Skip to main content
Log in

Dose–response meta-analysis of poultry intake and colorectal cancer incidence and mortality

  • Original Contribution
  • Published:
European Journal of Nutrition Aims and scope Submit manuscript

Abstract

Purpose

Poultry intake has been inconsistently associated with incidence or mortality of colorectal cancer (CRC) in epidemiologic studies. The purpose of this study was to assess their relationships by performing a dose–response meta-analysis.

Methods

We conducted a search of PubMed database between January 1966 and July 2013 for prospective studies that reported relative risks (RRs) with 95 % confidence interval (CIs) of CRC for at least three categories of poultry intake. Dose–response relationships were examined with the generalized least-squares trend estimation. Study-specific results were pooled with a random-effects model. Subgroup, sensitivity, and meta-regression analyses were also conducted to explore heterogeneity.

Results

Sixteen studies on poultry intake and CRC incidence, and four studies regarding poultry intake and CRC mortality were identified. These studies involved a total of 13,949 incident CRC cases and 983 CRC deaths. The RRs of CRC for higher compared with lower intake of poultry were reported in these studies, and the reported levels of poultry intake varied substantially. Results of the dose–response meta-analysis conferred a RR of 0.89 (95 % CI 0.81–0.97) for an increase in poultry intake of 50 g/day. The results were not sensitive to any individual studies and were similar for colon and rectal cancer. Poultry intake was not associated with CRC mortality (RR for 50 g/day = 0.97, 95 % CI 0.79–1.20).

Conclusions

This meta-analysis indicates that poultry intake may be moderately associated with reduced incidence of CRC.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D (2011) Global cancer statistics. CA Cancer J Clin 61:69–90

    Article  Google Scholar 

  2. Doll R, Peto R (1981) The causes of cancer: quantitative estimates of avoidable risks of cancer in the United States today. J Natl Cancer Inst 66:1192–1308

    Google Scholar 

  3. Boyle P, Zaiudze D, Smans M (1985) Descriptive epidemiology of colorectal cancer. Int J Cancer 36:9–18

    Article  CAS  Google Scholar 

  4. World Cancer Research Fund/American Institute for Cancer Research (2007) Food, nutrition, physical activity, and the prevention of cancer: a global perspective. WCRF/AICR, Washington

    Google Scholar 

  5. Chan DS, Lau R, Aune D, Vieira R, Greenwood DC, Kampman E, Norat T (2011) Red and processed meat and colorectal cancer incidence: meta-analysis of prospective studies. PLoS ONE 6:e20456

    Article  CAS  Google Scholar 

  6. Bostick RM, Potter JD, Kushi LH, Sellers TA, Steinmetz KA, McKenzie DR, Gapstur SM, Folsom AR (1994) Sugar, meat, and fat intake, and non-dietary risk factors for colon cancer incidence in Iowa women (United States). Cancer Causes Control 5:38–52

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  8. Egeberg R, Olsen A, Christensen J, Halkjær J, Jakobsen MU, Overvad K, Tjønneland A (2013) Associations between red meat and risks for colon and rectal cancer depend on the type of red meat consumed. J Nutr 143:464–472

    Article  CAS  Google Scholar 

  9. English DR, MacInnis RJ, Hodge AM, Hopper JL, Haydon AM, Giles GG (2004) Red meat, chicken, and fish consumption and risk of colorectal cancer. Cancer Epidemiol Biomarkers Prev 13:1509–1514

    Google Scholar 

  10. Giovannucci E, Rimm EB, Stampfer MJ, Colditz GA, Ascherio A, Willett WC (1994) Intake of fat, meat, and fiber in relation to risk of colon cancer in men. Cancer Res 54:2390–2397

    CAS  Google Scholar 

  11. Kato I, Akhmedkhanov A, Koenig K, Toniolo PG, Shore RE, Riboli E (1997) Prospective study of diet and female colorectal cancer: the New York University Women’s Health Study. Nutr Cancer 28:276–281

