Skip to main content

Advertisement

SpringerLink
Log in

Consumption of animal foods and endometrial cancer risk: a systematic literature review and meta-analysis

  • Original Paper
  • Published:
Cancer Causes & Control Aims and scope Submit manuscript

Abstract

This article summarizes and quantifies the current evidence relating dietary intake of animal products and endometrial cancer. Literature searches were conducted to identify peer-reviewed manuscripts published up to December 2006. Twenty-two manuscripts from three cohort studies and 16 case–control studies were identified. One of these cohort studies evaluated only fried meat and another only milk consumption; they were not included in our meta-analyses. The third cohort study identified did not present exposure levels and could not be included in dose–response meta-analysis. This cohort study did not show an association with meat or red meat consumption. Random-effects dose–response summary estimates for case–control studies evaluating these foods were 1.26 (95% CI: 1.03–1.54) per 100 g/day of total meat, 1.51 (95% CI: 1.19–1.93) per 100 g/day of red meat, 1.03 (95% CI: 0.32–3.28) per 100 g/day of poultry, 1.04 (95% CI: 0.55–1.98) per 100 g/day of fish, and 0.97 (95% CI: 0.93–1.01) per serving of dairy. Our meta-analysis, based on case–control data, suggests that meat consumption, particularly red meat, increases endometrial cancer risk. The current literature does not support an association with dairy products, while the evidence is inconsistent for poultry, fish, and eggs. More studies, particularly prospective studies, are needed.

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

Access this article

Log in via an institution

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
Fig 5
Fig 6

Similar content being viewed by others

Abbreviations

WCRF:

World Cancer Research Fund International

AICR:

American Institute for Cancer Research

SLR:

Systematic Literature Review

OR:

Odds Ratio

RR:

Relative Risk

CI:

Confidence Interval

FFQ:

Food Frequency Questionnaire

BMI:

Body Mass Index

HRT:

Hormone Replacement Therapy

References

  1. American Cancer Society (2006) Cancer facts and figures

  2. Persson I, Adami H-O (2002) Endometrial cancer. In: Adami H-O, Hunter D, Trichopoulos D (eds) Textbook of cancer epidemiology. Oxford University Press, New York, NY

    Google Scholar 

  3. IARC (2002) Handbooks of cancer prevention, vol. 6. Weight control and physical activity. International Agency for Research on Cancer, World Health Organization, Lyon

  4. World Cancer Research Fund, American Institute for Cancer Research (1997) Food, nutrition and the prevention of cancer: a global perspective. American Cancer Institute for Cancer Research, Washington, DC

    Google Scholar 

  5. Larsson SC, Wolk A (2006) Meat consumption and risk of colorectal cancer: a meta-analysis of prospective studies. Int J Cancer 119:2657–2664

    Article  PubMed  CAS  Google Scholar 

  6. Daxenberger A, Ibarreta D, Meyer HH (2001) Possible health impact of animal oestrogens in food. Hum Reprod Update 7:340–355

    Article  PubMed  CAS  Google Scholar 

  7. Levi F, Franceschi S, Negri E, La Vecchia C (1993) Dietary factors and the risk of endometrial cancer. Cancer 71:3575–3581

    Article  PubMed  CAS  Google Scholar 

  8. La Vecchia C, Decarli A, Fasoli M, Gentile A (1986) Nutrition and diet in the etiology of endometrial cancer. Cancer 57:1248–1253

    Article  PubMed  Google Scholar 

  9. Shu XO, Zheng W, Potischman N et al (1993) A population-based case-control study of dietary factors and endometrial cancer in Shanghai, People’s Republic of China. Am J Epidemiol 137:155–165

    PubMed  CAS  Google Scholar 

  10. Bandera EV, Kushi LH, Moore DF, Gifkins DM, McCullough ML (2007) The association between food, nutrition, and physical activity and the risk of endometrial cancer and underlying mechanisms. In: Second Report on food, nutrition, physical activity and the prevention of cancer. World Cancer Research Fund International/American Institute for Cancer Research (In Press)

