Skip to main content

Advertisement

Log in

Endometriosis and mammographic density measurements in the Nurses’ Health Study II

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

Abstract

Purpose

Endometriosis and mammographic density have been hypothesized to be influenced by sex steroid hormonal exposures in adolescence and early adulthood. We investigated the association between endometriosis and mammographic density, a consistent and independent risk factor for breast cancer.

Methods

We conducted a cross-sectional analysis among 1,581 pre- and postmenopausal women not previously diagnosed with breast cancer in the Nurses’ Health Study II cohort. We measured average percent mammographic density and absolute dense and non-dense breast area using a validated computer-assisted method. Multivariable linear regression was used to estimate the association between endometriosis and mammographic density among pre- and postmenopausal women separately.

Results

Among premenopausal women, average percent mammographic density was 43.1 % among women with endometriosis (n = 91) and 40.5 % among women without endometriosis (n = 1,150). Endometriosis was not associated significantly with mammographic density among premenopausal (% difference = 2.00 percentage points 95 % CI −1.33, 5.33) or among postmenopausal women (% difference = −0.89 percentage points 95 % CI −5.10, 3.33). Among premenopausal women, there was heterogeneity by BMI at age 18 (p value = 0.003), with a suggested association among those who were lean at age 18 (BMI < 20.6 kg/m2) (% difference = 3.74 percentage points 95 % CI −0.29, 7.78).

Conclusion

Endometriosis was not found to be associated with overall measurements of mammographic density.

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

Similar content being viewed by others

References

  1. Giudice LC, Kao LC (2004) Endometriosis. Lancet 364:1789–1799

    Article  PubMed  Google Scholar 

  2. Missmer SA, Cramer DW (2003) The epidemiology of endometriosis. Obstet Gynecol Clin N Am 30:1–19 vii

    Article  Google Scholar 

  3. Missmer SA, Hankinson SE, Spiegelman D et al (2004) Reproductive history and endometriosis among premenopausal women. Obstet Gynecol 104:965–974

    Article  PubMed  Google Scholar 

  4. Parente Barbosa C, Bentes De Souza AM, Bianco B, Christofolini DM (2011) The effect of hormones on endometriosis development. Minerva Ginecol 63:375–386

    CAS  PubMed  Google Scholar 

  5. Jones RK, Bulmer JN, Searle RF (1998) Phenotypic and functional studies of leukocytes in human endometrium and endometriosis. Hum Reprod Update 4:702–709

    Article  CAS  PubMed  Google Scholar 

  6. Osteen KG, Rodgers WH, Gaire M, Hargrove JT, Gorstein F, Matrisian LM (1994) Stromal–epithelial interaction mediates steroidal regulation of metalloproteinase expression in human endometrium. Proc Natl Acad Sci USA 91:10129–10133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Giudice LC (2010) Clinical practice. Endometriosis. N Engl J Med 362:2389–2398

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Kvaskoff M, Mu F, Terry KL, Harris HR, Poole EM, Farland L, Missmer SA (2015) Endometriosis: a high-risk population for major chronic diseases? Hum Reprod Update 21(4):500–516

    Article  PubMed  PubMed Central  Google Scholar 

  9. Anifantaki F, Boutas I, Kalampokas T, Kalampokas E, Sofoudis C, Salakos N (2016) Association of endometriosis and breast cancer: mini review of the literature. Arch Gynecol Obstet 293:5–10

    Article  CAS  PubMed  Google Scholar 

  10. Munksgaard PS, Blaakaer J (2011) The association between endometriosis and gynecological cancers and breast cancer: a review of epidemiological data. Gynecol Oncol 123:157–163

    Article  PubMed  Google Scholar 

  11. Pontikaki A, Sifakis S, Spandidos DA (2016) Endometriosis and breast cancer: a survey of the epidemiological studies. Oncol Lett 11:23–30

    PubMed  Google Scholar 

  12. Farland LV, Tamimi RM, Eliassen AH, Spiegelman D, Hankinson SE, Chen WY, Missmer SA. The relationship between laparoscopically confirmed endometriosis and breast cancer in the Nurses’ Health Study II. Obstet Gynecol (in press)

  13. Mogensen JB, Kjær SK, Mellemkjær L, Jensen A (2016) Endometriosis and risks for ovarian, endometrial and breast cancers: a nationwide cohort study. Gynecol Oncol S0090–8258(16):30964–30967

