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Associations of established breast cancer risk factors with urinary estrogens in postmenopausal women

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Abstract

Purpose

Circulating estrogens are an established risk factor for postmenopausal breast cancer (BCa). We describe the distribution of urinary estrogens, their metabolites, and relevant metabolic pathway ratios among healthy postmenopausal women and examine associations of several known BCa factors with these estrogen measures.

Methods

Eligible postmenopausal women (n = 167) had no history of hormone use (previous 6 months) and cancer/metabolic disorders and had a body mass index (BMI) ≤ 35 kg/m2. Estrogens were quantified in spot urine samples with liquid chromatography-high-resolution mass spectrometry and corrected for creatinine. We assessed overall distributions of estrogens and associations of age, BMI, race/ethnicity, parity/age at first birth, age at menarche, alcohol, and smoking with log-transformed estrogen measures using multivariate regression.

Results

BMI was positively associated with estrone (β per unit = 0.04, 95% Confidence Interval [CI] 0.00; 0.07), combined parent estrogens (β = 0.04, 95% CI 0.01; 0.07), and E2:total estrogens (β = 0.04, 95% CI 0.02; 0.06), and inversely associated with 4-MeOE1 (β = − 0.17, 95% CI − 0.33; − 0.02), E3:parent estrogens (β = − 0.04, 95% CI − 0.07; − 0.00), and 16-pathway:parent (β = − 0.04, 95% CI − 0.07; − 0.01). Being African American vs. white was associated with higher levels of 4-MeOE1 (β = 3.41, 95% CI 0.74; 6.08), 17-epiE3 (β = 1.19, 95% CI 0.07; 2.31), 2-pathway:parent (β = 0.54, 95% CI 0.04; 1.04), and lower levels of E2:total estrogens (β = − 0.48, 95% CI − 0.83; − 0.13). Having < 7 alcohol drinks/week vs. none was associated with higher levels of 16-ketoE2 (β = 1.32, 95% CI 0.36; 2.27), 16-epiE3 (β = 1.02, 95% CI 0.24; 1.79), and 17-epiE3 (β = 0.55, 95% CI 0.02; 1.08). Smoking was positively associated with E3:parent (β = 0.29, 95% CI 0.01; 0.57), 16-pathway:parent (β = 0.25, 95% CI 0.01; 0.49), and inversely associated with estradiol (β = − 0.52, 95% CI − 0.93; − 0.10). As compared to nulliparous, parous women with age at first birth ≥ 25 years had lower levels of estrone, combined parent estrogens, 2-OHE1, and 2-OHE2.

Conclusion

Our findings suggest that BMI, race/ethnicity, and some reproductive and lifestyle factors may contribute to postmenopausal BCa through their effects on circulating estrogens.

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Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  1. Yager JD (2000) Endogenous estrogens as carcinogens through metabolic activation. J Natl Cancer Inst Monogr 2000:67–73

    Article  Google Scholar 

  2. Yager JD, Davidson NE (2006) Estrogen carcinogenesis in breast cancer. N Engl J Med 354:270–282

    Article  CAS  PubMed  Google Scholar 

  3. Yue W, Yager JD, Wang JP, Jupe ER, Santen RJ (2013) Estrogen receptor-dependent and independent mechanisms of breast cancer carcinogenesis. Steroids 78:161–170

    Article  CAS  PubMed  Google Scholar 

  4. Thomas HV, Reeves GK, Key TJA (1997) Endogenous estrogen and postmenopausal breast cancer: a quantitative review. Cancer Causes Control 8:922

    Article  CAS  PubMed  Google Scholar 

  5. Ziegler RG, Fuhrman BJ, Moore SC, Matthews CE (2015) Epidemiologic studies of estrogen metabolism and breast cancer. Steroids 99:67–75

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Samavat H, Kurzer MS (2015) Estrogen metabolism and breast cancer. Cancer Lett 356:231–243

    Article  CAS  PubMed  Google Scholar 

  7. Bradlow HL, Telang NT, Sepkovic DW, Osborne MP (1996) 2-hydroxyestrone: the “good” estrogen. J Endocrinol 150(Suppl):S259–S265

