Cellular and hormonal content of breast nipple aspirate fluid in relation to the risk of breast cancer

Biomarkers in Medicine

Volumn 2, Issue 5, 2008, Pages 479-493

  Khan, Seema A ^a   Chatterton Jr , Robert T ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Breast cancer; Cytologic atypia; Estradiol; Estrogen response proteins; Hormones; Nipple aspiration fluid; Risk

Indexed keywords

ANDROSTENEDIONE; AROMATASE INHIBITOR; ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR; ESTRONE SULFATE; ETHINYLESTRADIOL; GROWTH FACTOR; NONSTEROID ANTIINFLAMMATORY AGENT; ORAL CONTRACEPTIVE AGENT; PRASTERONE; PRASTERONE SULFATE; PROGESTERONE RECEPTOR; SEX HORMONE BINDING GLOBULIN; SOMATOMEDIN C; STERYL SULFATASE;

ANTIINFLAMMATORY ACTIVITY; BREAST CANCER; BREAST CARCINOGENESIS; CANCER RISK; CELL PROLIFERATION; DIAGNOSTIC ACCURACY; HORMONE BLOOD LEVEL; HORMONE INHIBITION; HORMONE SYNTHESIS; HORMONE URINE LEVEL; HUMAN; MAMMOGRAPHY; NIPPLE ASPIRATION; NONHUMAN; OXIDATIVE STRESS; POSTMENOPAUSE; PROTEIN CONTENT; REVIEW;

EID: 59949102350     PISSN: 17520363     EISSN: None     Source Type: Journal    
DOI: 10.2217/17520363.2.5.479     Document Type: Review

References (81)

