Top

Published in:

01-04-2006 | Review

The intraductal approach to the breast: raison d'être

Authors: Bonnie L King, Susan M Love

Published in: Breast Cancer Research | Issue 2/2006

Abstract

Opportunities for the detection, prediction, and treatment of breast cancer exist at three biological levels: systemically via the blood, at the whole organ level, and within the individual ductal lobular structures of the breast. This review covers the evaluation of approaches targeted to the ductal lobular units, where breast cancer begins. Studies to date suggest the presence of 5 to 12 independent ductal lobular systems per breast, each harboring complex cellular fluids contributed by local and systemic processes. New techniques for accessing and interrogating these systems offer the potential to gauge the microenvironment of the breast and distill biological risk profiles.

Available only for authorised users

Jensen HM, Rice JR, Wellings SR: Preneoplastic lesions in the human breast. Science. 1976, 191: 295-297.CrossRefPubMed

Ohtake T, Kimijima I, Fukushima T, Yasuda M, Sekikawa K, Takenoshita S, Abe R: Computer-assisted complete three-dimensional reconstruction of the mammary ductal/lobular systems: implications of ductal anastomoses for breast-conserving surgery. Cancer. 2001, 91: 2263-2272. 10.1002/1097-0142(20010615)91:12<2263::AID-CNCR1257>3.0.CO;2-5.CrossRefPubMed

Johnson-Maddux A, Ashfaq R, Cler L, Naftalis E, Leitch AM, Hoover S, Euhus DM: Reproducibility of cytologic atypia in repeat nipple duct lavage. Cancer. 2005, 103: 1129-1136. 10.1002/cncr.20884.CrossRefPubMed

Tot T: DCIS, cytokeratins, and the theory of the sick lobe. Virchows Arch. 2005, 447: 1-8. 10.1007/s00428-005-1274-7.CrossRefPubMed

Mai KT, Yazdi HM, Burns BF, Perkins DG: Pattern of distribution of intraductal and infiltrating ductal carcinoma: a three-dimensional study using serial coronal giant sections of the breast. Hum Pathol. 2000, 31: 464-474. 10.1053/hp.2000.6536.CrossRefPubMed

Holland R, Veling SH, Mravunac M, Hendriks JH: Histologic multifocality of Tis, T1-2 breast carcinomas. Implications for clinical trials of breast-conserving surgery. Cancer. 1985, 56: 979-990.CrossRefPubMed

King BL, Love SM, Rochman S, Kim JA: The Fourth International Symposium on the Intraductal Approach to Breast Cancer, Santa Barbara, California, 10–13 March 2005. Breast Cancer Res. 2005, 7: 198-204. 10.1186/bcr1288.CrossRefPubMedPubMedCentral

Cooper A: The Anatomy and Diseases of the Breast. 1845, Philadelphia: Lea and Blanchard

Love SM, Barsky SH: Anatomy of the nipple and breast ducts revisited. Cancer. 2004, 101: 1947-1957. 10.1002/cncr.20559.CrossRefPubMed

10.

Teboul M, Halliwell M: Atlas of Ultrasound and Ductal Echography of the Breast: The Introduction of Anatomic Intelligence into Breast Imaging. 1995, Oxford, United Kingdom: Blackwell Science

11.

Ramsay DT, Kent JC, Hartmann RA, Hartmann PE: Anatomy of the lactating human breast redefined with ultrasound imaging. J Anat. 2005, 206: 525-534. 10.1111/j.1469-7580.2005.00417.x.CrossRefPubMedPubMedCentral

12.

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. 1977, 59: 1073-1080.PubMed

13.

Dietz JR, Crowe JP, Grundfest S, Arrigain S, Kim JA: Directed duct excision by using mammary ductoscopy in patients with pathologic nipple discharge. Surgery. 2002, 132: 582-587. 10.1067/msy.2002.127672. discussion 587–588CrossRefPubMed

14.

