Breast Cancer

, Volume 25, Issue 4, pp 456–463 | Cite as

Preoperative breast MRI: reproducibility and significance of findings relevant to nipple–areolar complex involvement

  • Youichi Machida
  • Akiko Shimauchi
  • Takao Igarashi
  • Kazuei Hoshi
  • Eisuke Fukuma
Original Article



Eligibility of nipple-sparing mastectomy has been expanded. The purpose of this study was to evaluate interobserver agreement regarding magnetic resonance imaging (MRI) descriptors important in determining eligibility for mastectomy, and to investigate the significance of enhancement extending to the areola concerning nipple–areolar complex (NAC) involvement.


Fifty-one cases with histologically confirmed NAC involvement and 54 cases with negative NAC were enrolled. Two radiologists assessed the following factors: lesion morphology (mass or non-mass enhancement); intra-nipple bright signal; enhancement extending to the areola; abnormal nipple enhancement; and tumor–nipple distance. Factors that showed a significant association with outcome in the univariate analysis were assessed by means of multivariate analysis using a logistic regression model. Interobserver agreement between observers was assessed by calculating κ values (dichotomous variables), or intraclass correlation coefficients (ICCs; continuous variables).


In multivariate analysis of the results from the two observers, tumor–nipple distance (observer 1: odds ratio [OR] 0.93; 95% confidence interval [CI] 0.88–0.99; observer 2: OR 0.89; 95% CI 0.83–0.95) and enhancement extending to the areola (observer 1: OR 17.9; 95% CI 1.97–162.2; observer 2: OR 24.0; 95% CI 2.62–219.7) were found to be significant predictors of NAC involvement. A substantial agreement (κ = 0.64–0.71) for every dichotomous variable and an almost perfect agreement (ICC = 0.86) for continuous variable were observed.


Findings of breast MRI for NAC preservation had good interobserver agreement. Enhancement extending to the areola, together with tumor–nipple distance, was significant factors for NAC involvement.


Breast cancer Magnetic resonance imaging Nipple–areolar complex Nipple-sparing mastectomy Interobserver agreement 



This study was presented at the 24th Annual Meeting of the Japanese Breast Cancer Society, Fukuoka, July 13–15, 2017 (Presentation No. OS-1-01-04).

Compliance with ethical standards

Conflict of interest

All authors declare that they have no conflict of interest.

Supplementary material

12282_2018_845_MOESM1_ESM.tif (84 mb)
Supplementary material 1 (TIFF 86029 kb) Supplemental Fig. 1 The enrollment criteria. Primary systemic therapy was not performed, and no locoregional recurrence or metastasis was detected for ≥ 2 years after surgical treatment, in eligible cases. Bt, total mastectomy; NAC, nipple–areolar complex; NSM, nipple-sparing mastectomy; SSM, skin-sparing mastectomy
12282_2018_845_MOESM2_ESM.tif (84.9 mb)
Supplementary material 2 (TIFF 86943 kb) Supplemental Fig. 2 Receiver operating characteristic (ROC) curves of tumor–nipple distance, for the prediction of nipple–areolar complex involvement
12282_2018_845_MOESM3_ESM.tif (2.5 mb)
Supplementary material 3 (TIFF 2588 kb) Supplemental Fig. 3: Receiver operating characteristic (ROC) curves of tumor–nipple distance of 5 mm and enhancement attached to the areolar, for the prediction of nipple–areolar complex involvement


