Advertisement

Hormones and Cancer

, Volume 7, Issue 1, pp 65–74 | Cite as

Alcohol Consumption and Urinary Estrogens and Estrogen Metabolites in Premenopausal Women

  • Terryl J. HartmanEmail author
  • Julia S. Sisti
  • Susan E. Hankinson
  • Xia Xu
  • A. Heather Eliassen
  • Regina Ziegler
Original Paper

Abstract

In a cross-sectional analysis, we evaluated the associations of usual total alcohol and wine intake with a comprehensive profile of mid-luteal phase urinary estrogens and estrogen metabolites (referred to jointly as EM) in a sample of 603 premenopausal women participating in the Nurses’ Health Study II (NHSII). A total of 15 individual EM (pmol/mg creatinine) were measured by a liquid chromatography/tandem mass spectrometry (LC-MS/MS) method with high accuracy and reproducibility. We used linear mixed models to calculate the adjusted geometric means of individual EM, EM grouped by metabolic pathways, and pathway ratios by category of alcohol intake with non-drinkers of alcohol as the referent. Total alcohol intake was not associated with total EM but was positively associated with estradiol (26 % higher among women consuming >15 g/day vs. non-drinkers; P trend = 0.03). Wine consumption was positively associated with a number of EM measures including estradiol (22 % higher among women consuming ≥5 drinks/week vs. non-drinkers, P trend < 0.0001). In conclusion, the total alcohol intake was positively and significantly associated with urinary estradiol levels. Some differences in urinary estrogen metabolites were observed with wine drinking, when compared with non-drinkers. This study strengthens the evidence that alcohol consumption might play a role in breast cancer and other estrogen-related conditions. Additional studies of premenopausal women are needed to further explore the association of alcohol, particularly the specific types of alcohol, on patterns of estrogen metabolism in blood, urine, and tissue.

Keywords

Breast Cancer Risk Premenopausal Woman Luteal Phase Estrogen Metabolite Estrogen Metabolism 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

This study was supported by NIH UM1 CA176726 (Walter C. Willett) and R01 CA67262 (Susan E. Hankinson), and by Research Grants CA67262 and CA50385 from the National Cancer Institute (NCI). It was also supported by the Intramural Research Program of the NCI Division of Cancer Epidemiology and Genetics and with the federal funds of the NCI awarded under Contract HHSN261200900001E to SAIC-Frederick, now Leidos Biomedical Research, Inc. Julia Sisti was supported by training grants R25 CA098566 and T32 CA900137. We would like to thank the participants and staff of the Nurses’ Health Studies for their valuable contributions. The authors assume full responsibility for analyses and interpretation of these data.

Compliance with Ethical Standards

Conflict of Interest

The content of this publication does not necessarily reflect the views or policies of the US Department of Health and Human Services, nor does mention of trade names, commercial products, or organizations imply endorsement by the US Government.

No potential conflicts of interest were disclosed by the other authors.

Ethics Approval

This study was approved by the Committee on the Use of Human Subjects in Research at Brigham and Women’s Hospital (Boston, MA).