Going JJ, Moffat DF: Escaping from Flatland: clinical and biological aspects of human mammary duct anatomy in three dimensions. J Pathol. 2004, 203: 538-544. 10.1002/path.1556.CrossRefPubMed

15.

Papanicolaou GN, Bader GM, Holmquist DG, Falk EA: Cytologic evaluation of breast secretions. Ann NY Acad Sci. 1956, 63: 1409-1421.CrossRefPubMed

16.

Petrakis NL: Physiologic, biochemical, and cytologic aspects of nipple aspirate fluid. Breast Cancer Res Treat. 1986, 8: 7-19. 10.1007/BF01805919.CrossRefPubMed

17.

Wynder EL, Lahti H, Laakso K, Cheng SL, DeBevoise S, Rose DP: Nipple aspirates of breast fluid and the epidemiology of breast disease. Cancer. 1985, 56: 1473-1478.CrossRefPubMed

18.

Petrakis NL: Nipple aspirate fluid in epidemiologic studies of breast disease. Epidemiol Rev. 1993, 15: 188-195.PubMed

19.

Chatterton RT, 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. 2005, 90: 1686-1691. 10.1210/jc.2004-1861.CrossRefPubMed

20.

Chatterton RT, Geiger AS, Gann PH, Khan SA: Formation of estrone and estradiol from estrone sulfate by normal breast parenchymal tissue. J Steroid Biochem Mol Biol. 2003, 86: 159-166. 10.1016/S0960-0760(03)00266-8.CrossRefPubMed

21.

Chatterton RT, Geiger AS, Khan SA, Helenowski IB, Jovanovic BD, Gann PH: Variation in estradiol, estradiol precursors, and estrogen-related products in nipple aspirate fluid from normal premenopausal women. Cancer Epidemiol Biomarkers Prev. 2004, 13: 928-935.PubMed

22.

Petrakis NL, Wrensch MR, Ernster VL, Miike R, Murai J, Simberg N, Siiteri PK: Influence of pregnancy and lactation on serum and breast fluid estrogen levels: implications for breast cancer risk. Int J Cancer. 1987, 40: 587-591.CrossRefPubMed

23.

Leborgne RA: The Breast in Roentgen Diagnosis. 1953, Montevideo, Uruguay: Impresora Uruguaya SA – Juncal 1511

24.

Brogi E, Robson M, Panageas KS, Casadio C, Ljung BM, Montgomery L: Ductal lavage in patients undergoing mastectomy for mammary carcinoma: a correlative study. Cancer. 2003, 98: 2170-2176. 10.1002/cncr.11758.CrossRefPubMed

25.

Khan SA, Wiley EL, Rodriguez N, Baird C, Ramakrishnan R, Nayar R, Bryk M, Bethke KB, Staradub VL, Wolfman J, et al: Ductal lavage findings in women with known breast cancer undergoing mastectomy. J Natl Cancer Inst. 2004, 96: 1510-1517.CrossRefPubMed

26.

Love SM, Barsky SH: Breast-duct endoscopy to study stages of cancerous breast disease. Lancet. 1996, 348: 997-999. 10.1016/S0140-6736(96)04145-1.CrossRefPubMed

27.

Sauter ER, Ehya H, Schlatter L, MacGibbon B: Ductoscopic cytology to detect breast cancer. Cancer J. 2004, 10: 33-41. discussion 15–36CrossRefPubMed

28.

Dooley WC, Spiegel A, Cox C, Henderson R, Richardson L, Zabora J: Ductoscopy: defining its role in the management of breast cancer. Breast J. 2004, 10: 271-272. 10.1111/j.1075-122X.2004.21595.x.CrossRefPubMed

29.

Phillips HA, Howard GC, Miller WR: Nipple aspirate fluid in relation to breast cancer. Breast. 1999, 8: 169-174. 10.1054/brst.1999.0047.CrossRefPubMed

30.