  11. Bandera EV, Kushi LH, Moore DF, Gifkins DM, McCullough ML (2007) Fruits and vegetables and endometrial cancer risk: a systematic literature review and meta-analysis. Nutr Cancer 58:6–21

    PubMed  Google Scholar 

  12. Armstrong B, Doll R (1975) Environmental factors and cancer incidence and mortality in different countries, with special reference to dietary practices. Int J Cancer 15:617–631

    Article  PubMed  CAS  Google Scholar 

  13. Ganmaa D, Sato A (2005) The possible role of female sex hormones in milk from pregnant cows in the development of breast, ovarian and corpus uteri cancers. Med Hypotheses 65:1028–1037

    Article  PubMed  CAS  Google Scholar 

  14. Tao MH, Xu WH, Zheng W et al (2005) A case-control study in Shanghai of fruit and vegetable intake and endometrial cancer. Br J Cancer 92:2059–2064

    Article  PubMed  CAS  Google Scholar 

  15. Lissner L, Kroon UB, Bjorntorp P, Blosk S, Wilhelmsen L, Silverstolpe G (1993) Adipose tissue fatty acids and dietary fat sources in relation to endometrial cancer: a retrospective study of cases in remission, and population-based controls. Acta Obstet Gynecol Scand 72:481–487

    PubMed  CAS  Google Scholar 

  16. Weiderpass E, Adami HO, Baron JA et al (2000) Organochlorines and endometrial cancer risk. Cancer Epidemiol Biomarkers Prev 9:487–493

    PubMed  CAS  Google Scholar 

  17. Kinlen LJ (1982) Meat and fat consumption and cancer mortality: a study of strict religious orders in Britain. Lancet 1:946–949

    Article  PubMed  CAS  Google Scholar 

  18. Zemla B, Guminski S, Banasik R (1986) Study of risk factors in invasive cancer of the corpus uteri. Neoplasma 33:621–629

    PubMed  CAS  Google Scholar 

  19. Zemla B, Guminski S, Franek K, Kolosza Z, Banasik R (1991) Etiological factors in invasive corpus uteri carcinoma. Neoplasma 38:157–163

    PubMed  CAS  Google Scholar 

  20. Terry P, Vainio H, Wolk A, Weiderpass E (2002) Dietary factors in relation to endometrial cancer: a nationwide case-control study in Sweden. Nutr Cancer 42:25–32

    Article  PubMed  Google Scholar 

  21. Terry P, Wolk A, Vainio H, Weiderpass E (2002) Fatty fish consumption lowers the risk of endometrial cancer: a nationwide case-control study in Sweden. Cancer Epidemiol Biomarkers Prev 11:143–145

    PubMed  Google Scholar 

  22. La Vecchia C, Decarli A, Negri E, Parazzini F (1988) Epidemiological aspects of diet and cancer: a summary review of case-control studies from northern Italy. Oncology 45:364–370

    PubMed  Google Scholar 

  23. Tavani A, La Vecchia C, Gallus S et al (2000) Red meat intake and cancer risk: a study in Italy. Int J Cancer 86:425–428

    Article  PubMed  CAS  Google Scholar 

  24. Fernandez E, Chatenoud L, La Vecchia C, Negri E, Franceschi S (1999) Fish consumption and cancer risk. Am J Clin Nutr 70:85–90

    PubMed  CAS  Google Scholar 

  25. Rothman KJ (1986) Modern epidemiology, 1st edn. Little, Brown, Boston, pp 174–175

    Google Scholar 

  26. Chene G, Thompson SG (1996) Methods for summarizing the risk associations of quantitative variables in epidemiologic studies in a consistent form. Am J Epidemiol 144:610–621

    PubMed  CAS  Google Scholar 

  27. 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

    PubMed  CAS  Google Scholar 

  28. Huedo-Medina TB, Sanchez-Meca J, Marin-Martinez F, Botella J (2006) Assessing heterogeneity in meta-analysis: Q statistic or I2 index? Psychol Methods 11:193–206

