Skip to main content

Advertisement

Log in

Monitoring In-Vivo the Mammary Gland Microstructure during Morphogenesis from Lactation to Post-Weaning Using Diffusion Tensor MRI

  • Published:
Journal of Mammary Gland Biology and Neoplasia Aims and scope Submit manuscript

Abstract

Lactation and the return to the pre-conception state during post-weaning are regulated by hormonal induced processes that modify the microstructure of the mammary gland, leading to changes in the features of the ductal / glandular tissue, the stroma and the fat tissue. These changes create a challenge in the radiological workup of breast disorder during lactation and early post-weaning. Here we present non-invasive MRI protocols designed to record in vivo high spatial resolution, T2-weighted images and diffusion tensor images of the entire mammary gland. Advanced imaging processing tools enabled tracking the changes in the anatomical and microstructural features of the mammary gland from the time of lactation to post-weaning. Specifically, by using diffusion tensor imaging (DTI) it was possible to quantitatively distinguish between the ductal / glandular tissue distention during lactation and the post-weaning involution. The application of the T2-weighted imaging and DTI is completely safe, non-invasive and uses intrinsic contrast based on differences in transverse relaxation rates and water diffusion rates in various directions, respectively. This study provides a basis for further in-vivo monitoring of changes during the mammary developmental stages, as well as identifying changes due to malignant transformation in patients with pregnancy associated breast cancer (PABC).

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Hovey RC, Trott JF, Vonderhaar BK. Establishing a framework for the functional mammary gland: from endocrinology to morphology. J Mammary Gland Biol Neoplasia. 2002;7(1):17–38. Review

    Article  PubMed  Google Scholar 

  2. Neville MC, McFadden TB, Forsyth I. Hormonal regulation of mammary differentiation and milk secretion. J Mammary Gland Biol Neoplasia. 2002;7(1):49–66.

    Article  PubMed  Google Scholar 

  3. Kent JC. How breast feeding works. J Midwifery Women’s Heal. 2007;52:564–70.

    Article  Google Scholar 

  4. Neville MC, Allen JC, Archer PC, et al. Studies in human lactation: milk volume and nutrient composition during weaning and lactogenesis. Am J Clin Nutr. 1991;54:81–92.

    CAS  PubMed  Google Scholar 

  5. McDaniel SM, Rumer KK, Biroc SL, et al. Remodeling of the mammary microenvironment after lactation promotes breast tumor cell metastasis. Am J Pathol. 2006;168:608–20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Schedin P, O’Brien J, Rudolph M, Stein T, Borges V. Microenvironment of the involuting mammary gland mediates mammary cancer progression. J Mammary Gland Biol Neoplasia. 2007;12:71–82.

    Article  PubMed  Google Scholar 

  7. Cooper A. Anatomy of the breast. London: Longman, Orme, Green, Browne and Longmans; 1840.

    Google Scholar 

  8. Ramsay DT, Kent JC, Hartmann RA, Hartmann PE. Anatomy of the lactating human breast redefined with ultrasound imaging. J Anat. 2005;206:525–34.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Gooding MJ, Finlay J, Shipley JA, Halliwell M, Duck FA. Three-dimensional ultrasound imaging of mammary ducts in lactating women: a feasibility study. J Ultrasound Med. 2010;29:95–103.

    Article  PubMed  Google Scholar 

  10. Markiewicz E, Fan X, Mustafia D, Zamoraa M, Roman BB, Jansen SA, Macleod K, Conzen SD, and Karczmara GS, High resolution 3D MRI of mouse mammary glands with intra-ductal injection of contrast media. Magn Reson Imaging. 2015; 33(1):161–165, doi:10.1016/j.mri.2014.08.035

  11. Physics of MRI: a primer, DB Plewes, W Kucharczyk - J Magn Reson Imaging 2012; 35:1038–1054. doi:10.1002/jmri.23642

  12. Santyr GE. MR imaging of the breast. Imaging and tissue characterization without intravenous contrast. Rev Magn Reson Imaging Clin N Am. 1994;2(4):673–90.

    CAS  Google Scholar 

  13. Iima MD, Le Bihan MD. Clinical Intravoxel incoherent motion and diffusion MR imaging: past, present, and future. Radiology. 2016;278(1):13–32. doi:10.1148/radiol.2015150244. Review

    Article  PubMed  Google Scholar 

  14. Vashi R, Hooley R, Butler R, Geisel J, Philpotts L. Breast imaging of the pregnant and lactating patient: imaging modalities and pregnancy-associated breast cancer. Am J Roentgenol. 2013;200(2):321–8.