    CAS  PubMed  Google Scholar 

  8. Dallal C, Taioli E (2010) Urinary 2/16 estrogen metabolite ratio levels in healthy women: a review of the literature. Mutat Res 705:154–162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Sepkovic DW, Bradlow HL (2009) Estrogen hydroxylation–the good and the bad. Ann N Y Acad Sci 1155:57–67

    Article  CAS  PubMed  Google Scholar 

  10. Kabat GC, Chang CJ, Sparano JA et al (1997) Urinary estrogen metabolites and breast cancer: a case–control study. Cancer Epidemiol Biomark Prev 6:505–509

    CAS  Google Scholar 

  11. Meilahn EN, De Stavola B, Allen DS et al (1998) Do urinary oestrogen metabolites predict breast cancer? Guernsey III cohort follow-up. Br J Cancer 78:1250–1255

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Moore SC, Matthews CE, Ou Shu X et al (2016) Endogenous estrogens, estrogen metabolites, and breast cancer risk in postmenopausal Chinese women. J Natl Cancer Inst 108:djw103

    Article  PubMed Central  Google Scholar 

  13. Sampson JN, Falk RT, Schairer C et al (2017) Association of estrogen metabolism with breast cancer risk in different cohorts of postmenopausal women. Cancer Res 77:918–925

    Article  CAS  PubMed  Google Scholar 

  14. Maskarinec G, Beckford F, Morimoto Y, Franke AA, Stanczyk FZ (2015) Association of estrogen measurements in serum and urine of premenopausal women. Biomark Med 9:417–424

    Article  CAS  PubMed  Google Scholar 

  15. Lasley BL, Mobed K, Gold EB (1994) The use of urinary hormonal assessments in human studies. Ann N Y Acad Sci 709:299–311

    Article  CAS  PubMed  Google Scholar 

  16. Faqehi AMM, Cobice DF, Naredo G et al (2016) Derivatization of estrogens enhances specificity and sensitivity of analysis of human plasma and serum by liquid chromatography tandem mass spectrometry. Talanta 151:148–156

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Zhu BT, Conney AH (1998) Functional role of estrogen metabolism in target cells: review and perspectives. Carcinogenesis 19:1–27

    Article  PubMed  Google Scholar 

  18. Guillemette C, Bélanger A, Lépine J (2004) Metabolic inactivation of estrogens in breast tissue by UDP-glucuronosyltransferase enzymes: an overview. Breast Cancer Res 6:246–254

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Cleary MP, Grossmann ME (2009) Minireview: obesity and breast cancer: the estrogen connection. Endocrinology 150:2537–2542

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Lukanova A, Lundin E, Zeleniuch-Jacquotte A et al (2004) Body mass index, circulating levels of sex-steroid hormones, IGF-I and IGF-binding protein-3: a cross-sectional study in healthy women. Eur J Endocrinol 150:161–171

    Article  CAS  PubMed  Google Scholar 

  21. Madigan MP, Troisi R, Potischman N, Dorgan JF, Brinton LA, Hoover RN (1998) Serum hormone levels in relation to reproductive and lifestyle factors in postmenopausal women (United States). Cancer Causes Control 9:199–207

    Article  CAS  PubMed  Google Scholar 

  22. McTiernan A, Wu L, Chen C et al (2006) Relation of BMI and physical activity to sex hormones in postmenopausal women. Obesity (Silver Spring) 14:1662–1677

    Article  CAS  Google Scholar 

  23. Boyapati SM, Shu XO, Gao Y-T et al (2004) Correlation of blood sex steroid hormones with body size, body fat distribution, and other known risk factors for breast cancer in post-menopausal Chinese women. Cancer Causes Control 15:305–311

    Article  PubMed  Google Scholar 

  24. Bezemer ID, Rinaldi S, Dossus L et al (2005) C-peptide, IGF-I, sex-steroid hormones and adiposity: a cross-sectional study in healthy women within the European prospective investigation into cancer and nutrition (EPIC). Cancer Causes Control 16:561–572