  1. 1.
    Sakamoto N, Fukuma E, Teraoka K, Hoshi K. Local recurrence following treatment for breast cancer with an endoscopic nipple-sparing mastectomy. Breast Cancer. 2016;23:552–60.CrossRefPubMedGoogle Scholar
  2. 2.
    Frey JD, Alperovich M, Kim JC, Axelrod DM, Shapiro RL, Choi M, et al. Oncologic outcomes after nipple-sparing mastectomy: a single-institution experience. J Surg Oncol. 2016;113:8–11.CrossRefPubMedGoogle Scholar
  3. 3.
    Moo TA, Pinchinat T, Mays S, Landers A, Christos P, Alabdulkareem H, et al. Oncologic Outcomes After Nipple-Sparing Mastectomy. Ann Surg Oncol. 2016;23:3221–5.CrossRefPubMedGoogle Scholar
  4. 4.
    Poruk KE, Ying J, Chidester JR, Olson JR, Matsen CB, Neumayer L, et al. Breast cancer recurrence after nipple-sparing mastectomy: one institution’s experience. Am J Surg. 2015;209:212–7.CrossRefPubMedGoogle Scholar
  5. 5.
    El Hage Chehade H, Headon H, Wazir U, Carmaichael AR, Choy C, Kasem A, et al. Nipple-sparing mastectomy using a hemi-periareolar incision with or without minimal medial-lateral extensions; clinical outcome and patient satisfaction: a single centre prospective observational study. Am J Surg. 2017;213:1116–24.CrossRefPubMedGoogle Scholar
  6. 6.
    Wei CH, Scott AM, Price AN, Miller HC, Klassen AF, Jhanwar SM, et al. Psychosocial and sexual well-being following nipple-sparing mastectomy and reconstruction. Breast J. 2016;22:10–7.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Burdge EC, Yuen J, Hardee M, Gadgil PV, Das C, Henry-Tillman R, et al. Nipple skin-sparing mastectomy is feasible for advanced disease. Ann Surg Oncol. 2013;20:3294–302.CrossRefPubMedGoogle Scholar
  8. 8.
    Santoro S, Loreti A, Cavaliere F, Costarelli L, La Pinta M, Manna E, et al. Neoadjuvant chemotherapy is not a contraindication for nipple sparing mastectomy. Breast. 2015;24:661–6.CrossRefPubMedGoogle Scholar
  9. 9.
    Piato JR, de Andrade RD, Chala LF, de Barros N, Mano MS, Melitto AS, et al. MRI to predict nipple involvement in breast cancer patients. AJR Am J Roentgenol. 2016;206:1124–30.CrossRefPubMedGoogle Scholar
  10. 10.
    Cho J, Chung J, Cha ES, Lee JE, Kim JH. Can preoperative 3-T MRI predict nipple-areolar complex involvement in patients with breast cancer? Clin Imaging. 2016;40:119–24.CrossRefPubMedGoogle Scholar
  11. 11.
    Moon JY, Chang YW, Lee EH, Seo DY. Malignant invasion of the nipple-areolar complex of the breast: usefulness of breast MRI. AJR Am J Roentgenol. 2013;201:448–55.CrossRefPubMedGoogle Scholar
  12. 12.
    Karamchandani DM, Chetlen AL, Riley MP, Schetter S, Hollenbeak CS, Mack J. Pathologic-radiologic correlation in evaluation of retroareolar margin in nipple-sparing mastectomy. Virchows Arch. 2015;466:279–87.CrossRefPubMedGoogle Scholar
  13. 13.
    D’Alonzo M, Martincich L, Biglia N, Pisacane A, Maggiorotto F, Rosa GD, et al. Clinical and radiological predictors of nipple-areola complex involvement in breast cancer patients. Eur J Cancer. 2012;48:2311–8.CrossRefPubMedGoogle Scholar
  14. 14.
    Ponzone R, Maggiorotto F, Carabalona S, Rivolin A, Pisacane A, Kubatzki F, et al. MRI and intraoperative pathology to predict nipple-areola complex (NAC) involvement in patients undergoing NAC-sparing mastectomy. Eur J Cancer. 2015;51:1882–9.CrossRefPubMedGoogle Scholar
  15. 15.
    Cense HA, Rutgers EJ, Lopes Cardozo M, Van Lanschot JJ. Nipple-sparing mastectomy in breast cancer: a viable option? Eur J Surg Oncol. 2001;27:521–6.CrossRefPubMedGoogle Scholar
  16. 16.
    El Khoury M, Lalonde L, David J, Labelle M, Mesurolle B, Trop I. Breast imaging reporting and data system (BI-RADS) lexicon for breast MRI: interobserver variability in the description and assignment of BI-RADS category. Eur J Radiol. 2015;84:71–6.CrossRefPubMedGoogle Scholar
  17. 17.
    Grimm LJ, Anderson AL, Baker JA, Johnson KS, Walsh R, Yoon SC, et al. Interobserver variability between breast imagers using the fifth edition of the BI-RADS MRI Lexicon. Am J Roentgenol. 2015;204:1120–4.CrossRefGoogle Scholar
  18. 18.
    Kinkel K, Helbich TH, Esserman LJ, Barclay J, Schwerin EH, Sickles EA, et al. Dynamic high-spatial-resolution MR imaging of suspicious breast lesions: diagnostic criteria and interobserver variability. Am J Roentgenol. 2000;175:35–43.CrossRefGoogle Scholar
  19. 19.
    Machida Y, Tozaki M, Shimauchi A, Yoshida T. Two distinct types of linear distribution in nonmass enhancement at breast mr imaging: difference in positive predictive value between linear and branching patterns. Radiology. 2015;276:686–94.CrossRefPubMedGoogle Scholar
  20. 20.
    Steen ST, Chung AP, Han SH, Vinstein AL, Yoon JL, Giuliano AE. Predicting nipple-areolar involvement using preoperative breast MRI and primary tumor characteristics. Ann Surg Oncol. 2013;20:633–9.CrossRefPubMedGoogle Scholar
  21. 21.
    Byon W, Kim E, Kwon J, Park YL, Park C. Magnetic resonance imaging and clinicopathological factors for the detection of occult nipple involvement in breast cancer patients. J Breast Cancer. 2014;17:386–92.CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    D’Orsi CJ. ACR BI-RADS atlas: breast imaging reporting and data system: mammography, ultrasound, magnetic resonance imaging, follow-up and outcome monitoring, data dictionary. 5th edn. Am Coll Radiol. 2013.Google Scholar
  23. 23.
    Ryu JM, Nam SJ, Kim SW, Lee SK, Bae SY, Yi HW, et al. Feasibility of nipple-sparing mastectomy with immediate breast reconstruction in breast cancer patients with tumor-nipple distance less than 2.0 cm. World J Surg. 2016;40:2028–35.CrossRefPubMedGoogle Scholar
  24. 24.
    Cho JW, Yoon ES, You HJ, Kim HS, Lee BI, Park SH. Nipple-areola complex necrosis after nipple-sparing mastectomy with immediate autologous breast reconstruction. Arch Plast Surg. 2015;42:601–7.CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Komorowski AL, Zanini V, Regolo L, Carolei A, Wysocki WM, Costa A. Necrotic complications after nipple- and areola-sparing mastectomy. World J Surg. 2006;30:1410–3.CrossRefPubMedGoogle Scholar

Copyright information

© The Japanese Breast Cancer Society 2018

Authors and Affiliations

  • Youichi Machida
    • 1
    • 2
  • Akiko Shimauchi
    • 1
  • Takao Igarashi
    • 3
  • Kazuei Hoshi
    • 4
  • Eisuke Fukuma
    • 2
  1. 1.RadiologyKameda Kyobashi ClinicTokyoJapan
  2. 2.Breast Center, Kameda Medical CenterKamogawaJapan
  3. 3.Department of Diagnostic ImagingJikei University School of Medicine HospitalTokyoJapan
  4. 4.Anatomic PathologyKameda Medical CenterKamogawaJapan

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