    Article  PubMed  Google Scholar 

  29. Ursin G, Bjelke E, Heuch I, Vollset SE (1990) Milk consumption and cancer incidence: a Norwegian prospective study. Br J Cancer 61:456–459

    PubMed  CAS  Google Scholar 

  30. Knekt P, Steineck G, Jarvinen R, Hakulinen T, Aromaa A (1994) Intake of fried meat and risk of cancer: a follow-up study in Finland. Int J Cancer 59:756–760

    Article  PubMed  CAS  Google Scholar 

  31. Zheng W, Kushi LH, Potter JD et al (1995) Dietary intake of energy and animal foods and endometrial cancer incidence. The Iowa Women’s Health Study. Am J Epidemiol 142:388–394

    PubMed  CAS  Google Scholar 

  32. Potischman N, Swanson CA, Brinton LA et al (1993) Dietary associations in a case-control study of endometrial cancer. Cancer Causes Control 4:239–250

    PubMed  CAS  Google Scholar 

  33. Goodman MT, Hankin JH, Wilkens LR et al (1997) Diet, body size, physical activity, and the risk of endometrial cancer. Cancer Res 57:5077–5085

    PubMed  CAS  Google Scholar 

  34. Jain MG, Howe GR, Rohan TE (2000) Nutritional factors and endometrial cancer in Ontario, Canada. Cancer Control 7:288–296

    PubMed  CAS  Google Scholar 

  35. McCann SE, Freudenheim JL, Marshall JR, Brasure JR, Swanson MK, Graham S (2000) Diet in the epidemiology of endometrial cancer in western New York (United States). Cancer Causes Control 11:965–974

    Article  PubMed  CAS  Google Scholar 

  36. Littman AJ, Beresford SA, White E (2001) The association of dietary fat and plant foods with endometrial cancer (United States). Cancer Causes Control 12:691–702

    Article  PubMed  CAS  Google Scholar 

  37. Xu WH, Dai Q, Xiang YB et al (2006) Animal food intake and cooking methods in relation to endometrial cancer risk in Shanghai. Br J Cancer 95:1568–1592

    Article  CAS  Google Scholar 

  38. Tzonou A, Lipworth L, Kalandidi A et al (1996) Dietary factors and the risk of endometrial cancer: a case–control study in Greece. Br J Cancer 73:1284–1290

    PubMed  CAS  Google Scholar 

  39. Mettlin CJ, Schoenfeld ER, Natarajan N (1990) Patterns of milk consumption and risk of cancer. Nutr Cancer 13:89–99

    Article  PubMed  CAS  Google Scholar 

  40. Barbone F, Austin H, Partridge EE (1993) Diet and endometrial cancer: a case-control study. Am J Epidemiol 137:393–403

    PubMed  CAS  Google Scholar 

  41. Hirose K, Tajima K, Hamajima N et al (1996) Subsite (cervix/endometrium)-specific risk and protective factors in uterus cancer. Jpn J Cancer Res 87:1001–1009

    PubMed  CAS  Google Scholar 

  42. Petridou E, Kedikoglou S, Koukoulomatis P, Dessypris N, Trichopoulos D (2002) Diet in relation to endometrial cancer risk: a case-control study in Greece. Nutr Cancer 44:16–22

    Article  PubMed  Google Scholar 

  43. Salazar-Martinez E, Lazcano-Ponce E, Sanchez-Zamorano LM, Gonzalez-Lira G, Escudero de los Rios P, Hernandez-Avila M (2005) Dietary factors and endometrial cancer risk. Results of a case-control study in Mexico. Int J Gynecol Cancer 15:938–945

    Article  PubMed  CAS  Google Scholar 

  44. Kushi LH, Byers T, Doyle C et al (2006) American Cancer Society guidelines on nutrition and physical activity for cancer prevention: reducing the risk of cancer with healthy food choices and physical activity. CA Cancer J Clin 56:254–281; quiz 313–314