References

  1. 1.
    Lee YC, Hashibe M (2014) Tobacco, alcohol, and cancer in low and high income countries. Ann Glob Health 80:378–383CrossRefPubMedGoogle Scholar
  2. 2.
    World Cancer Research Fund \American Institute for Cancer Research (2007) Food, nutrition, physical activity, and the prevention of cancer: a global perspective. AICR, WashingtonGoogle Scholar
  3. 3.
    Smith-Warner SA, Spiegelman D, Yaun SS, van den Brandt PA, Folsum AR, Goldbohm RA et al (1998) Alcohol and breast cancer in women: a pooled analysis of cohort studies. JAMA 279:535–540CrossRefPubMedGoogle Scholar
  4. 4.
    Allen NE, Beral V, Casabonne D, Kan SW, Reeves GK, Brown A, Green J (2009) Moderate alcohol intake and cancer incidence in women. J Natl Cancer Inst 101:296–305CrossRefPubMedGoogle Scholar
  5. 5.
    Zhang SM, Lee IM, Manson JE, Cook NR, Willett WC, Buring JE (2007) Alcohol consumption and breast cancer risk in the Women’s Health Study. Am J Epidemiol 165:667–676CrossRefPubMedGoogle Scholar
  6. 6.
    World Cancer Research Fund/American Institute for Cancer Research (2010) Breast cancer report continuous update project: food, nutrition, physical activity, and the prevention of breast cancer. AICR, WashingtonGoogle Scholar
  7. 7.
    Dorgan JF, Baer DJ, Albert PS, Judd JT, Brown ED, Corle DK et al (2001) Serum hormones and the alcohol-breast cancer association in postmenopausal women. J Natl Cancer Inst 93:710–715CrossRefPubMedGoogle Scholar
  8. 8.
    Dorgan JF, Reichman ME, Judd JT, Brown C, Longcope C, Schatzkin A et al (1994) The relation of reported alcohol ingestion to plasma levels of estrogens and androgens in premenopausal women. Cancer Causes Control 5:53–60CrossRefPubMedGoogle Scholar
  9. 9.
    Reichman ME, Judd JT, Longcope C, Schatzkin A, Clevidence BA, Nair PP et al (1993) Effects of alcohol consumption on plasma and urinary hormone concentrations in premenopausal women. J Natl Cancer Inst 85:722–727CrossRefPubMedGoogle Scholar
  10. 10.
    Hirko KA, Spiegelman D, Willett WC, Hankinson SE, Eliassen AH (2014) Alcohol consumption in relation to plasma sex hormones, prolactin, and sex hormone-binding globulin in premenopausal women. Cancer Epidemiol Biomarkers Prev 23:2943–2953PubMedCentralCrossRefPubMedGoogle Scholar
  11. 11.
    Lyngso J, Toft G, Hoyer BB, Guldbrandsen K, Olsen J, Ramlau-Hansen CH (2014) Moderate alcohol intake and menstrual cycle characteristics. Hum Reprod 29:351–358CrossRefPubMedGoogle Scholar
  12. 12.
    Cooper GS, Sandler DP, Whelan EA, Smith KR (1996) Association of physical and behavioral characteristics with menstrual cycle patterns in women age 29–31 years. Epidemiology 7:624–628CrossRefPubMedGoogle Scholar
  13. 13.
    Liu Y, Gold EB, Lasley BL, Johnson WO (2004) Factors affecting menstrual cycle characteristics. Am J Epidemiol 160:131–140CrossRefPubMedGoogle Scholar
  14. 14.
    Samavat H, Kurzer MS (2015) Estrogen metabolism and breast cancer. Cancer Lett 356:231–243CrossRefPubMedGoogle Scholar
  15. 15.
    Seeger H, Wallwiener D, Kraemer E, Mueck AO (2006) Comparison of possible carcinogenic estradiol metabolites: effects on proliferation, apoptosis and metastasis of human breast cancer cells. Maturitas 54:72–77CrossRefPubMedGoogle Scholar
  16. 16.
    Hurh YJ, Chen ZH, Na HK, Han SY, Surh YJ (2004) 2-Hydroxyestradiol induces oxidative DNA damage and apoptosis in human mammary epithelial cells. J Toxicol Environ Health A 67(23–24):1939–1953CrossRefPubMedGoogle Scholar
  17. 17.