1. Vona-Davis L, Howard-McNatt M, Rose DP: Adiposity, Type 2 diabetes and the metabolic syndrome in breast cancer. Obes. Rev. 8, 395-408 (2007).
2. Friedenreich CM. Orenstein MR: Physical activity and cancer prevention: etiologic evidence and biological mechanisms. J. Nutr. 132(Suppl. 11), S3456-S3464 (2002).
3. Kendall A, Folkerd EJ, Dowsen M: Influences on circulating oestrogens in postmenopausal women: relationship with breast cancer. J. Steroid Biochem. Mol. Biol. 103. 99-109 (2007).
4. Gail MH, Brinton LA, Byar DP et al.: Projecting individualized probabilities of developing breast cancer for white females who are being examined annually. J. Natl Cancer Inst. 81, 1879-1886 (1989).
5. Fisher B, Costantino JP, Wickerham DL et al.: Tamoxifen for prevention of breast cancer: report of the National Surgical Adjuvant Breast and Bowel Project P-1 Study. J. Natl Cancer Inst. 90, 1371-1388 (1998).
6. Rockhill B. Spiegelman D, Byrne C, Hunter DJ, Colditz GA: Validation of the Gail et al. model of breast cancer risk prediction and implications for chemoprevention. J. Natl Cancer Inst. 93, 358-366 (2001).
7. Tyrer J, Duffy SW, Cuzick J: A breast cancer prediction model incorporating familial and personal risk factors. Stat. Med. 23, 1111-1130 (2004).
8. Kabuto M, Akiba, S, Stevens RG, Neriishi K, Land CE: A prospective study of estradiol and breast cancer in Japanese women. Cancer Epidemiol. Biomarkers Prev. 9, 575-579 (2000).
9. Toniolo PG, Levitz M, Zeleniuch-Jacquotte A et al.: A prospective study of endogenous estrogen and breast cancer in postmenopausal women. J. Natl Cancer Inst. 87, 190-197 (1995).
10. Key T, Appleby P, Barnes I, Reeves G: Endogenous sex hormones and breast cancer in postmenopausal women: reanalysis of nine prospective studies. J. Natl Cancer Inst. 94, 606-616 (2002).
11. Hankinson SE, Willett WC, Manson JE et al.: Plasma sex steroid hormone levels and risk of breast cancer in postmenopausal women. J Natl Cancer Inst. 90, 1292-1299 (1998).
12. Thomas HV, Reeves GK, Key TJ: Endogenous estrogen and postmenopausal breast cancer: a quantitative review. Cancer Causes Control 8, 922-928 (1997).
13. Tworoger SS, Missmer SA, Barbleri RL. Willett WC, Colditz GA, Hankinson SE: Plasma sex hormone concentrations and subsequent risk of breast cancer among women using postmenopausal hormones. J Natl Cancer Inst. 97, 595-602 (2005).
14. Kaaks R, Berrino F, Key T et al.: Serum sex steroids in premenopausal women and breast cancer risk within the European Prospective Investigation into Cancer and Nutrition (EPIC). J. Natl Cancer Inst. 97, 755-765 (2005).
15. Page JH, Colditz GA, Rifai N, Barbieri RL, Willett WC, Hankinson SE: Plasma adrenal androgens and risk of breast cancer in premenopausal women. Cancer Epidemiol. Biomarkers Prev. 13, 1032-1036 (2004).
16. Eliassen AH, Missmer SA, Tworoger SS et al.: Endogenous steroid hormone concentrations and risk of breast cancer among premenopausal women. J. Natl Cancer Inst. 98, 1406-1415 (2006).
17. Muti P, Trevisan M, Michell A et al.: Reliability of serum hormones in premenopausal and postmenopausal women over a one-year period. Cancer Epidemiol. Biomarkers Prev. 5, 917-922 (1996).
18. Chatterton RT Jr, Mateo ET, Hou N et al.: Characteristics of salivary profiles of oestradiol and progesterone in premenopausal women. J. Endocrinol. 186(1), 77-84 (2005).
19. Shaughnessy JA, Kelloff GJ, Gordon GB et al.: Treatment and prevention of Intraepithelial neoplasia: an important target for accelerated new agent development: recommendations of the American Association for Cancer Research Task Force on the Treatment and Prevention of Intraepithetial Neoplasia. Clin. Cancer Res. 8, 314-346 (2002).
20. Dupont WD, Page DL: Risk factors for breast cancer in women with proliferative breast disease. N. Engl. J. Med. 312, 146-151 (1985).
21. Carter CL, Corle DK, Micozzi MS, Schatzkin A, Taylor PR: A Prospective study of the development of breast cancer in 16,692 women with benign breast disease. Am. J. Epidemiol. 123(3), 467-477 (1988).