    Article  PubMed  Google Scholar 

  45. Bingham SA (1999) High-meat diets and cancer risk. Proc Nutr Soc 58:243–248

    PubMed  CAS  Google Scholar 

  46. Weinberg ED (1996) The role of iron in cancer. Eur J Cancer Prev 5:19–36

    PubMed  CAS  Google Scholar 

  47. McCord JM (1998) Iron, free radicals, and oxidative injury. Semin Hematol 35:5–12

    PubMed  CAS  Google Scholar 

  48. Andersson AM, Skakkebaek NE (1999) Exposure to exogenous estrogens in food: possible impact on human development and health. Eur J Endocrinol 140:477–485

    Article  PubMed  CAS  Google Scholar 

  49. Matthews KH, Bernstein J, J.C. B. (2003) International trade of meat/poultry products and food safety issues. In: Buzby JC (ed) International trade and food safety: economic theory and case studies. Economic Research Service/USDA. Agricultural Economic Report No. AER828 (http://www.ers.usda.gov/publications/aer828/aer828f.pdf), pp 48–73

  50. European Commission, Health and Consumer Protection Directorate-General (2002) Opinion of the Scientific Committee on Veterinary Measures Relating to Public Health on Review of previous SCVPH opinions of 30 April 1999 and 3 May 2000 on the potential risks to human health from hormones residues in bovine meat and meat products (Adopted on 10 April 2002)

  51. Malekinejad H, Scherpenisse P, Bergwerff AA (2006) Naturally occurring estrogens in processed milk and in raw milk (from gestated cows). J Agric Food Chem 54:9785–9791

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgment

We would like to thank James Thomas for his valuable help with the data extraction Access® program.

Author information

Authors and Affiliations

  1. Robert Wood Johnson Medical School, The Cancer Institute of New Jersey, 195 Little Albany St, 5568, New Brunswick, NJ, 08903, USA

    Elisa V. Bandera & Dina M. Gifkins

  2. School of Public Health, University of Medicine and Dentistry of New Jersey, Piscataway, NJ, USA

    Elisa V. Bandera & Dirk F. Moore

  3. Division of Research, Kaiser Permanente, Oakland, CA, USA

    Lawrence H. Kushi

  4. Epidemiology and Surveillance Research, American Cancer Society, Atlanta, GA, USA

    Marjorie L. McCullough

Authors
  1. Elisa V. Bandera
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lawrence H. Kushi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dirk F. Moore
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dina M. Gifkins
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Marjorie L. McCullough
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Elisa V. Bandera.

Additional information

This work was funded in part by the WCRF and NIH-K07 CA095666. Although this work was funded in part by WCRF, interpretation of the evidence may not represent the views of WCRF and our conclusions may differ from those in the 2007 WCRF report summarizing evidence related to food, nutrition, physical activity, and cancer risk.

Appendix 1: WCRF—Pubmed search strategy

Appendix 1: WCRF—Pubmed search strategy

  1. #1

    diet therapy[MeSH Terms] OR nutrition[MeSH Terms]

  2. #2

    diet[tiab] OR diets[tiab] OR dietetic[tiab] OR dietary[tiab] OR eating[tiab] OR intake[tiab] OR nutrient*[tiab] OR nutrition[tiab] OR vegetarian*[tiab] OR vegan*[tiab] OR “seventh day adventist”[tiab] OR macrobiotic[tiab] OR breastfeed*[tiab] OR breast feed*[tiab] OR breastfed[tiab] OR breast fed[tiab] OR breastmilk[tiab] OR breast milk[tiab]

  3. #3

    food and beverages[MeSH Terms]

  4. #4

    food*[tiab] OR cereal*[tiab] OR grain*[tiab] OR granary[tiab] OR wholegrain[tiab] OR wholewheat[tiab] OR roots[tiab] OR plantain*[tiab] OR tuber[tiab] OR tubers[tiab] OR vegetable*[tiab] OR fruit*[tiab] OR pulses[tiab] OR beans[tiab] OR lentils[tiab] OR chickpeas[tiab] OR legume*[tiab] OR soy[tiab] OR soya[tiab] OR nut[tiab] OR nuts[tiab] OR peanut*[tiab] OR groundnut*[tiab] OR seeds[tiab] OR meat[tiab] OR beef[tiab] OR pork[tiab] OR lamb[tiab] OR poultry[tiab] OR chicken[tiab] OR turkey[tiab] OR duck[tiab] OR fish[tiab] OR fat[tiab] OR fats[tiab] OR fatty[tiab] OR egg[tiab] OR eggs[tiab] OR bread[tiab] OR oils[tiab] OR shellfish[tiab] OR seafood[tiab] OR sugar[tiab] OR syrup[tiab] OR dairy[tiab] OR milk[tiab] OR herbs[tiab] OR spices[tiab] OR chilli[tiab] OR chillis[tiab] OR pepper*[tiab] OR condiments[tiab]