    Google Scholar 

  14. Weiss HA, Brinton LA, Potischman NA et al (1999) Breast cancer risk in young women and history of selected medical conditions. Int J Epidemiol 28:816–823

    Article  CAS  PubMed  Google Scholar 

  15. Borgfeldt C, Andolf E (2004) Cancer risk after hospital discharge diagnosis of benign ovarian cysts and endometriosis. Acta Obstet Gynecol Scand 83:395–400

    Article  PubMed  Google Scholar 

  16. Brinton LA, Gridley G, Persson I, Baron J, Bergqvist A (1997) Cancer risk after a hospital discharge diagnosis of endometriosis. Am J Obstet Gynecol 176:572–579

    Article  CAS  PubMed  Google Scholar 

  17. Melin A, Sparen P, Bergqvist A (2007) The risk of cancer and the role of parity among women with endometriosis. Hum Reprod 22:3021–3026

    Article  CAS  PubMed  Google Scholar 

  18. Moseson M, Koenig KL, Shore RE, Pasternack BS (1993) The influence of medical conditions associated with hormones on the risk of breast cancer. Int J Epidemiol 22:1000–1009

    Article  CAS  PubMed  Google Scholar 

  19. Schairer C, Persson I, Falkeborn M, Naessen T, Troisi R, Brinton LA (1997) Breast cancer risk associated with gynecologic surgery and indications for such surgery. Int J Cancer 70:150–154

    Article  CAS  PubMed  Google Scholar 

  20. Kok VC, Tsai HJ, Su CF, Lee CK (2015) The risks for ovarian, endometrial, breast, colorectal, and other cancers in women with newly diagnosed endometriosis or adenomyosis: a population-based study. Int J Gynecol Cancer 25:968–976

    Article  PubMed  Google Scholar 

  21. Nichols HB, Visvanathan K, Newcomb PA et al (2011) Bilateral oophorectomy in relation to risk of postmenopausal breast cancer: confounding by nonmalignant indications for surgery? Am J Epidemiol 173:1111–1120

    Article  PubMed  PubMed Central  Google Scholar 

  22. Chuang SC, Wu GJ, Lu YS, Lin CH, Hsiung CA (2015) Associations between medical conditions and breast cancer risk in asians: a nationwide population-based study in Taiwan. PLoS One 10:e0143410

    Article  PubMed  PubMed Central  Google Scholar 

  23. Bertelsen L, Mellemkjaer L, Frederiksen K et al (2007) Risk for breast cancer among women with endometriosis. Int J Cancer 120:1372–1375

    Article  CAS  PubMed  Google Scholar 

  24. Melin A, Sparen P, Persson I, Bergqvist A (2006) Endometriosis and the risk of cancer with special emphasis on ovarian cancer. Hum Reprod 21:1237–1242

    Article  CAS  PubMed  Google Scholar 

  25. Olson JE, Cerhan JR, Janney CA, Anderson KE, Vachon CM, Sellers TA (2002) Postmenopausal cancer risk after self-reported endometriosis diagnosis in the Iowa Women’s Health Study. Cancer 94:1612–1618

    Article  PubMed  Google Scholar 

  26. Venn A, Watson L, Bruinsma F, Giles G, Healy D (1999) Risk of cancer after use of fertility drugs with in vitro fertilisation. Lancet 354:1586–1590

    Article  CAS  PubMed  Google Scholar 

  27. Matta JL, Flores I, Morales LM, Monteiro J, Alvarez-Garriga C, Bayona M (2013) Women with endometriosis have a higher DNA repair capacity and diminished breast cancer risk. Mol Cancer Biol 1(1). doi:10.9777/mcb.2013.10005

  28. Baron JA, Weiderpass E, Newcomb PA et al (2001) Metabolic disorders and breast cancer risk (United States). Cancer Causes Control 12:875–880

    Article  CAS  PubMed  Google Scholar 

  29. Brinton LA, Westhoff CL, Scoccia B et al (2005) Causes of infertility as predictors of subsequent cancer risk. Epidemiology 16:500–507

    Article  PubMed  Google Scholar 

  30. Gemmill JA, Stratton P, Cleary SD, Ballweg ML, Sinaii N (2010) Cancers, infections, and endocrine diseases in women with endometriosis. Fertil Steril 94:1627–1631