Higgins S, Matloff E, Rimm D, Dziura J, Haffty B, King B: Patterns of reduced nipple aspirate fluid production and ductal lavage cellularity in women at high risk for breast cancer. Breast Cancer Research. 2005, 7: R1017-R1022. 10.1186/bcr1335.CrossRefPubMedPubMedCentral

31.

Mitchell G, Antill Y, Murray W, Kirk J, Salisbury E, Lindeman G, Di Iulio J, Milner A, Devereaux L, Phillips K-A: Nipple aspiration and ductal lavage in women with a germline BRCA1 or BRCA2 mutation. Breast Cancer Research. 2005, 7: R1122-R1131. 10.1186/bcr1348.CrossRefPubMedPubMedCentral

32.

Sanchez LM, Vizoso F, Diez-Itza I, Lopez-Otin C: Identification of the major protein components in breast secretions from women with benign and malignant breast diseases. Cancer Res. 1992, 52: 95-100.PubMed

33.

Dooley WC, Ljung BM, Veronesi U, Cazzaniga M, Elledge RM, O'Shaughnessy JA, Kuerer HM, Hung DT, Khan SA, Phillips RF, et al: Ductal lavage for detection of cellular atypia in women at high risk for breast cancer. J Natl Cancer Inst. 2001, 93: 1624-1632.CrossRefPubMed

34.

Kurian AW, Mills MA, Jaffee M, Sigal BM, Chun NM, Kingham KE, Collins LC, Nowels KW, Plevritis SK, Garber JE, et al: Ductal lavage of fluid-yielding and non-fluid-yielding ducts in BRCA1 and BRCA2 mutation carriers and other women at high inherited breast cancer risk. Cancer Epidemiol Biomarkers Prev. 2005, 14: 1082-1089. 10.1158/1055-9965.EPI-04-0776.CrossRefPubMed

35.

Bhandare D, Nayar R, Bryk M, Hou N, Cohn R, Golewale N, Parker NP, Chatterton RT, Rademaker A, Khan SA: Endocrine biomarkers in ductal lavage samples from women at high risk for breast cancer. Cancer Epidemiol Biomarkers Prev. 2005, 14: 2620-2627. 10.1158/1055-9965.EPI-05-0302.CrossRefPubMed

36.

Maddux AJ, Ashfaq R, Naftalis E, Leitch AM, Hoover S, Euhus D: Patient and duct selection for nipple duct lavage. Am J Surg. 2004, 188: 390-394. 10.1016/j.amjsurg.2004.06.021.CrossRefPubMed

37.

Khan SA, Wolfman JA, Segal L, Benjamin S, Nayar R, Wiley EL, Bryk M, Morrow M: Ductal lavage findings in women with mammographic microcalcifications undergoing biopsy. Ann Surg Oncol. 2005, 12: 689-696. 10.1245/ASO.2005.04.037.CrossRefPubMed

38.

King EB, Chew KL, Petrakis NL, Ernster VL: Nipple aspirate cytology for the study of breast cancer precursors. J Natl Cancer Inst. 1983, 71: 1115-1121.PubMed

39.

King BL, Tsai SC, Gryga ME, D'Aquila TG, Seelig SA, Morrison LE, Jacobson KK, Legator MS, Ward DC, Rimm DL, et al: Detection of chromosomal instability in paired breast surgery and ductal lavage specimens by interphase fluorescence in situ hybridization. Clin Cancer Res. 2003, 9: 1509-1516.PubMed

40.

Krishnamurthy S, Sneige N, Thompson PA, Marcy SM, Singletary SE, Cristofanilli M, Hunt KK, Kuerer HM: Nipple aspirate fluid cytology in breast carcinoma. Cancer. 2003, 99: 97-104. 10.1002/cncr.10958.CrossRefPubMed

41.