    Article  CAS  Google Scholar 

  12. Larsson SC, Rafter J, Holmberg L, Bergkvist L, Wolk A (2005) Red meat consumption and risk of cancers of the proximal colon, distal colon and rectum: the Swedish Mammography Cohort. Int J Cancer 113:829–834

    Article  CAS  Google Scholar 

  13. Lüchtenborg M, Weijenberg MP, de Goeij AF, Wark PA, Brink M, Roemen GM, Lentjes MH, de Bruïne AP, Goldbohm RA, van‘t Veer P (2005) Meat and fish consumption, APCGene mutations and hMLH1 expression in colon and rectal cancer: a prospective cohort study (The Netherlands). Cancer Causes Control 16:1041–1054

    Article  Google Scholar 

  14. Ma J, Giovannucci E, Pollak M, Chan JM, Gaziano JM, Willett W, Stampfer MJ (2001) Milk intake, circulating levels of insulin-like growth factor-I, and risk of colorectal cancer in men. J Natl Cancer Inst 93:1330–1336

    Article  CAS  Google Scholar 

  15. Norat T, Bingham S, Ferrari P, Slimani N, Jenab M, Mazuir M, Overvad K, Olsen A, Tjønneland A, Clavel F (2005) Meat, fish, and colorectal cancer risk: the European prospective investigation into cancer and nutrition. J Natl Cancer Inst 97:906–916

    Article  Google Scholar 

  16. Parr CL, Hjartåker A, Lund E, Veierød MB (2013) Meat intake, cooking methods and risk of proximal colon, distal colon and rectal cancer: the Norwegian Women and Cancer (NOWAC) cohort study. Int J Cancer 133:1153–1163

    Article  CAS  Google Scholar 

  17. Pietinen P, Malila N, Virtanen M, Hartman TJ, Tangrea JA, Albanes D, Virtamo J (1999) Diet and risk of colorectal cancer in a cohort of Finnish men. Cancer Causes Control 10:387–396

    Article  CAS  Google Scholar 

  18. Sato Y, Nakaya N, Kuriyama S, Nishino Y, Tsubono Y, Tsuji I (2006) Meat consumption and risk of colorectal cancer in Japan: the Miyagi Cohort Study. Eur J Cancer Prev 15:211–218

    Article  Google Scholar 

  19. Spencer EA, Key TJ, Appleby PN, Dahm CC, Keogh RH, Fentiman IS, Akbaraly T, Brunner EJ, Burley V, Cade JE (2010) Meat, poultry and fish and risk of colorectal cancer: pooled analysis of data from the UK dietary cohort consortium. Cancer Causes Control 21:1417–1425

    Article  Google Scholar 

  20. Tiemersma EW, Kampman E, de Mesquita HBB, Bunschoten A, van Schothorst EM, Kok FJ, Kromhout D (2002) Meat consumption, cigarette smoking, and genetic susceptibility in the etiology of colorectal cancer: results from a Dutch prospective study. Cancer Causes Control 13:383–393

    Article  Google Scholar 

  21. Willett WC, Stampfer MJ, Colditz GA, Rosner BA, Speizer FE (1990) Relation of meat, fat, and fiber intake to the risk of colon cancer in a prospective study among women. N Engl J Med 323:1664–1672

    Article  CAS  Google Scholar 

  22. Hsing AW, McLaughlin JK, Chow WH, Schuman LM, Co Chien HT, Gridley G, Bjelke E, Wacholder S, Blot WJ (1998) Risk factors for colorectal cancer in a prospective study among US white men. Int J Cancer 77:549–553

    Article  CAS  Google Scholar 

  23. Kojima M, Wakai K, Tamakoshi K, Tokudome S, Toyoshima H, Watanabe Y, Hayakawa N, Suzuki K, Hashimoto S, Ito Y (2004) Diet and colorectal cancer mortality: results from the Japan Collaborative Cohort Study. Nutr Cancer 50:23–32