    Article  PubMed  Google Scholar 

  25. Tsuchiya Y, Nakajima M, Yokoi T (2005) Cytochrome P450-mediated metabolism of estrogens and its regulation in human. Cancer Lett 227:115–124

    Article  CAS  PubMed  Google Scholar 

  26. Rodríguez-Morató J, Goday A, Langohr K et al (2019) Short- and medium-term impact of bariatric surgery on the activities of CYP2D6, CYP3A4, CYP2C9, and CYP1A2 in morbid obesity. Sci Rep 9:20405

    Article  PubMed  PubMed Central  Google Scholar 

  27. Kotlyar M, Carson SW (1999) Effects of obesity on the cytochrome P450 enzyme system. Int J Clin Pharmacol Ther 37:8–19

    CAS  PubMed  Google Scholar 

  28. Barrett ES, Parlett LE, Windham GC, Swan SH (2014) Differences in ovarian hormones in relation to parity and time since last birth. Fertil Steril 101:1773–80.e1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Bernstein L, Pike MC, Ross RK, Judd HL, Brown JB, Henderson BE (1985) Estrogen and sex hormone-binding globulin levels in nulliparous and parous women. J Natl Cancer Inst 74:741–745

    CAS  PubMed  Google Scholar 

  30. Onland-Moret NC, Peeters PHM, van der Schouw YT, Grobbee DE, van Gils CH (2005) Alcohol and endogenous sex steroid levels in postmenopausal women: a cross-sectional study. J Clin Endocrinol Metab 90:1414–1419

    Article  CAS  PubMed  Google Scholar 

  31. Hines LM, Hankinson SE, Smith-Warner SA et al (2000) A prospective study of the effect of alcohol consumption and ADH3 genotype on plasma steroid hormone levels and breast cancer risk. Cancer Epidemiol Biomark Prev 9:1099–1105

    CAS  Google Scholar 

  32. Brand JS, Chan M-F, Dowsett M et al (2011) Cigarette smoking and endogenous sex hormones in postmenopausal women. J Clin Endocrinol Metab 96:3184–3192

    Article  CAS  PubMed  Google Scholar 

  33. Frydenberg H, Flote VG, Larsson IM et al (2015) Alcohol consumption, endogenous estrogen and mammographic density among premenopausal women. Breast Cancer Res 17:103

    Article  PubMed  PubMed Central  Google Scholar 

  34. Darville LNF, Cline JK, Rozmeski C et al (2020) LC-HRMS of derivatized urinary estrogens and estrogen metabolites in postmenopausal women. J Chromatogr B 1154:122288

    Article  CAS  Google Scholar 

  35. MacLean B, Tomazela DM, Shulman N et al (2010) Skyline: an open source document editor for creating and analyzing targeted proteomics experiments. Bioinformatics (Oxford) 26:966–968

    Article  CAS  Google Scholar 

  36. Miller RC, Brindle E, Holman DJ et al (2004) Comparison of specific gravity and creatinine for normalizing urinary reproductive hormone concentrations. Clin Chem 50:924–932

    Article  CAS  PubMed  Google Scholar 

  37. Shi L, Remer T, Buyken AE, Hartmann MF, Hoffmann P, Wudy SA (2010) Prepubertal urinary estrogen excretion and its relationship with pubertal timing. Am J Physiol Endocrinol Meta 299:E990–E997

    Article  CAS  Google Scholar 

  38. Li J, Zhang W, Zhao H et al (2020) Trimester-specific, gender-specific, and low-dose effects associated with non-monotonic relationships of bisphenol a on estrone, 17β-estradiol and estriol. Environ Int 134:105304

    Article  CAS  PubMed  Google Scholar 

  39. Chubak J, Tworoger SS, Yasui Y, Ulrich CM, Stanczyk FZ, McTiernan A (2004) Associations between reproductive and menstrual factors and postmenopausal sex hormone concentrations. Cancer Epidemiol Biomark Prev 13:1296–1301