    Article  PubMed  Google Scholar 

  31. Morales L, Alvarez-Garriga C, Matta J et al (2013) Factors associated with breast cancer in Puerto Rican women. J Epidemiol Glob Health 3:205–215

    Article  PubMed  Google Scholar 

  32. Byrne C, Schairer C, Wolfe J et al (1995) Mammographic features and breast cancer risk: effects with time, age, and menopause status. J Natl Cancer Inst 87:1622–1629

    Article  CAS  PubMed  Google Scholar 

  33. Boyd NF, Martin LJ, Bronskill M, Yaffe MJ, Duric N, Minkin S (2010) Breast tissue composition and susceptibility to breast cancer. J Natl Cancer Inst 102:1224–1237

    Article  PubMed  PubMed Central  Google Scholar 

  34. McCormack VA, dos Santos SilvaI (2006) Breast density and parenchymal patterns as markers of breast cancer risk: a meta-analysis. Cancer Epidemiol Biomark Prev 15:1159–1169

    Article  Google Scholar 

  35. Gierach GL, Patel DA, Falk RT et al (2015) Relationship of serum estrogens and metabolites with area and volume mammographic densities. Horm Cancer 6:107–119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Bertrand KA, Eliassen AH, Hankinson SE et al (2012) Urinary estrogens and estrogen metabolites and mammographic density in premenopausal women. Breast Cancer Res Treat 136:277–287

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Martin LJ, Boyd NF (2008) Mammographic density. Potential mechanisms of breast cancer risk associated with mammographic density: hypotheses based on epidemiological evidence. Breast Cancer Res 10:201

    Article  PubMed  PubMed Central  Google Scholar 

  38. Boyd NF, Martin LJ, Yaffe MJ, Minkin S (2006) Mammographic density: a hormonally responsive risk factor for breast cancer. J Br Menopause Soc 12:186–193

    Article  PubMed  Google Scholar 

  39. Greendale GA, Reboussin BA, Slone S, Wasilauskas C, Pike MC, Ursin G (2003) Postmenopausal hormone therapy and change in mammographic density. J Natl Cancer Inst 95:30–37

    Article  CAS  PubMed  Google Scholar 

  40. Harvey JA, Pinkerton JV, Herman CR (1997) Short-term cessation of hormone replacement therapy and improvement of mammographic specificity. J Natl Cancer Inst 89:1623–1625

    Article  CAS  PubMed  Google Scholar 

  41. Leung W, Goldberg F, Zee B, Sterns E (1997) Mammographic density in women on postmenopausal hormone replacement therapy. Surgery 122:669–673 discussion 73–74

    Article  CAS  PubMed  Google Scholar 

  42. Lundstrom E, Wilczek B, von Palffy Z, Soderqvist G, von Schoultz B (1999) Mammographic breast density during hormone replacement therapy: differences according to treatment. Am J Obstet Gynecol 181:348–352

    Article  CAS  PubMed  Google Scholar 

  43. McTiernan A, Martin CF, Peck JD et al (2005) Estrogen-plus-progestin use and mammographic density in postmenopausal women: Women’s Health Initiative randomized trial. J Natl Cancer Inst 97:1366–1376

    Article  CAS  PubMed  Google Scholar 

  44. Persson I, Thurfjell E, Holmberg L (1997) Effect of estrogen and estrogen-progestin replacement regimens on mammographic breast parenchymal density. J Clin Oncol 15:3201–3207

    CAS  PubMed  Google Scholar 

  45. Stomper PC, Van Voorhis BJ, Ravnikar VA, Meyer JE (1990) Mammographic changes associated with postmenopausal hormone replacement therapy: a longitudinal study. Radiology 174:487–490

    Article  CAS  PubMed  Google Scholar 

  46. Vachon CM, Kuni CC, Anderson K, Anderson VE, Sellers TA (2000) Association of mammographically defined percent breast density with epidemiologic risk factors for breast cancer (United States). Cancer Causes Control 11:653–662

    Article  CAS  PubMed  Google Scholar 

  47. Rutter CM, Mandelson MT, Laya MB, Seger DJ, Taplin S (2001) Changes in breast density associated with initiation, discontinuation, and continuing use of hormone replacement therapy. J Am Med Assoc 285:171–176