    Article  Google Scholar 

  15. Ayyappan AP, Kulkarni S, Crystal P. Pregnancy-associated breast cancer: spectrum of imaging appearances. Br J Radiol. 2010;83(990):529–34. doi:10.1259/bjr/17982822.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Turnbull LW. Dynamic contrast-enhanced MRI in the diagnosis and management of breast cancer. NMR Biomed. 2009;22(1):28–39. doi:10.1002/nbm.1273. Review

    Article  PubMed  Google Scholar 

  17. Moon M, Cornfeld D, Weinreb J. Dynamic contrast-enhanced breast MR imaging. Magn Reson Imaging Clin N Am. 2009;17(2):351–62. doi:10.1016/j.mric.2009.01.010. Review

    Article  PubMed  Google Scholar 

  18. Pinker K, Helbich TH, Morris EA. The potential of multiparametric MRI of the breast. Br J Radiol. 2017;90(1069):20160715. doi:10.1259/bjr.20160715. Review

    Article  PubMed  Google Scholar 

  19. Sundgren PC, Leander P. Is administration of gadolinium-based contrast media to pregnant women and small children justified? J Magn Reson Imaging. 2011;34(4):750–7. Review

    Article  PubMed  Google Scholar 

  20. Kanal E, Barkovich AJ, Bell C, et al. ACR guidance document on MR safe practices. J Magn Reson Imaging. 2013;37(3):501–30.

    Article  PubMed  Google Scholar 

  21. Boivin G, de Korvin B, Marion J, Duvauferrier R. Is a breast MRI possible and indicated in case of suspicion of breast cancer during lactation? Diagn Interv Imaging. 2012;93(11):823–7. doi:10.1016/j.diii.2012.05.013.

    Article  CAS  PubMed  Google Scholar 

  22. Talele AC, Slanetz PJ, Edmister WB, Yeh ED, Kopans DB. The lactating breast: MRI findings and literature review. The lactating breast: MRI findings and literature review. Breast J. 2003;9(3):237–40.

    Article  PubMed  Google Scholar 

  23. Espinosa LA, Daniel BL, Vidarsson L, Zakhour M, Ikeda DM, Herfkens RJ. The lactating breast: contrast-enhanced MR imaging of normal tissue and cancer. Radiology. 2005;237(2):429–36.

    Article  PubMed  Google Scholar 

  24. Spick C, Pinker-Domenig K, Rudas M, Helbich TH. Baltzer PA.MRI-only lesions: application of diffusion weighted imaging obviates unnecessary MR-guided breast biopsies. Eur Radiol. 2014;24(6):1204–10. doi:10.1007/s00330-014-3153-6.

    Article  PubMed  Google Scholar 

  25. Partridge SC, McDonald ES. Diffusion weighted magnetic resonance imaging of the breast: protocol optimization, interpretation, and clinical applications. Magn Reson Imaging Clin N Am. 2013;21(3):601–24. doi:10.1016/j.mric.2013.04.007. and references cited therein)

    Article  PubMed  PubMed Central  Google Scholar 

  26. Sah RG, Agarwal K, Sharma U, Parshad R, Seenu V, Jagannathan NR. Characterization of malignant breast tissue of breast cancer patients and the normal breast tissue of healthy lactating women volunteers using diffusion MRI and in vivo 1H MR spectroscopy. J Magn Reson Imaging. 2015;41:169–74.

    Article  PubMed  Google Scholar 

  27. Paran Y, Bendel P, Margalit R, Degani H. Water diffusion in the different microenvironments of breast cancer. NMR Biomed. 2004;17:170–80.

    Article  PubMed  Google Scholar 

  28. Jiang R, Ma Z, Dong H, Sun S, Zeng X, Li X. Diffusion tensor imaging of breast lesions: evaluation of apparent diffusion coefficient and fractional anisotropy and tissue cellularity. Br J Radiol. 2016;89(1064):20160076. doi:10.1259/bjr.20160076.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Le Bihan D, Mangin JF, Poupon C, et al. Diffusion tensor imaging: concepts and applications. J Magn Reson Imaging. 2001;13:534–46.

    Article  PubMed  Google Scholar 

  30. Westin CF, Maier SE, Mamata H, Nabavi A, Jolesz FA, Kikinis R. Processing and visualization for diffusion tensor MRI. Med Image Anal. 2002;6:93–108.

    Article  PubMed  Google Scholar 

  31. Furman-Haran E, Grobgeld D, Nissan N, Shapiro-Feinberg M, Degani H. Can diffusion tensor anisotropy indices assist in breast cancer detection? J Magn Reson Imaging. 2016;44(6):1624–32. doi:10.1002/jmri.25292.

    Article  PubMed  Google Scholar 

  32. Eyal E, Shapiro-Feinberg M, Furman-Haran E, et al. Parametric diffusion tensor imaging of the breast. Investig Radiol. 2012;47:284–91.