22. London SJ, Connolly JL. Schnitt SJ, Colditz GA: A prospective study of benign breast disease and the risk of breast cancer. JAMA 267, 941-944 (1992).
23. Hartmann LC, Sellers TA, Frost MH et al.: Benign breast disease and the risk of breast cancer. N. Engl. J. Med. 353, 229-237 (2005).
24. Hargreaves DF, Knox F, Swindell R, Potten CS, Bundred NJ: Epithelial proliferation and hormone receptor status in the normal post-menopausal breast and the effects of hormone replacement therapy. Br. J. Cancer 78, 945-949 (1998).
25. McCormack VA, dos Santos Silva SS: I. Breast density and parenchymal patterns as markers of breast cancer risk: a meta-analysis. Cancer Epidemiol. Biomarkers Prev. 15, 1159-1169 (2006).
26. Byrne C, Schairer C, Wolfe J et al.: Mammographic features and breast cancer risk: effects with time, age, and menopause status. J Natl Cancer Inst. 87, 1622-1629 (1995).
27. Boyd NF, Guo H, Martin LJ et al.: Mammographic density and the risk and detection of breast cancer. N. Engl. J. Med. 356, 227-236 (2007).
28. Greendale GA, Reboussin BA, Sie A et al.: Effects of estrogen and estrogen-progestin on mammographic parenchymal density. Postmenopausal Estrogen/Progestin Interventions (PEPI) Investigators. Ann. Intern. Med. 130, 262-269 (1999).
29. Rutter CM, Mandelson MT, Laya MB, Seger DJ, Taplin S: Changes in breast density associated with initiation, discontinuation, and continuing use of hormone replacement therapy. JAMA 295, 171-176 (2001).
30. Cuzick J, Warwick J, Pinney E, Warren RM, Duffy SW: Tamoxifen and breast density in women at increased risk of breast cancer. J. Natl Cancer Inst. 96, 621-628 (2004).
31. Spicer DV, Ursin G, Parisky YR et al.: Changes in mammographic densities induced by a hormonal contraceptive designed to reduce breast cancer risk. J. Natl Cancer Inst. 86, 431-436 (1994).
32. Verheus M, Peeters PH, van Noord PA, van der Schouw YT, Grobbee DE, van Gils CH: No relationship between circulating levels of sex steroids and mammographic breast density: the Prospect-EPIC cohort. Breast Cancer Res. 9, R53 (2007).
33. Tamimi RM, Byrne C, Colditz GA, Hankinson SE: Endogenous hormone levels, mammographic density, and subsequent risk of breast cancer in postmenopausal women. J. Natl Cancer Inst. 99, 1178-1187 (2007).
34. Boyd NF, Stone J, Martin LJ et al: The association of breast mitogens with mammographic densities. Br. J. Cancer 87, 876-882 (2002).
35. Bremnes Y, Ursin G, Bjurstam N, Rinaldi S, Kaaks R, Gram IT: Endogenous sex hormones, prolactin and mammographic density in postmenopausal Norwegian women. Int. J. Cancer 121, 2506-2511 (2007).
36. Tworoger SS, Eliassen AH, Sluss P, Hankinson SE: A prospective study of plasma prolactin concentrations and risk of premenopausal and postmenopausal breast cancer. J. Clin. Oncol. 25, 1482-1488 (2007).
37. Greendale GA, Huang MH, Ursin G et al.: Serum prolactin levels are positively associated with mammographic density in postmenopausal women. Breast Cancer Res. Treat. 105, 337-346 (2007).
38. Vorherr H: Human lactation and breast feeding. In: Lactation: A Comprehensive Treatise. Larson BL (Ed.). Academic Press, New York, NY, USA 181-280 (1978).
39. Damiani S, Cattani MG, Buonamici L, Eusebi V: Mammary foam cells. Characterization by immunohistochemistry and in situ hybridization. Virchows Arch. 432, 433-440 (1998).
40. Mor G, Yue W, Santen RJ et al.: Macrophages, estrogen and the microenvironment of breast cancer. J. Steroid Biochem. Mol. Biol. 67, 403-411 (1998).
41. Miller WR, Hawkins RA, Creel RJ, Forrest AP: Oestrogen in breast fluid. Lancet 2, 1179 (1977).
42. Chatterton RT, Geiger AS, Khan SA: Influence of ovarian secretions, oral contraceptives, and hormone replacement therapy on progesterone concentrations in breast fluids. Breast Cancer Res. 82(2), S110 (2004).
