Abstract
Purpose
Our previous study suggests that the cross-sectional morphology of ducts and branching of ducts in the nipple are associated with the presence of breast cancer. In this study, we evaluated whether cross-sectional morphology and duct branching of human nipple obtained by X-ray dark-field imaging tomographic technique (XDFI-CT) could predict the likelihood of the presence of intraductal cancer into the nipple.
Methods
A total of 51 nipple specimens were obtained from consecutive total mastectomies performed for breast cancer in Nagoya Medical Center. After reconstructing 3D images of the nipple using XDFI-CT, the cross-sectional images and the 3D arrangement of ducts were extracted. These cross-sectional images of ducts were classified into four patterns based on the status of the lumen without being informed of pathology results.
Results
Of the four patterns, the distended ducts with heterogenous content were highly correlated with the presence of ductal carcinoma in situ confirmed by histopathology. The total number of orifices identified in the 51 specimens was 1298, and 182 (14%) at the tip and 19 (1.5%) at least 5 mm depth from the tip were composed of two or more ducts.
Conclusions
Anatomy of nipple ducts is essential to evaluate risk of local recurrence after nipple-sparing mastectomy because cancerous spread occurs within the duct of the same segment of the mammary duct-lobular system in the in situ stage. The 3D microscale anatomy of nipple ducts revealed by XDFI-CT provides useful information to assess the risk of breast cancer involvement at the preserved portion in nipple-sparing mastectomy.
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Availability of data and materials
The datasets generated and analyzed during the current study are available from the corresponding author on reasonable request.
Code availability
Not applicable.
References
Young WA, Degnim AC, Hoskin TL, Jakub JW, Nguyen M, Tran NV, Harless CA, Manrique OJ, Boughey JC, Hieken TJ (2019) Outcomes of >1300 nipple-sparing mastectomies with immediate reconstruction: The impact of expanding indications on complications. Ann Surg Oncol 26(10):3115–3123
Lee CH, Cheng MH, Wu CW, Kuo WL, Yu CC, Huang JJ (2019) Nipple-sparing mastectomy and immediate breast reconstruction after recurrence from previous breast conservation therapy. Ann Plast Surg 82(1S):S95-102
Going JJ, Moffat DF (2004) Escaping from Flatland: clinical and biological aspects of human mammary duct anatomy in three dimensions. J Pathol 203(1):538–544
Taneri F, Kurukahvecioglu O, Akyurek N, Tekin EH, İlhan MN, Cifter C, Bozkurt S, Dursun A, Bayram O, Onuk E (2006) Microanatomy of milk ducts in the nipple. Eur Surg Res 38(6):545–549
Rusby JE, Brachtel EF, Michaelson JS, Koerner FC, Smith BL (2007) Breast duct anatomy in the human nipple: three-dimensional patterns and clinical implications. Breast Cancer Res Treat 106(2):171–179
Norton KA, Namazi S, Barnard N, Fujibayashi M, Bhanot G, Ganesan S, Iyatomi H, Ogawa K, Shinbrot T (2012) Automated reconstruction algorithm for identification of 3D architectures of cribriform ductal carcinoma in situ. PLoS ONE 7:e44011
Booth ME, Treanor D, Roberts N, Magee DR, Speirs V, Hanby AM (2015) Three-dimensional reconstruction of ductal carcinoma in situ with virtual slides. Histopathology 66:966–973
Ando M, Maksimenko A, Sugiyama H, Pattanasiriwisawa W, Hyodo K, Uyama C (2002) Simple X-ray dark-and bright-field imaging using achromatic Laue optics. Jpn J Appl Phys 41(9A):L1016–L1018
Sunaguchi N, Yuasa T, Huo Q, Ichihara S, Ando M (2010) X-ray refraction contrast computed tomography images using dark-feild imaging optics. Appl Phys Lett 97(15):153701–153703
Sunaguchi N, Shimao D, Yuasa T, Ichihara S, Nishimura R, Oshima R, Watanabe A, Niwa K, Ando M (2020) Three-dimensional microanatomy of human nipple visualized by X-ray dark-field computed tomography. Breast Cancer Res Treat 180(2):397–405
Tot T (2005) DCIS, cytokeratins, and the theory of the sick lobe. Virchows Arch 447(1):1–8
Tot T (2007) The theory of the sick breast lobe and the possible consequences. Int J Surg Pathol 15(4):369–375
Tan MP, Tot T (2018) The sick lobe hypothesis, field cancerisation and the new era of precision breast surgery. Gland Surg 7(6):611–618
Snigirev A, Snigireva I, Kohn V, Kuznetsov S, Schelokov I (1995) On the possibilities of X-ray phase contrast microimaging by coherent high-energy synchrotron radiation. Rev Sci Instrum 66(12):5486–5492
Momose A, Takeda T, Itai Y, Yoneyama A, Hirano K (1998) Phase-contrast tomographic imaging using an X-ray interferometer. J Synchrotron Radiat 5(3):309–314
Chapman D, Thomlinson W, Johnston RE, Washburn D, Pisano E, Gmür N, Zhong Z, Menk R, Arfelli F, Sayers D (1997) Diffraction enhanced x-ray imaging. Phys Med Biol 42(11):2015–2025
Momose A, Kawamoto S, Koyama I, Hamaishi Y, Takai K, Suzuki Y (2003) Demonstration of X-ray Talbot interferometry. Jpn J Appl Phys 42(7B):L866–L868
Ando M, Gupta R, Iwakoshi A, Kim J, Shimao D, Sugiyama H, Sunaguchi N, Yuasa T, Ichihara S (2020) X-ray dark-field phase-contrast imaging: origins of the concept to practical implementation and applications. Phys Med 79:188–208
Sunaguchi N, Yuasa T, Gupta R, Ando M (2015) An efficient reconstruction algorithm for differential phase-contrast tomographic images from a limited number of views. Appl Phys Lett 107(25):253701–253704
Tabár L, Tot T, Dean PB (2005) Breast cancer—the art and science of early detection with mammography. Thieme publisher, ISBN: 9783131353719
Goodfellow IJ, Pouget-Abadie J, Mirza M, Xu B, Warde-Farley D, Ozair S, Courville A, Bengio Y (2014) Generative adversarial networks. arXiv preprint arXiv:1406.2661
Acknowledgements
The experiments were performed as part of five research projects (2008S2002, 2012G562, 2015G597, 2016G0625, 2019G598, and 2020G583) funded by KEK. This research was partially supported by a Grant-in-Aid for Scientific Research (Grant Numbers 16K01369, 15H01129, 26286079, 18K13765, and 21K04077) from the Japanese Ministry of Education, Culture, Sports, Science and Technology and “Knowledge Hub Aichi,” a Priority Research Project from Aichi Prefectural Government.
Funding
This research was partially supported by a Grant-in-Aid for Scientific Research (Grant Numbers 16K01369, 15H01129, 26286079, and 18K13765) from the Japanese Ministry of Education, Culture, Sports, Science and Technology and “Knowledge Hub Aichi,” Priority Research Project from Aichi Prefectural Government.
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Sunaguchi, N., Shimao, D., Nishimura, R. et al. Usefulness of X-ray dark-field imaging in the evaluation of local recurrence after nipple-sparing mastectomy. Int J CARS 16, 1915–1923 (2021). https://doi.org/10.1007/s11548-021-02472-4
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DOI: https://doi.org/10.1007/s11548-021-02472-4