    Article  CAS  Google Scholar 

  40. Fuhrman BJ, Feigelson HS, Flores R et al (2014) Associations of the fecal microbiome with urinary estrogens and estrogen metabolites in postmenopausal women. J Clin Endocrinol Metab 99:4632–4640

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Xu X, Veenstra TD, Fox SD et al (2005) Measuring fifteen endogenous estrogens simultaneously in human urine by high-performance liquid chromatography-mass spectrometry. Anal Chem 77:6646–6654

    Article  CAS  PubMed  Google Scholar 

  42. Oh H, Coburn SB, Matthews CE et al (2017) Anthropometric measures and serum estrogen metabolism in postmenopausal women: the women’s health initiative observational study. Breast Cancer Res 19:28

    Article  PubMed  PubMed Central  Google Scholar 

  43. Freeman EW, Sammel MD, Lin H, Gracia CR (2010) Obesity and reproductive hormone levels in the transition to menopause. Menopause (New York) 17:718–726

    Article  Google Scholar 

  44. Richardson H, Ho V, Pasquet R et al (2020) Baseline estrogen levels in postmenopausal women participating in the MAP.3 breast cancer chemoprevention trial. Menopause (New York) 27:693–700

    Google Scholar 

  45. Group EHBCC (2003) Body mass index, serum sex hormones, and breast cancer risk in postmenopausal women. JNCI J Natl Cancer Inst 95:1218–1226

    Article  Google Scholar 

  46. Setiawan VW, Haiman CA, Stanczyk FZ, Le Marchand L, Henderson BE (2006) Racial/ethnic differences in postmenopausal endogenous hormones: the multiethnic cohort study. Cancer Epidemiol Biomark Prev 15:1849–1855

    Article  CAS  Google Scholar 

  47. Probst-Hensch NM, Pike MC, McKean-Cowdin R, Stanczyk FZ, Kolonel LN, Henderson BE (2000) Ethnic differences in post-menopausal plasma oestrogen levels: high oestrone levels in Japanese-American women despite low weight. Br J Cancer 82:1867–1870

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Zhang SM, Lee I-M, Manson JE, Cook NR, Willett WC, Buring JE (2007) Alcohol consumption and breast cancer risk in the women’s health study. Am J Epidemiol 165:667–676

    Article  PubMed  Google Scholar 

  49. Taneri PE, Kiefte-de Jong JC, Bramer WM, Daan NMP, Franco OH, Muka T (2016) Association of alcohol consumption with the onset of natural menopause: a systematic review and meta-analysis. Hum Reprod Update 22:516–528

    Article  PubMed  Google Scholar 

  50. Mahabir S, Pfeiffer R, Xu X, Baer DJ, Taylor PR (2017) Effects of low-to-moderate alcohol supplementation on urinary estrogen metabolites in postmenopausal women in a controlled feeding study. Cancer Med 6:2419–2423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Key TJ, Appleby PN, Reeves GK et al (2011) Circulating sex hormones and breast cancer risk factors in postmenopausal women: reanalysis of 13 studies. Br J Cancer 105:709–722

    Article  CAS  PubMed  Google Scholar 

  52. Zevin S, Benowitz NL (1999) Drug interactions with tobacco smoking. An update. Clin Pharmacokinet 36:425–438

    Article  CAS  PubMed  Google Scholar 

  53. O’Malley M, King AN, Conte M, Ellingrod VL, Ramnath N (2014) Effects of cigarette smoking on metabolism and effectiveness of systemic therapy for lung cancer. J Thorac Oncol 9:917–926

    Article  PubMed  Google Scholar 

  54. Yang H, Anderson G, Behan S et al (2016) Abstract 4296: serum estrogen and estrogen metabolites and smoking among postmenopausal women in the women’s health initiative observational study. Cancer Res 76:4296

    Article  Google Scholar 

  55. Rinaldi S, Moret CN, Kaaks R et al (2003) Reproducibility over time of measurements of androgens, estrogens and hydroxy estrogens in urine samples from post-menopausal women. Eur J Epidemiol 18:417–424