43. Papanicolaou GN, Holmquist DG, Bader GM, Falk EA: Exfoliative cytology of the human mammary gland and its value in the diagnosis of cancer and other diseases of the breast. Cancer 11(2), 377-409 (1958).
44. Sartorius OW, Smith HS, Morris P, Benedict D, Friesen L: Cytologic evaluation of breast fluid in the detection of breast disease. J. Natl Cancer Inst. 59, 1073-1080 (1977).
45. Sauter ER, Ross E, Daly M et al.: Nipple aspirate fluid: a promising non-invasive method to identify cellular markers of breast cancer risk. Br. J. Cancer 76, 494-501 (1997).
46. Wrensch MR, Petrakis NL, Gruenke LD et al.: Factors associated with obtaining nipple aspirate fluid: analysis of (1428) women and literature review. Breast Cancer Res. Treat 15, 39-51 (1990).
47. Baltzell KA, Wrensch M, Sison JD: A descriptive study of variables associated with obtaining nipple aspirate fluid in a cohort of non-lactating women. BMC Womens Health 6, 15 (2006).
48. Huang Y, Anderson KE, Nagamani M, Grady JJ, Lu LJ: Dietary Intake of lactose as a strong predictor for secretor status of nipple aspirate fluid in healthy premenopausal nonlactating women. Clin. Cancer Res. 14, 1386-1392 (2008).
49. Gann PH, Geiger AS, Helenowski IB, Vonesh EF, Chatterton RT. Estrogen and progesterone levels in nipple aspirate fluid of healthy premenopausal women: relationship to steroid precursors and response proteins. Cancer Epidemiol. Biomarkers Prev. 15, 39-44 (2006).
50. Chatterton RT Jr, Geiger AS, Gann PH, Khan SA: Formation of estrone and estradiol from estrone sulfate by normal breast parenchymal tissue. J. Steroid Biochem. Mol. Biol. 86, 159-166 (2003).
51. Thijssen JH, van Landeghem AA, Poortman J: Uptake and concentration of steroid hormones in mammary tissues. Ann. NY Acad. Sci. 464, 106-116 (1986).
52. Blankenstein MA, Szymczak J, Daroszewski J, Milewicz A, Thijssen JH: Estrogens in plasma and fatty tissue from breast cancer patients and women undergoing surgery for non-oncological reasons. Gynecol. Endocrinol. 6, 13-17 (1992).
53. Geisler J: Breast cancer tissue estrogens and their manipulation with aromatase inhibitors and inactivators. J. Steroid Biochem. Mol. Biol. 86, 245-253 (2003).
54. Bulun SE, Sharda G, Rink J, Sharma S, Simpson ER: Distribution of aromatase P450 transcripts and adipose fibroblasts in the human breast. J. Clin. Endocrinol. Metab. 81, 1273-1277 (1996).
55. Chatterton RT Jr, Geiger AS, Khan SA, Helenowski IB, Jovanovic BD, Cann PH: Variation in estradiol, estradiol precursors, and estrogen-related products in nipple aspirate fluid from normal premenopausal women. Cancer Epidemiol. Biomarkers Prev. 13, 928-935 (2004).
56. Chatterton RT Jr, Geiger AS, Mateo ET, Helenowski IB, Gann PH: Comparison of hormone levels in nipple aspirate fluid of pre- and postmenopausal women: effect of oral contraceptives and hormone replacement. J. Clin. Endocrinol. Metab. 90, 1686-1691 (2005).
57. Sauter ER, Tichansky DS. Chervoneva I. Diamandis EP: Circulating testosterone and prostate-specific antigen in nipple aspirate fluid and tissue are associated with breast cancer. Environ. Health Perspect. 110, 241-246 (2002).
58. Zaichuk T, Ivancic D, Scholtens D, Schiller C, Khan SA: Tissue-specific transcripts of human steroid sulfatase are under control of estrogen signaling pathways in breast carcinoma. J. Steroid Biochem. Mol. Biol. 105, 76-84 (2007).
59. Gann P, Chatterton R, Vogelsong K, Dupuis J, Ellman A: Mitogenic growth factors in breast fluid obtained from healthy women: evaluation of biological and extraneous sources of variability. Cancer Epidemiol. Biomarkers Prev. 6. 421-428 (1997).
60. Good P: Permutation Test: A Practical Guide to Resampling Methods far Testing Hypotheses (3rd Edition). Springer-Verlag, New York, NY, USA (2004).
61. Ernster VL, Wrensch MR, Petrakis NL et al.: Benign and malignant breast disease: initial study results of serum and breast fluid analyses of endogenous estrogens. J. Natl Cancer Inst. 79, 949-960 (1987).