    Liu ZJ, Zhu BT (2004) Concentration-dependent mitogenic and antiproliferative actions of 2-methoxyestradiol in estrogen receptor-positive human breast cancer cells. J Steroid Biochem Mol Biol 88:265–275CrossRefPubMedGoogle Scholar
  18. 18.
    Ziegler RG, Faupel-Badger JM, Sue LY, Frhrman BJ, Falk RT, Boyd-Morin J, Henderson MK, Hoover RN, Beenstra TD, Keefer LK, Xu X (2010) A new approach to measuring estrogen exposure and metabolism in epidemiologic studies. J Steroid Biochem Mol Biol 121:538–545CrossRefPubMedGoogle Scholar
  19. 19.
    Xu X, Veenstra TD, Fox SD, Roman JM, Isaaq HJ, Falk R, Saavedra JE, Keefer LK, Ziegler RG (2005) Measuring fifteen endogenous estrogens simultaneously in human urine by high-performance liquid chromatography-mass spectrometry. Anal Chem 77:6646–6654CrossRefPubMedGoogle Scholar
  20. 20.
    Fortner RT, Hankinson SE, Schairer C, Xu X, Ziegler RG, Eliassen AH (2012) Association between reproductive factors and urinary estrogens and estrogen metabolites in premenopausal women. Cancer Epidemiol Biomarkers Prev 21:959–968PubMedCentralCrossRefPubMedGoogle Scholar
  21. 21.
    Matthews CE, Fortner RT, Xu X, Hankinson SE, Eliassen AH, Ziegler RG (2012) Association between physical activity and urinary estrogens and estrogen metabolites in premenopausal women. J Clin Endocrinol Metab 97:3724–3733PubMedCentralCrossRefPubMedGoogle Scholar
  22. 22.
    Gu F, Caporaso NE, Schairer C, Fortner RT, Xu X, Hankinson SE et al (2013) Urinary concentrations of estrogens and estrogen metabolites and smoking in Caucasian women. Cancer Epidemiol Biomarkers Prev 22:58–68PubMedCentralCrossRefPubMedGoogle Scholar
  23. 23.
    Fortner RT, Oh H, Daugherty SE, Xu X, Hankinson SE, Ziegler RG, Eliassen AH (2014) Analgesic use and patterns of estrogen metabolism in premenopausal women. Horm Cancer 5:104–112PubMedCentralCrossRefPubMedGoogle Scholar
  24. 24.
    Eliassen AH, Missmer SA, Tworoger SS, Spiegelman D, Barbieri RL, Dowsett M, Hankinson SE (2006) Endogenous steroid hormone concentrations and risk of breast cancer among premenopausal women. J Natl Cancer Inst 98:1406–1415CrossRefPubMedGoogle Scholar
  25. 25.
    Eliassen AH, Spiegelman D, Xu X, Keefer LK, Veenstra TD, Barbieri RL et al (2012) Urinary estrogens and estrogen metabolites and subsequent risk of breast cancer among premenopausal women. Cancer Res 72:696–706PubMedCentralCrossRefPubMedGoogle Scholar
  26. 26.
    Eliassen AH, Ziegler RG, Rosner B, Veenstra TD, Roman JM, Xu X, Hankinson SE (2009) Reproducibility of fifteen urinary estrogens and estrogen metabolites over a 2- to 3-year period in premenopausal women. Cancer Epidemiol Biomarkers Prev 18:2860–2868PubMedCentralCrossRefPubMedGoogle Scholar
  27. 27.
    Tworoger SS, Sluss P, Hankinson SE (2006) Association between plasma prolactin concentrations and risk of breast cancer among predominately premenopausal women. Cancer Res 66:2476–2482CrossRefPubMedGoogle Scholar
  28. 28.
    Rosner B (1983) Percentage points for a generalized ESD many-outlier procedure. Technometrics 25(2):165–172CrossRefGoogle Scholar
  29. 29.
    Sowers MR, Crawford S, McConnell DS, Randolph JF, Gold EB, Wilkin MK et al (2006) Selected diet and lifestyle factors are associated with estrogen metabolites in a multiracial/ethnic population of women. J Nutr 136:1588–1595PubMedGoogle Scholar
  30. 30.
    Giovannucci E, Colditz G, Stampfer MJ, Rimm EB, Litin L, Sampson L et al (1991) The assessment of alcohol consumption by a simple self-administered questionnaire. Am J Epidemiol 133:810–817PubMedGoogle Scholar
  31. 31.
    Dumitrescu RG, Shields PG (2005) The etiology of alcohol-induced breast cancer. Alcohol 35:213–225CrossRefPubMedGoogle Scholar