  5. #5

    fluid intake[tiab] OR water[tiab] OR drinks[tiab] OR drinking[tiab] OR tea[tiab] OR coffee[tiab] OR caffeine[tiab] OR juice[tiab] OR beer[tiab] OR spirits[tiab] OR liquor[tiab] OR wine[tiab] OR alcohol[tiab] OR alcoholic[tiab] OR beverage*[tiab] OR ethanol[tiab] OR yerba mate[tiab] OR ilex paraguariensis[tiab]

  6. #6

    pesticides[MeSH Terms] OR fertilizers[MeSH Terms] OR “veterinary drugs”[MeSH Terms]

  7. #7

    pesticide*[tiab] OR herbicide*[tiab] OR DDT[tiab] OR fertiliser*[tiab] OR fertilizer*[tiab] OR organic[tiab] OR contaminants[tiab] OR contaminate*[tiab] OR veterinary drug*[tiab] OR polychlorinated dibenzofuran*[tiab] OR PCDF*[tiab] OR polychlorinated dibenzodioxin*[tiab] OR PCDD*[tiab] OR polychlorinated biphenyl*[tiab] OR PCB*[tiab] OR cadmium[tiab] OR arsenic[tiab] OR chlorinated hydrocarbon*[tiab] OR microbial contamination*[tiab]

  8. #8

    food preservation[MeSH Terms]

  9. #9

    mycotoxin*[tiab] OR aflatoxin*[tiab] OR pickled[tiab] OR bottled[tiab] OR bottling[tiab] OR canned[tiab] OR canning[tiab] OR vacuum pack*[tiab] OR refrigerate*[tiab] OR refrigeration[tiab] OR cured[tiab] OR smoked[tiab] OR preserved[tiab] OR preservatives[tiab] OR nitrosamine[tiab] OR hydrogenation[tiab] OR fortified[tiab] OR additive*[tiab] OR colouring*[tiab] OR coloring*[tiab] OR flavouring*[tiab] OR flavoring*[tiab] OR nitrates[tiab] OR nitrites[tiab] OR solvent[tiab] OR solvents[tiab] OR ferment*[tiab] OR processed[tiab] OR antioxidant*[tiab] OR genetic modif*[tiab] OR genetically modif*[tiab] OR vinyl chloride[tiab] OR packaging[tiab] OR labelling[tiab] OR phthalates[tiab]

  10. #10

    cookery[MeSH Terms]

  11. #11

    cooking[tiab] OR cooked[tiab] OR grill[tiab] OR grilled[tiab] OR fried[tiab] OR fry[tiab] OR roast[tiab] OR bake[tiab] OR baked[tiab] OR stewing[tiab] OR stewed[tiab] OR casserol*[tiab] OR broil[tiab] OR broiled[tiab] OR boiled[tiab] OR microwave[tiab] OR microwaved[tiab] OR re-heating[tiab] OR reheating[tiab] OR heating[tiab] OR re-heated[tiab] OR heated[tiab] OR poach[tiab] OR poached[tiab] OR steamed[tiab] OR barbecue*[tiab] OR chargrill*[tiab] OR heterocyclic amines[tiab] OR polycyclic aromatic hydrocarbons[tiab]

  12. #12

    dietary carbohydrates[MeSH Terms] OR dietary proteins[MeSH Terms] OR sweetening agents[MeSH Terms]