    Article  CAS  PubMed  Google Scholar 

  56. Travis RC, Key TJ (2003) Oestrogen exposure and breast cancer risk. Breast Cancer Res 5:239–247

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Yoong SL, Carey ML, D’Este C, Sanson-Fisher RW (2013) Agreement between self-reported and measured weight and height collected in general practice patients: a prospective study. BMC Med Res Methodol 13:38

    Article  PubMed  PubMed Central  Google Scholar 

  58. Dahl AK, Hassing LB, Fransson EI, Pedersen NL (2010) Agreement between self-reported and measured height, weight and body mass index in old age—a longitudinal study with 20 years of follow-up. Age Ageing 39:445–451

    Article  PubMed  PubMed Central  Google Scholar 

  59. Lin CJ, DeRoo LA, Jacobs SR, Sandler DP (2012) Accuracy and reliability of self-reported weight and height in the sister study. Public Health Nutr 15:989–999

    Article  PubMed  Google Scholar 

  60. Spencer E, Appleby P, Davey G, Key T (2002) Validity of self-reported height and weight in 4808 EPIC-Oxford participants. Public Health Nutr 5:561–565

    Article  PubMed  Google Scholar 

  61. Hodge JM, Shah R, McCullough ML, Gapstur SM, Patel AV (2020) Validation of self-reported height and weight in a large, nationwide cohort of U.S. adults. PLoS ONE 15:e0231229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Lucas R, Azevedo A, Barros H (2008) Self-reported data on reproductive variables were reliable among postmenopausal women. J Clin Epidemiol 61:945–950

    Article  PubMed  Google Scholar 

  63. Slanger T, Mutschelknauss E, Kropp S, Braendle W, Flesch-Janys D, Chang-Claude J (2007) Test-retest reliability of self-reported reproductive and lifestyle data in the context of a German case–control study on breast cancer and postmenopausal hormone therapy. Ann Epidemiol 17:993–998

    Article  PubMed  Google Scholar 

  64. Cairns BJ, Liu B, Clennell S et al (2011) Lifetime body size and reproductive factors: comparisons of data recorded prospectively with self reports in middle age. BMC Med Res Methodol 11:7

    Article  PubMed  PubMed Central  Google Scholar 

  65. Soulakova JN, Hartman AM, Liu B, Willis GB, Augustine S (2012) Reliability of adult self-reported smoking history: data from the tobacco use supplement to the current population survey 2002–2003 cohort. Nicotine Tob Res 14:952–960

    Article  PubMed  PubMed Central  Google Scholar 

  66. Huerta M, Chodick G, Balicer RD, Davidovitch N, Grotto I (2005) Reliability of self-reported smoking history and age at initial tobacco use. Prev Med 41:646–650

    Article  PubMed  Google Scholar 

  67. van der Aalst CM, de Koning HJ (2016) Biochemical verification of the self-reported smoking status of screened male smokers of the Dutch-Belgian randomized controlled lung cancer screening trial. Lung Cancer 94:96–101

    Article  PubMed  Google Scholar 

  68. Hatziandreu EJ, Pierce JP, Fiore MC, Grise V, Novotny TE, Davis RM (1989) The reliability of self-reported cigarette consumption in the United States. Am J Public Health 79:1020–1023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Liu B, Henschke CI, Flores RM, Taioli E (2020) Serum cotinine verification of self-reported smoking status among adults eligible for lung cancer screening in the 1999–2018 national health and nutrition examination survey. Lung Cancer 144:49–56

    Article  PubMed  Google Scholar 

  70. Vartiainen E, Seppälä T, Lillsunde P, Puska P (2002) Validation of self reported smoking by serum cotinine measurement in a community-based study. J Epidemiol Community Health 56:167–170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Williams GD, Aitken SS, Malin H (1985) Reliability of self-reported alcohol consumption in a general population survey. J Stud Alcohol 46:223–227

    Article  CAS  PubMed  Google Scholar 

  72. Gruenewald PJ, Johnson FW (2006) The stability and reliability of self-reported drinking measures. J Stud Alcohol 67:738–745