62. Petrakis NL, Wrensch MR, Ernster VL et al.: Influence of pregnancy and lactation on serum and breast fluid estrogen levels: Implications for breast cancer risk. Int. J. Cancer 40, 587-591 (1987).
63. Bhandare D, Nayar R, Bryk M et al.: Endocrine biomarkers in ductal lavage samples from women at high risk for breast cancer. Cancer Epidemiol Biomarkers Prev. 14, 2620-2627 (2005).
64. Dickson RB, Huff KK, Spencer EM, Lippman ME: Induction of epidermal growth factor related polypeptides by 17β-estradiol in MCF-7 human breast cancer cells. Endocrinology 118, 138-142 (1986).
65. Kim H, Muller WJ: The role of the epidermal growth factor receptor family in mammary tumorigenesis and metastasis. Exp. Cell. Res. 253, 78-87 (1999).
66. Harding C, Osundeko O, Tetlow L, Faragher EB, Howell A, Bundred NJ: Hormonally-regulated proteins in breast secretions are markers of target organ sensitivity. Br. J. Cancer 82, 354-360 (2000).
67. Hargreaves DF, Potten CS, Harding C et al.: Two-week dietary soy supplementation has an estrogenic effect an normal premenopausal breast. J. Clin. Endocrinol. Metab. 84, 4017-4024 (1999).
68. Sartippour MR, Zhang L, Lu M, Wang H-J, Brooks MN: Nipple fluid basic fibroblast growth factor in patients with breast cancer. Cancer Epidem. Biomark. Prev. 14, 2995-2998 (2005).
69. Sauter ER, Chervoneva I, Diamandis A, Khosravi JM, Litwin S, Diamandis EP: Prostate-specific antigen and insulin-like growth factor binding protein-3 in nipple aspirate fluid are associated with breast cancer. Cancer Detect. Prev. 26, 149-157 (2002).
70. Sauter ER, Klein G, Wagner-Mann C, Diamandis EP: Prostate-specific antigen expression in nipple aspirate fluid is associated with advanced breast cancer. Cancer Detect. Prev. 28, 27-31 (2004).
71. Foretova L, Garber JE, Sadowsky NL et al.: Carcinoembryonic antigen in breast nipple aspirate fluid. Cancer Epidemiol. Biomarkers Prev. 7. 195-198 (1998).
72. Zhao Y, Verselis SJ, Klar N et al.: Nipple fluid carcinoembryonic antigen and prostate-specific antigen in cancer-bearing and tumor-free breasts. J. Clin. Oncol. 19, 1462-1467 (2001).
73. Alexander H, Stegner AL, Wagner-Mann C, Du Bois GC, Alexander S, Sauter ER: Proteomic analysis to identify breast cancer biomarkers in nipple aspirate fluid. Clin. Cancer Res. 10(22), 7500-7510 (2004).
74. Sauter ER, Shan S, Hewett JE, Speckman P, Du Bois GC: Proteomic analysis of nipple aspirate fluid using SELDI-TOF-MS. Int. J. Cancer 114, 791-796 (2005).
75. Pawlik TM, Hawke DH, Liu Y et al.: Proteomic analysis of nipple aspirate fluid from women with early-stage breast cancer using isotope-coded affinity tags and tandem mass spectrometry reveals differential expression of vitamin D binding protein. BMC Cancer 6, 68 (2006).
76. Pawlik TM, Fritsche H, Coombes KR et al.: Significant differences in nipple aspirate fluid protein expression between healthy women and those with breast cancer demonstrated by time-of-flight mass spectrometry. Breast Cancer Res. Treat. 89, 149-157 (2005).
77. Wrensch MR, Petrakis NL, King EB et al.: Breast cancer incidence in women with abnormal cytology in nipple aspirates of breast fluid. Am. J. Epidemiol. 135, 130-141 (1992).
78. Wrensch MR, Petrakis NL, Miike R et al.: Breast cancer risk in women with abnormal cytology in nipple aspirates of breast fluid. J. Natl Cancer Inst. 93, 1791-1798 (2001).
79. Chen G, Djuric Z: Detection of 2,6-cyclolycopene-1,5-diol in breast nipple aspirate fluids and plasma: a potential marker of oxidative stress. Cancer Epidemiol. Biomarkers Prev. 11, 1592-1596 (2002).
80. Kato I, Chen G, Djuric Z: Non-steroidal anti-inflammatory drug (NSAID) use and levels of a lipid oxidation marker in plasma and nipple aspirate fluids. Breast Cancer Res. Treat. 97, 145-148 (2006).
81. Mannello F, Tonti GA, Pagliarani S et al.: The 8-epimer of prostaglandin F(2α), a marker of lipid peroxidation and oxidative stress, is decreased in the nipple aspirate fluid of women with breast cancer. Int. J. Cancer 120, 1971-1976 (2007).