomis D, Guyton KZ et al (2015) Carcinogenicity of consumption of red and processed meat. Lancet Oncol 16:1599–1600

    Article  PubMed  Google Scholar 

  46. Stolzenberg-Solomon RZ, Cross AJ, Silverman DT et al (2007) Meat and meat-mutagen intake and pancreatic cancer risk in the NIH-AARP cohort. Cancer Epidemiol Biomarkers Prev 16:2664–2675

    Article  CAS  PubMed  Google Scholar 

  47. Friedman GD, van den Eeden SK (1993) Risk factors for pancreatic cancer: an exploratory study. Int J Epidemiol 22:30–37

    Article  CAS  PubMed  Google Scholar 

  48. Miller PE, Van Elswyk M, Alexander DD (2014) Long-chain omega-3 fatty acids eicosapentaenoic acid and docosahexaenoic acid and blood pressure: a meta-analysis of randomized controlled trials. Am J Hypertens 27:885–896

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Mozaffarian D, Wu JH (2011) Omega-3 fatty acids and cardiovascular disease: effects on risk factors, molecular pathways, and clinical events. J Am Coll Cardiol 58:2047–2067

    Article  CAS  PubMed  Google Scholar 

  50. Konkel L (2016) Organoarsenic drugs over time: the pharmacokinetics of roxarsone in chicken meat. Environ Health Perspect 124:A150

    Article  PubMed  PubMed Central  Google Scholar 

  51. Nachman KE, Baron PA, Raber G, Francesconi KA, Navas-Acien A, Love DC (2013) Roxarsone, inorganic arsenic, and other arsenic species in chicken: a U.S.-based market basket sample. Environ Health Perspect 121:818–824

    Article  PubMed  PubMed Central  Google Scholar 

  52. Nigra AE, Nachman KE, Love DC, Grau-Perez M, Navas-Acien A (2017) Poultry consumption and arsenic exposure in the U.S. Population Environ Health Perspect 125:370–377

    Article  CAS  PubMed  Google Scholar 

  53. Humans IWGotEoCRt (2012) Arsenic, metals, fibres, and dusts. IARC Monogr Eval Carcinog Risks Hum 100:11–465

    Google Scholar 

  54. Liu-Mares W, Mackinnon JA, Sherman R et al (2013) Pancreatic cancer clusters and arsenic-contaminated drinking water wells in Florida. BMC Cancer 13:111

    Article  PubMed  PubMed Central  Google Scholar 

  55. Adeva MM, Souto G (2011) Diet-induced metabolic acidosis. Clin Nutr 30:416–421

    Article  CAS  PubMed  Google Scholar 

  56. Espino L, Suarez ML, Santamarina G, Goicoa A, Fidalgo LE (2005) Effects of dietary cation-anion difference on blood cortisol and ACTH levels in reproducing ewes. J Vet Med A Physiol Pathol Clin Med 52:8–12

    Article  CAS  PubMed  Google Scholar 

  57. Rizza RA, Mandarino LJ, Gerich JE (1982) Cortisol-induced insulin resistance in man: impaired suppression of glucose production and stimulation of glucose utilization due to a postreceptor detect of insulin action. J Clin Endocrinol Metab 54:131–138

    Article  CAS  PubMed  Google Scholar 

  58. Robey IF (2012) Examining the relationship between diet-induced acidosis and cancer. Nutr Metab (Lond) 9:72

    Article  CAS  PubMed  Google Scholar 

  59. Thomas D, Radhakrishnan P (2020) Role of tumor and stroma-derived IGF/IGFBPs in pancreatic cancer. Cancers (Basel) 12:1228

    Article  CAS  PubMed  Google Scholar 

  60. Stolzenberg-Solomon RZ, Graubard BI, Chari S et al (2005) Insulin, glucose, insulin resistance, and pancreatic cancer in male smokers. JAMA 294:2872–2878

    Article  CAS  PubMed  Google Scholar 

  61. Disthabanchong S, Niticharoenpong K, Radinahamed P, Stitchantrakul W, Ongphiphadhanakul B, Hongeng S (2011) Metabolic acidosis lowers circulating adiponectin through inhibition of adiponectin gene transcription. Nephrol Dial Transplant 26:592–598

    Article  CAS  PubMed  Google Scholar 

  62. Hursting SD, Berger NA (2010) Energy balance, host-related factors, and cancer progression. J Clin Oncol 28:4058–4065

    Article  PubMed  PubMed Central  Google Scholar 

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YK: developed study concept and design and contributed to critical revision of the manuscript for important intellectual content; YK: wrote the manuscript; YK: researched data, conducted the statistical analysis; YK: contributed to discussion and reviewed/edited the manuscript.

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Correspondence to Youngyo Kim.

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Kim, Y. The association between red, processed and white meat consumption and risk of pancreatic cancer: a meta-analysis of prospective cohort studies. Cancer Causes Control 34, 569–581 (2023). https://doi.org/10.1007/s10552-023-01698-8

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