    Article  CAS  Google Scholar 

  48. Yaghjyan L, Colditz GA, Rosner B, Tamimi RM (2015) Mammographic breast density and breast cancer risk: interactions of percent density, absolute dense, and non-dense areas with breast cancer risk factors. Breast Cancer Res Treat 150:181–189

    Article  PubMed  PubMed Central  Google Scholar 

  49. Tamimi RM, Hankinson SE, Colditz GA, Byrne C (2005) Endogenous sex hormone levels and mammographic density among postmenopausal women. Cancer Epidemiol Biomark Prev 14:2641–2647

    Article  CAS  Google Scholar 

  50. Pettersson A, Graff RE, Ursin G, Santos Silva ID, McCormack V, Baglietto L, Vachon C, Bakker MF, Giles GG, Chia KS, Czene K, Eriksson L, Hall P, Hartman M, Warren RM, Hislop G, Chiarelli AM, Hopper JL, Krishnan K, Li J, Li Q, Pagano I, Rosner BA, Wong CS, Scott C, Stone J, Maskarinec G, Boyd NF, van Gils CH, Tamimi RM (2014) Mammographic density phenotypes and risk of breast cancer: a meta-analysis. J Natl Cancer Inst 106(5)

  51. Pettersson A, Hankinson SE, Willett WC, Lagiou P, Trichopoulos D, Tamimi RM (2011) Nondense mammographic area and risk of breast cancer. Breast Cancer Res 13:R100

    Article  PubMed  PubMed Central  Google Scholar 

  52. Lokate M, Peeters PH, Peelen LM, Haars G, Veldhuis WB, van Gils CH (2011) Mammographic density and breast cancer risk: the role of the fat surrounding the fibroglandular tissue. Breast Cancer Res 13:R103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Stone J, Ding J, Warren RM, Duffy SW, Hopper JL (2010) Using mammographic density to predict breast cancer risk: dense area or percentage dense area. Breast Cancer Res 12:R97

    Article  PubMed  PubMed Central  Google Scholar 

  54. Byng JW, Boyd NF, Little L et al (1996) Symmetry of projection in the quantitative analysis of mammographic images. Eur J Cancer Prev 5:319–327

    Article  CAS  PubMed  Google Scholar 

  55. Tamimi RM, Byrne C, Colditz GA, Hankinson SE (2007) Endogenous hormone levels, mammographic density, and subsequent risk of breast cancer in postmenopausal women. J Natl Cancer Inst 99:1178–1187

    Article  CAS  PubMed  Google Scholar 

  56. Rosner B, Cook N, Portman R, Daniels S, Falkner B (2008) Determination of blood pressure percentiles in normal-weight children: some methodological issues. Am J Epidemiol 167:653–666

    Article  CAS  PubMed  Google Scholar 

  57. Hediger ML, Hartnett HJ, Louis GM (2005) Association of endometriosis with body size and figure. Fertil Steril 84:1366–1374

    Article  PubMed  PubMed Central  Google Scholar 

  58. Lafay Pillet MC, Schneider A, Borghese B et al (2012) Deep infiltrating endometriosis is associated with markedly lower body mass index: a 476 case–control study. Hum Reprod 27:265–272

    Article  PubMed  Google Scholar 

  59. Bertrand KA, Baer HJ, Orav EJ et al (2015) Body fatness during childhood and adolescence and breast density in young women: a prospective analysis. Breast Cancer Res 17:95

    Article  PubMed  PubMed Central  Google Scholar 

  60. Andersen ZJ, Baker JL, Bihrmann K, Vejborg I, Sorensen TI, Lynge E (2014) Birth weight, childhood body mass index, and height in relation to mammographic density and breast cancer: a register-based cohort study. Breast Cancer Res 16:R4

    Article  PubMed  PubMed Central  Google Scholar 

  61. Bertrand KA, Tamimi RM, Scott CG et al (2013) Mammographic density and risk of breast cancer by age and tumor characteristics. Breast Cancer Res 15:R104

    Article  PubMed  PubMed Central  Google Scholar 

  62. Vitonis AF, Baer HJ, Hankinson SE, Laufer MR, Missmer SA (2010) A prospective study of body size during childhood and early adulthood and the incidence of endometriosis. Hum Reprod 25:1325–1334