  13. #13

    salt[tiab] OR salting[tiab] OR salted[tiab] OR fiber[tiab] OR fibre[tiab] OR polysaccharide*[tiab] OR starch[tiab] OR starchy[tiab] OR carbohydrate*[tiab] OR lipid*[tiab] OR linoleic acid*[tiab] OR sterols[tiab] OR stanols[tiab] OR sugar*[tiab] OR sweetener*[tiab] OR saccharin*[tiab] OR aspartame[tiab] OR acesulfame[tiab] OR cyclamates[tiab] OR maltose[tiab] OR mannitol[tiab] OR sorbitol[tiab] OR sucrose[tiab] OR xylitol[tiab] OR cholesterol[tiab] OR protein[tiab] OR proteins[tiab] OR hydrogenated dietary oils[tiab] OR hydrogenated lard[tiab] OR hydrogenated oils[tiab]

  14. #14

    vitamins[MeSH Terms]

  15. #15

    supplements[tiab] OR supplement[tiab] OR vitamin*[tiab] OR retinol[tiab] OR carotenoid*[tiab] OR tocopherol[tiab] OR folate*[tiab] OR folic acid[tiab] OR methionine[tiab] OR riboflavin[tiab] OR thiamine[tiab] OR niacin[tiab] OR pyridoxine[tiab] OR cobalamin[tiab] OR mineral*[tiab] OR sodium[tiab] OR iron[tiab] OR calcium[tiab] OR selenium[tiab] OR iodine[tiab] OR magnesium[tiab] OR potassium[tiab] OR zinc[tiab] OR copper[tiab] OR phosphorus[tiab] OR manganese[tiab] OR chromium[tiab] OR phytochemical[tiab] OR allium[tiab] OR isothiocyanate*[tiab] OR glucosinolate*[tiab] OR indoles[tiab] OR polyphenol*[tiab] OR phytoestrogen*[tiab] OR genistein[tiab] OR saponin*[tiab] OR coumarin*[tiab]

  16. #16

    physical fitness[MeSH Terms] OR exertion[MeSH Terms] OR physical endurance[MeSH Terms] or walking[MeSH Terms]

  17. #17

    recreational activit*[tiab] OR household activit*[tiab] OR occupational activit*[tiab] OR physical activit*[tiab] OR physical inactivit*[tiab] OR exercise[tiab] OR exercising[tiab] OR energy intake[tiab] OR energy expenditure[tiab] OR energy balance[tiab] OR energy density[tiab]

  18. #18

    growth[MeSH Terms] OR anthropometry[MeSH Terms] OR body composition[MeSH Terms] OR body constitution[MeSH Terms]

  19. #19

    weight loss[tiab] or weight gain[tiab] OR anthropometry[tiab] OR birth weight[tiab] OR birthweight[tiab] OR birth-weight[tiab] OR child development[tiab] OR height[tiab] OR body composition[tiab] OR body mass[tiab] OR BMI[tiab] OR obesity[tiab] OR obese[tiab] OR overweight[tiab] OR over-weight[tiab] OR over weight[tiab] OR skinfold measurement*[tiab] OR skinfold thickness[tiab] OR DEXA[tiab] OR bio-impedence[tiab] OR waist circumference[tiab] OR hip circumference[tiab] OR waist hip ratio*[tiab]

  20. #20

    #1 OR #2 OR #3 OR #4 OR #5 OR #6 OR #7 OR #8 OR #9 OR #10 OR #11 OR #12 OR #13 OR #14 OR #15 OR #16 OR #17 OR #18 OR #19

Key

[tiab]

searches the title and abstract fields only

[MeSH Terms]

searches the Medical Subject Headings field only

NB—explosion of MeSH terms is automatic

*

truncation symbol—searches all words with this combination of letters at the beginning

Table A Foods included in food groups in papers contributing to meta-analyses
Full size table

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bandera, E.V., Kushi, L.H., Moore, D.F. et al. Consumption of animal foods and endometrial cancer risk: a systematic literature review and meta-analysis. Cancer Causes Control 18, 967–988 (2007). https://doi.org/10.1007/s10552-007-9038-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10552-007-9038-0

Keywords

Search

Navigation