Mendrinos S, Nolen JD, Styblo T, Carlson G, Pohl J, Lewis M, Ritchie J: Cytologic findings and protein expression profiles associated with ductal carcinoma of the breast in ductal lavage specimens using surface-enhanced laser desorption and ionization-time of flight mass spectrometry. Cancer. 2005, 105: 178-183. 10.1002/cncr.21052.CrossRefPubMed

42.

Inaji H, Yayoi E, Maeura Y, Matsuura N, Tominaga S, Koyama H, Takatsuka Y, Mori T: Carcinoembryonic antigen estimation in nipple discharge as an adjunctive tool in the diagnosis of early breast cancer. Cancer. 1987, 60: 3008-3013.CrossRefPubMed

43.

Krassenstein R, Sauter E, Dulaimi E, Battagli C, Ehya H, Klein-Szanto A, Cairns P: Detection of breast cancer in nipple aspirate fluid by CpG island hypermethylation. Clin Cancer Res. 2004, 10: 28-32. 10.1158/1078-0432.CCR-0410-3.CrossRefPubMed

44.

Dupont WD, Page DL: Risk factors for breast cancer in women with proliferative breast disease. N Engl J Med. 1985, 312: 146-151.CrossRefPubMed

45.

Dupont WD, Parl FF, Hartmann WH, Brinton LA, Winfield AC, Worrell JA, Schuyler PA, Plummer WD: Breast cancer risk associated with proliferative breast disease and atypical hyperplasia. Cancer. 1993, 71: 1258-1265.CrossRefPubMed

46.

Wrensch MR, Petrakis NL, King EB, Miike R, Mason L, Chew KL, Lee MM, Ernster VL, Hilton JF, Schweitzer R, et al: Breast cancer incidence in women with abnormal cytology in nipple aspirates of breast fluid. Am J Epidemiol. 1992, 135: 130-141.PubMed

47.

Wrensch MR, Petrakis NL, Miike R, King EB, Chew K, Neuhaus J, Lee MM, Rhys M: Breast cancer risk in women with abnormal cytology in nipple aspirates of breast fluid. J Natl Cancer Inst. 2001, 93: 1791-1798. 10.1093/jnci/93.23.1791.CrossRefPubMed

48.

Fabian CJ, Kimler BF, Zalles CM, Klemp JR, Kamel S, Zeiger S, Mayo MS: Short-term breast cancer prediction by random periareolar fine-needle aspiration cytology and the Gail risk model. J Natl Cancer Inst. 2000, 92: 1217-1227. 10.1093/jnci/92.15.1217.CrossRefPubMed

49.

Page DL, Dupont WD, Rogers LW, Rados MS: Atypical hyper-plastic lesions of the female breast. A long-term follow-up study. Cancer. 1985, 55: 2698-2708.CrossRefPubMed

50.

Fackler MJ, McVeigh M, Mehrotra J, Blum MA, Lange J, Lapides A, Garrett E, Argani P, Sukumar S: Quantitative multiplex methylation-specific PCR assay for the detection of promoter hyper-methylation in multiple genes in breast cancer. Cancer Res. 2004, 64: 4442-4452. 10.1158/0008-5472.CAN-03-3341.CrossRefPubMed

51.

Evron E, Dooley WC, Umbricht CB, Rosenthal D, Sacchi N, Gabrielson E, Soito AB, Hung DT, Ljung B, Davidson NE, et al: Detection of breast cancer cells in ductal lavage fluid by methylation-specific PCR. Lancet. 2001, 357: 1335-1336. 10.1016/S0140-6736(00)04501-3.CrossRefPubMed

52.

Isaacs C, Cavalli LR, Cohen Y, Pennanen M, Shankar LK, Freedman M, Singh B, Liu M, Gallagher A, Rone JD, et al: Detection of LOH and mitochondrial DNA alterations in ductal lavage and nipple aspirate fluids from hngh-risk patients. Breast Cancer Res Treat. 2004, 84: 99-105. 10.1023/B:BREA.0000018406.03679.2e.CrossRefPubMed

53.