    Article  PubMed  PubMed Central  Google Scholar 

  63. Shah DK, Correia KF, Vitonis AF, Missmer SA (2013) Body size and endometriosis: results from 20 years of follow-up within the Nurses’ Health Study II prospective cohort. Hum Reprod 28:1783–1792

    Article  PubMed  PubMed Central  Google Scholar 

  64. Harris RE, Chlebowski RT, Jackson RD et al (2003) Breast cancer and nonsteroidal anti-inflammatory drugs: prospective results from the Women’s Health Initiative. Cancer Res 63:6096–6101

    CAS  PubMed  Google Scholar 

  65. Samimi G, Colditz GA, Baer HJ, Tamimi RM (2008) Measures of energy balance and mammographic density in the Nurses’ Health Study. Breast Cancer Res Treat 109:113–122

    Article  PubMed  Google Scholar 

  66. Harris HR, Tamimi RM, Willett WC, Hankinson SE, Michels KB (2011) Body size across the life course, mammographic density, and risk of breast cancer. Am J Epidemiol 174:909–918

    Article  PubMed  PubMed Central  Google Scholar 

  67. Dorgan JF, Klifa C, Shepherd JA et al (2012) Height, adiposity and body fat distribution and breast density in young women. Breast Cancer Res 14:R107

    Article  PubMed  PubMed Central  Google Scholar 

  68. Baer HJ, Tworoger SS, Hankinson SE, Willett WC (2010) Body fatness at young ages and risk of breast cancer throughout life. Am J Epidemiol 171:1183–1194

    Article  PubMed  PubMed Central  Google Scholar 

  69. Nyante SJ, Sherman ME, Pfeiffer RM, Berrington de Gonzalez A, Brinton LA, Aiello Bowles EJ, Hoover RN, Glass A, Gierach GL (2015) Prognostic significance of mammographic density change after initiation of tamoxifen for ER-positive breast cancer. J Natl Cancer Inst 107(3)

  70. Cuzick J, Warwick J, Pinney E et al (2011) Tamoxifen-induced reduction in mammographic density and breast cancer risk reduction: a nested case–control study. J Natl Cancer Inst 103:744–752

    Article  CAS  PubMed  Google Scholar 

  71. Boyd NF, Byng JW, Jong RA et al (1995) Quantitative classification of mammographic densities and breast cancer risk: results from the Canadian National Breast Screening Study. J Natl Cancer Inst 87:670–675

    Article  CAS  PubMed  Google Scholar 

  72. Zondervan KT, Cardon LR, Kennedy SH (2002) What makes a good case–control study? Design issues for complex traits such as endometriosis. Hum Reprod 17:1415–1423

    Article  PubMed  Google Scholar 

  73. Rothman KJ, Greenland S, Lash TL (2008) Modern epidemiology, 3rd edn. Lippincott Williams & Wilkins, Philidelphia

    Google Scholar 

  74. Jones KL, Buzdar AU (2004) A review of adjuvant hormonal therapy in breast cancer. Endocr Relat Cancer 11:391–406

    Article  CAS  PubMed  Google Scholar 

  75. Spicer DV, Ursin G, Parisky YR et al (1994) Changes in mammographic densities induced by a hormonal contraceptive designed to reduce breast cancer risk. J Natl Cancer Inst 86:431–436

    Article  CAS  PubMed  Google Scholar 

  76. Saltiel E, Garabedian-Ruffalo SM (1991) Pharmacologic management of endometriosis. Clin Pharm 10:518–531

    CAS  PubMed  Google Scholar 

  77. Rosner B, Glynn RJ, Tamimi RM et al (2013) Breast cancer risk prediction with heterogeneous risk profiles according to breast cancer tumor markers. Am J Epidemiol 178:296–308

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This work was supported by National Institutes of Health, National Cancer Institute [UM1 CA176726, 3R25CA057711 to LVF], National Institute of Child Health and Human Development [HD57210, T32HD060454 to LVF], the Dana Farber and Harvard Cancer Center Mazzone Award, and the Breast Cancer Research Foundation.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Leslie V. Farland.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Farland, L.V., Tamimi, R.M., Eliassen, A.H. et al. Endometriosis and mammographic density measurements in the Nurses’ Health Study II. Cancer Causes Control 27, 1229–1237 (2016). https://doi.org/10.1007/s10552-016-0801-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10552-016-0801-y

Keywords

Navigation