  32. 32.
    Hankinson SE, Eliassen AH (2010) Circulating sex steroids and breast cancer risk in premenopausal women. Horm Cancer 1:2–10PubMedCentralCrossRefPubMedGoogle Scholar
  33. 33.
    Dallal CM, Stone RA, Cauley JA, Ness RB, Vogel VG, Fentiman IS et al (2013) Urinary estrogen metabolites and breast cancer: a combined analysis of individual level data. Int J Biol Markers 28:3–16CrossRefPubMedGoogle Scholar
  34. 34.
    Ziegler RG, Fuhrman BJ, Moore SC, Matthews CE (2015) Epidemiologic studies of estrogen metabolism and breast cancer. Steroids 99:67–75CrossRefPubMedGoogle Scholar
  35. 35.
    Lieber CS (2004) The discovery of the microsomal ethanol oxidizing system and its physiologic and pathologic role. Drug Metab Rev 36:511–529CrossRefPubMedGoogle Scholar
  36. 36.
    Novak RF, Woodcroft KJ (2000) The alcohol-inducible form of cytochrome P450 (CYP 2E1): role in toxicology and regulation of expression. Arch Pharm Res 23:267–282CrossRefPubMedGoogle Scholar
  37. 37.
    Hartman TJ, Baer DJ, Graham LB, Stone WL, Gunter EW, Parker CE et al (2005) Moderate alcohol consumption and levels of antioxidant vitamins and isoprostanes in postmenopausal women. Eur J Clin Nutr 59:161–168CrossRefPubMedGoogle Scholar
  38. 38.
    Laufer EM, Hartman TJ, Baer DJ, Gunter EW, Dorgan JF, Campbell WS et al (2004) Effects of moderate alcohol consumption on folate and vitamin B(12) status in postmenopausal women. Eur J Clin Nutr 58:1518–1524CrossRefPubMedGoogle Scholar
  39. 39.
    Missmer SA, Spiegelman D, Bertone-Johnson ER, Barbieri RL, Pollak MN, Hankinson SE (2006) Reproducibility of plasma hormone and growth factor levels among premenopausal women over a 2–3 year period. Cancer Epidemiol Biomarkers Prev 15:972–978CrossRefPubMedGoogle Scholar
  40. 40.
    Mady EA, Ramadan EE, Ossman AA (2000) Sex steroid hormones in serum and tissue of benign and malignant breast tumor patients. Dis Markers 16:151–157PubMedCentralCrossRefPubMedGoogle Scholar
  41. 41.
    National Institute on Alcohol Abuse and Alcoholism (2006) Alcohol use and alcohol disorders in the United States: main findings from the 2001–2002 National Epidemiologic Survey on Alcohol and Related Conditions (NESARC). National Institutes of Health, Bethesda, NIH Publication No. 05–5737Google Scholar
  42. 42.
    Kerr WC, Greenfield TK, Bond J, Ye Y, Rehm J (2004) Age, period and cohort influences on beer, wine and spirits consumption trends in US National Alcohol Surveys. Addiction 99:1111–1120CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York (outside the USA) 2015

Authors and Affiliations

  • Terryl J. Hartman
    • 1
    Email author
  • Julia S. Sisti
    • 2
    • 3
  • Susan E. Hankinson
    • 2
    • 3
    • 4
  • Xia Xu
    • 5
  • A. Heather Eliassen
    • 2
    • 3
  • Regina Ziegler
    • 6
  1. 1.Department of Epidemiology, Rollins School of Public Health & Winship Cancer InstituteEmory UniversityAtlantaUSA
  2. 2.Department of EpidemiologyHarvard T. H. Chan School of Public HealthBostonUSA
  3. 3.Channing Division of Network Medicine, Department of MedicineBrigham and Women’s Hospital and Harvard Medical SchoolBostonUSA
  4. 4.Division of Biostatistics and Epidemiology, School of Public Health and Health SciencesUniversity of MassachusettsAmherstUSA
  5. 5.Cancer Research Technology Program, Leidos Biomedical Research, Inc.Frederick National Laboratory for Cancer ResearchFrederickUSA
  6. 6.Division of Cancer Epidemiology and GeneticsNational Cancer InstituteBethesdaUSA

Personalised recommendations