    Article  Google Scholar 

  24. Takata Y, Shu X-O, Gao Y-T, Li H, Zhang X, Gao J, Cai H, Yang G, Xiang Y-B, Zheng W (2013) Red meat and poultry intakes and risk of total and cause-specific mortality: results from cohort studies of Chinese adults in Shanghai. PLoS ONE 8:e56963

    Article  CAS  Google Scholar 

  25. Donaldson MS (2004) Nutrition and cancer: a review of the evidence for an anti-cancer diet. Nutr J 3:19

    Article  Google Scholar 

  26. 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

    CAS  Google Scholar 

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

    Google Scholar 

  28. Bandera EV, Kushi LH, Moore DF, Gifkins DM, McCullough ML (2007) Consumption of animal foods and endometrial cancer risk: a systematic literature review and meta-analysis. Cancer Causes Control 18:967–988

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  30. 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  Google Scholar 

  31. Higgins JP, Thompson SG (2002) Quantifying heterogeneity in a meta-analysis. Stata Med 21:1539–1558

    Article  Google Scholar 

  32. 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  Google Scholar 

  33. Goldbohm RA, van den Brandt PA, van’t Veer P, Brants HA, Dorant E, Sturmans F, Hermus RJ (1994) A prospective cohort study on the relation between meat consumption and the risk of colon cancer. Cancer Res 54:718–723

    CAS  Google Scholar 

  34. Järvinen R, Knekt P, Hakulinen T, Rissanen H, Heliövaara M (2001) Dietary fat, cholesterol and colorectal cancer in a prospective study. Br J Cancer 85:357

    Article  Google Scholar 

  35. Flood A, Rastogi T, Wirfält E, Mitrou PN, Reedy J, Subar AF, Kipnis V, Mouw T, Hollenbeck AR, Leitzmann M (2008) Dietary patterns as identified by factor analysis and colorectal cancer among middle-aged Americans. Am J Clin Nutr 88:176–184

    CAS  Google Scholar 

  36. Xu B, Sun J, Sun Y, Huang L, Tang Y, Yuan Y (2013) No evidence of decreased risk of colorectal adenomas with white meat, poultry, and fish intake: a meta-analysis of observational studies. Ann Epidemiol 23:215–222

    Article  Google Scholar 

  37. Nimptsch K, Bernstein AM, Giovannucci E, Fuchs CS, Willett WC, Wu K (2013) Dietary intakes of red meat, poultry, and fish during high school and risk of colorectal adenomas in women. Am J Epidemiol 178:172–183

    Article  Google Scholar 

  38. Bingham SA, Hughes R, Cross AJ (2002) Effect of white versus red meat on endogenous N-nitrosation in the human colon and further evidence of a dose response. J Nutr 132:3522S–3525S

    CAS  Google Scholar 

  39. Bastide NM, Pierre FH, Corpet DE (2011) Heme iron from meat and risk of colorectal cancer: a meta-analysis and a review of the mechanisms involved. Cancer Prev Res (Phila) 4:177–184

    Article  CAS  Google Scholar 

  40. Wei EK, Giovannucci E, Wu K, Rosner B, Fuchs CS, Willett WC, Colditz GA (2004) Comparison of risk factors for colon and rectal cancer. Int J Cancer 108:433–442

    Article  CAS  Google Scholar 

  41. Lev R (1990) Adenomatous polyps of the colon. Springer, New York

    Book  Google Scholar 

Download references

Conflict of interest

None.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dong-Zhu Zeng.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 19 kb)

Supplementary material 2 (DOCX 14 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shi, Y., Yu, PW. & Zeng, DZ. Dose–response meta-analysis of poultry intake and colorectal cancer incidence and mortality. Eur J Nutr 54, 243–250 (2015). https://doi.org/10.1007/s00394-014-0705-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00394-014-0705-0

Keywords

Navigation