Krishnamurthy S, Zhao L, Hayes K, Glassman AB, Cristofanilli M, Singletary SE, Hunt KK, Kuerer HM, Sneige N: Feasibility and utility of using chromosomal aneusomy to further define the cytologic categories in nipple aspirate fluid specimens: a preliminary study. Cancer. 2004, 102: 322-327. 10.1002/cncr.20558.CrossRefPubMed

54.

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. 2004, 10: 7500-7510. 10.1158/1078-0432.CCR-04-1002.CrossRefPubMed

55.

Kuerer HM, Goldknopf IL, Fritsche H, Krishnamurthy S, Sheta EA, Hunt KK: Identification of distinct protein expression patterns in bilateral matched pair breast ductal fluid specimens from women with unilateral invasive breast carcinoma. High-throughput biomarker discovery. Cancer. 2002, 95: 2276-2282. 10.1002/cncr.10974.CrossRefPubMed

56.

Varnum SM, Covington CC, Woodbury RL, Petritis K, Kangas LJ, Abdullah MS, Pounds JG, Smith RD, Zangar RC: Proteomic characterization of nipple aspirate fluid: identification of potential biomarkers of breast cancer. Breast Cancer Res Treat. 2003, 80: 87-97. 10.1023/A:1024479106887.CrossRefPubMed

57.

Foretova L, Garber JE, Sadowsky NL, Verselis SJ, Joseph DM, Andrade AF, Gudrais PG, Fairclough D, Li FP: Carcinoembryonic antigen in breast nipple aspirate fluid. Cancer Epidemiol Bio-markers Prev. 1998, 7: 195-198.

58.

Kuerer HM, Thompson PA, Krishnamurthy S, Fritsche HA, Marcy SM, Babiera GV, Singletary SE, Cristofanilli M, Sneige N, Hunt KK: High and differential expression of HER-2/neu extracellular domain in bilateral ductal fluids from women with unilateral invasive breast cancer. Clin Cancer Res. 2003, 9: 601-605.PubMed

59.

Liu Y, Wang JL, Chang H, Barsky SH, Nguyen M: Breast-cancer diagnosis with nipple fluid bFGF. Lancet. 2000, 356: 567-10.1016/S0140-6736(00)02587-3.CrossRefPubMed

60.

Qin W, Zhu W, Wagner-Mann C, Folk W, Sauter ER: Association of uPA, PAT-1, and uPAR in nipple aspirate fluid (NAF) with breast cancer. Cancer J. 2003, 9: 293-301.CrossRefPubMed

61.

Sauter ER, Daly M, Linahan K, Ehya H, Engstrom PF, Bonney G, Ross EA, Yu H, Diamandis E: Prostate-specific antigen levels in nipple aspirate fluid correlate with breast cancer risk. Cancer Epidemiol Biomarkers Prev. 1996, 5: 967-970.PubMed

62.

Zhao Y, Verselis SJ, Klar N, Sadowsky NL, Kaelin CM, Smith B, Foretova L, Li FP: Nipple fluid carcinoembryonic antigen and prostate-specific antigen in cancer-bearing and tumor-free breasts. J Clin Oncol. 2001, 19: 1462-1467.PubMed

63.

Kuerer HM, Coombes KR, Chen JN, Xiao L, Clarke C, Fritsche H, Krishnamurthy S, Marcy S, Hung MC, Hunt KK: Association between ductal fluid proteomic expression profiles and the presence of lymph node metastases in women with breast cancer. Surgery. 2004, 136: 1061-1069. 10.1016/j.surg.2004.04.011.CrossRefPubMed

64.

Li J, Zhao J, Yu X, Lange J, Kuerer H, Krishnamurthy S, Schilling E, Khan SA, Sukumar S, Chan DW: Identification of biomarkers for breast cancer in nipple aspiration and ductal lavage fluid. Clin Cancer Res. 2005, 11: 8312-8320. 10.1158/1078-0432.CCR-05-1538.CrossRefPubMed

65.