    Article  Google Scholar 

  33. Partridge SC, Ziadloo A, Murthy R, et al. Diffusion tensor MRI: preliminary anisotropy measures and mapping of breast tumors. J Magn Reson Imaging. 2010;31:339–47.

    Article  PubMed  Google Scholar 

  34. PAT B, Schäfer A, Dietzel M, et al. Diffusion tensor magnetic resonance imaging of the breast: a pilot study. Eur Radiol. 2011;21:1–10.

    Article  Google Scholar 

  35. Cakir O, Arslan A, Inan N, et al. Comparison of the diagnostic performances of diffusion parameters in diffusion weighted imaging and diffusion tensor imaging of breast lesions. Eur J Radiol. 2013;82:e801–6.

    Article  PubMed  Google Scholar 

  36. Onaygil C, Kaya H, Ugurlu MU. Aribal E diagnostic performance of diffusion tensor imaging parameters in breast cancer and correlation with the prognostic factors. J Magn Reson Imaging. 2017;45(3):660–72. doi:10.1002/jmri.25481.

    Article  PubMed  Google Scholar 

  37. Nissan N, Furman-Haran E, Shapiro-Feinberg M, Grobgeld D, Degani H. Diffusion-tensor MR imaging of the breast: hormonal regulation. Radiology. 2014;271:672–80.

    Article  PubMed  Google Scholar 

  38. Just N. Improving tumour heterogeneity MRI. Br J Cancer. 2014;111:2205–13. doi:10.1038/bjc.2014.512.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Geddes DT. Inside the lactating breast: the latest anatomy research. J Midwifery Womens Health. 2007;52:556–63.

    Article  PubMed  Google Scholar 

  40. Mortazavi SN, Hassiotou F, Geddes D, Hassanipour F. Mathematical modeling of mammary ducts in lactating human females. J Biomech Eng. 2015;137(7):071009 Paper No: BIO-14-1167. doi:10.1115/1.4028967.

  41. Panaritis V, Despotidis P, Kyriakidis A. Diameter of mammary terminal ducts as an additional tool in evaluation of women with polycystic ovarium disease. Arch Gynecol Obstet. 2004;270:252–4. doi:10.1007/s00404-003-0555-0.

    Article  CAS  PubMed  Google Scholar 

  42. Mayr NA, Staples JJ, Robinson RA, Vanmetre JE, Hussey DH. Morphometric studies in intraductal breast carcinoma using computerized image analysis. Cancer. 1991;67(11):2805–12.

    Article  CAS  PubMed  Google Scholar 

  43. Reisert M, Weigel M, Eyal E, Grobgeld D, Degani H, Hennig J. Diffusion tensor based reconstruction of the ductal tree. In: Proc Intl Soc Mag Reson Med. 2011;19:1011.

    Google Scholar 

  44. Dewey KG, Finley DA, Lönnerdal B. Breast milk volume and composition during late lactation (7-20 months). J Pediatr Gastroenterol Nutr. 1984;3:713–20.

    Article  CAS  PubMed  Google Scholar 

  45. Shapiro-Feinberg M, Weisenberg N, Zehavi T, et al. Clinical results of DTI. Eur J Radiol. 2012;81:S151–2.

    Article  PubMed  Google Scholar 

  46. Middleton LP, Amin M, Gwyn K, Theriault R, Sahin A. Breast carcinoma in pregnant women: assessment of clinicopathologic and immunohistochemical features. Cancer. 2003;98(5):1055–60.

    Article  PubMed  Google Scholar 

  47. Kakoulidis I, Skagias L, Politi E. Pregnancy associated breast cancer (PABC): aspects in diagnosis. Breast Dis. 2015;35:157–66. Review

    Article  CAS  PubMed  Google Scholar 

  48. Nissan N, Furman-Haran E, Feinberg-Shapiro M, et al. Tracking the mammary architectural features and detecting breast cancer with magnetic resonance diffusion tensor imaging. J Vis Exp. 2014:e52048. doi:10.3791/52048.

Download references

Acknowledgements

The professional work of the MR imaging technicians, Fanny Attar and Nachum Stern, is gratefully acknowledged. H. Degani holds the Fred and Andrea Fallek Chair for Breast Cancer Research. E. Furman-Haran holds the Calin and Elaine Rovinescu Research Fellow Chair for Brain Research.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hadassa Degani.

Ethics declarations

Conflict of Interest

No conflict of interest declared.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nissan, N., Furman-Haran, E., Shapiro-Feinberg, M. et al. Monitoring In-Vivo the Mammary Gland Microstructure during Morphogenesis from Lactation to Post-Weaning Using Diffusion Tensor MRI. J Mammary Gland Biol Neoplasia 22, 193–202 (2017). https://doi.org/10.1007/s10911-017-9383-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10911-017-9383-x

Keywords

Navigation