    Article  PubMed  Google Scholar 

  73. Coburn SB, Stanczyk FZ, Falk RT et al (2019) Comparability of serum, plasma, and urinary estrogen and estrogen metabolite measurements by sex and menopausal status. Cancer Causes Control 30:75–86

    Article  PubMed  Google Scholar 

  74. Onizuka Y, Nagai K, Ideno Y et al (2019) Association between FSH, E1, and E2 levels in urine and serum in premenopausal and postmenopausal women. Clin Biochem 73:105–108

    Article  CAS  PubMed  Google Scholar 

  75. Toniolo PG, Levitz M, Zeleniuch-Jacquotte A et al (1995) A prospective study of endogenous estrogens and breast cancer in postmenopausal women. J Natl Cancer Inst 87:190–197

    Article  CAS  PubMed  Google Scholar 

  76. Yu H, Shu XO, Shi R et al (2003) Plasma sex steroid hormones and breast cancer risk in Chinese women. Int J Cancer 105:92–97

    Article  CAS  PubMed  Google Scholar 

  77. Missmer SA, Eliassen AH, Barbieri RL, Hankinson SE (2004) Endogenous estrogen, androgen, and progesterone concentrations and breast cancer risk among postmenopausal women. J Natl Cancer Inst 96:1856–1865

    Article  CAS  PubMed  Google Scholar 

  78. Hankinson SE, Eliassen AH (2007) Endogenous estrogen, testosterone and progesterone levels in relation to breast cancer risk. J Steroid Biochem Mol Biol 106:24–30

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Key TJ, Wang DY, Brown JB et al (1996) A prospective study of urinary oestrogen excretion and breast cancer risk. Br J Cancer 73:1615–1619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Onland-Moret NC, Kaaks R, van Noord PA et al (2003) Urinary endogenous sex hormone levels and the risk of postmenopausal breast cancer. Br J Cancer 88:1394–1399

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Fuhrman BJ, Schairer C, Gail MH et al (2012) Estrogen metabolism and risk of breast cancer in postmenopausal women. J Natl Cancer Inst 104:326–339

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This research was supported by pilot funding from the Florida Academic Cancer Center Alliance (FACCA) and the UF Health Cancer Center Bridge Funding. This work has been supported in part by the Tissue Core and the Proteomics & Metabolomics Core facilities at the H. Lee Moffitt Cancer Center & Research Institute, an NCI designated Comprehensive Cancer Center (Grant No. P30-CA076292). The authors would like to thank Martin Abrams at Moffitt Cancer Center Clinical Laboratory for performing the creatinine assays.

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Authors and Affiliations

  1. Department of Epidemiology, College of Public Health and Health Professions and College of Medicine, University of Florida, 2004 Mowry Rd., Gainesville, FL, 32610, USA

    Lusine Yaghjyan, Shannan Rich & Rebecca J. Austin-Datta

  2. Proteomics & Metabolomics Core, H. Lee Moffitt Cancer Center & Research Institute, Tampa, FL, USA

    Lancia N. F. Darville, Jayden Cline & John M. Koomen

  3. Department of Cancer Epidemiology, H. Lee Moffitt Cancer Center & Research Institute, Tampa, FL, USA

    Yessica C. Martinez, Shelley S. Tworoger & Kathleen M. Egan

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  1. Lusine Yaghjyan
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The study was approved by the Moffitt Cancer Center and UF Institutional Review Boards (UF: IRB 201500572 and IRB 201600709; Moffitt Cancer Center Advarra IRB# Pro00014574). Women were offered a $25 gift card for their participation. The study was performed in accordance with the ethical standards as laid down in the 1964 Declaration of Helsinki and its later amendments.

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Yaghjyan, L., Darville, L.N.F., Cline, J. et al. Associations of established breast cancer risk factors with urinary estrogens in postmenopausal women. Cancer Causes Control 33, 279–291 (2022). https://doi.org/10.1007/s10552-021-01528-9

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