Paweletz CP, Trock B, Pennanen M, Tsangaris T, Magnant C, Liotta LA, Petricoin EF: Proteomic profiles of nipple aspirate fluids obtained by SELDI-TOF: Potential for new biomarkers to aid in the diagnosis of breast cancer. Disease Markers. 2001, 17: 301-307.CrossRefPubMed

66.

Pawlik TM, Fritsche H, Coombes KR, Xiao L, Krishnamurthy S, Hunt KK, Pusztai L, Chen JN, Clarke CH, Arun B, 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. 2005, 89: 149-157. 10.1007/s10549-004-1710-4.CrossRefPubMed

67.

Petricoin EE, Paweletz CP, Liotta LA: Clinical applications of proteomics: proteomic pattern diagnostics. J Mammary Gland Biol Neoplasia. 2002, 7: 433-440. 10.1023/A:1024042200521.CrossRefPubMed

68.

Sauter ER, Shan S, Hewett JE, Speckman P, Du Bois GC: Proteomic analysis of nipple aspirate fluid using SELDI-TOF-MS. Int J Cancer. 2005, 114: 791-796. 10.1002/ijc.20742.CrossRefPubMed

69.

Sauter ER, Zhu W, Fan XJ, Wassell RP, Chervoneva I, Du Bois GC: Proteomic analysis of nipple aspirate fluid to detect biologic markers of breast cancer. Br J Cancer. 2002, 86: 1440-1443. 10.1038/sj.bjc.6600285.CrossRefPubMedPubMedCentral

70.

Yamamoto D, Senzaki H, Nakagawa H, Okugawa H, Gondo H, Tanaka K: Detection of chromosomal aneusomy by fluorescence in situ hybridization for patients with nipple discharge. Cancer. 2003, 97: 690-694. 10.1002/cncr.11091.CrossRefPubMed

71.

Linder J: Editorial: ductal lavage of the breast. Diagn Cytopathol. 2004, 30: 140-142. 10.1002/dc.20002.CrossRefPubMed

72.

Hollingsworth AB, Nall S, Dill D: The evolution of breast cancer risk assessment. J Okla State Med Assoc. 2002, 95: 639-644.PubMed

73.

Miyazaki M, Tamaki Y, Sakita I, Fujiwara Y, Kadota M, Masuda N, Ooka M, Ohnishi T, Ohue M, Sekimoto M, et al: Detection of microsatellite alterations in nipple discharge accompanied by breast cancer. Breast Cancer Res Treat. 2000, 60: 35-41. 10.1023/A:1006336110322.CrossRefPubMed

Title: The intraductal approach to the breast: raison d'être
Authors: Bonnie L King
Susan M Love
Publication date: 01-04-2006
Publisher: BioMed Central
Published in: Breast Cancer Research / Issue 2/2006
Electronic ISSN: 1465-542X
DOI: https://doi.org/10.1186/bcr1410

Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Watch now

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras

Prof. Fabrice Barlesi

Developed by: Springer Medicine

At a glance: The STEP trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 2/2006

Breast asymmetry and predisposition to breast cancer

Key stages in mammary gland development - The alveolar switch: coordinating the proliferative cues and cell fate decisions that drive the formation of lobuloalveoli from ductal epithelium

Spontaneous and therapeutic abortions and the risk of breast cancer among BRCAmutation carriers

Type I insulin-like growth factor receptor over-expression induces proliferation and anti-apoptotic signaling in a three-dimensional culture model of breast epithelial cells

Key stages in mammary gland development - Involution: apoptosis and tissue remodelling that convert the mammary gland from milk factory to a quiescent organ

Is there a positive association between mammographic density and bone mineral density? Authors' response

Keynote webinar | Spotlight on antibody–drug conjugates in cancer