Annals of Surgical Oncology

, Volume 26, Issue 13, pp 4302–4309 | Cite as

A Nomogram to Predict Factors Associated with Lymph Node Metastasis in Ductal Carcinoma In Situ with Microinvasion

  • Jessica C. Gooch
  • Freya Schnabel
  • Jennifer Chun
  • Elizabeth Pirraglia
  • Andrea B. Troxel
  • Amber Guth
  • Richard Shapiro
  • Deborah Axelrod
  • Daniel RosesEmail author
Breast Oncology



Ductal carcinoma in situ (DCIS) with foci of invasion measuring ≤ 1 mm (DCISM), represents < 1% of all invasive breast cancers. Sentinel lymph node biopsy (SLNB) has been a standard component of surgery for patients with invasive carcinoma or extensive DCIS. We hypothesize that selective performance of SLNB may be appropriate given the low incidence of sentinel node (SN) metastasis for DCISM. We investigated the clinicopathologic predictors for SN positivity in DCISM, to identify which patients might benefit from SLNB.


A retrospective review of the National Cancer Database was performed for cases from 2012 to 2015. Clinical and tumor characteristics, including SN results, were evaluated, and Pearson’s Chi square tests and logistic regression were performed.


Of 7803 patients with DCISM, 306 (4%) had at least one positive SN. Patients with positive SNs were younger, more often of Black race, had higher-grade histology and larger tumor size, and were more likely to have lymphovascular invasion (LVI; all p < 0.001). In an adjusted model, the presence of LVI was associated with the highest odds ratio (OR) for node positivity (OR 8.80, 95% confidence interval 4.56–16.96).


Among women with DCISM, only 4% had a positive SN. Node positivity was associated with more extensive and higher-grade DCIS, and the presence of LVI was strongly correlated with node positivity. Our data suggest that LVI is the most important factor in determining which patients with DCISM will benefit from SN biopsy.



Jessica C. Gooch, Freya Schnabel, Jennifer Chun, Elizabeth Pirraglia, Andrea B. Troxel, Amber Guth, Richard Shapiro, Deborah Axelrod, and Daniel Roses have no disclosures to report.


  1. 1.
    Ozkan-Gurdal S, Cabioglu N, Ozcinar B, Muslumanoglu M, et al. Factors predicting microinvasion in ductal carcinoma in situ. Asian Pac J Cancer Prev. 2014;15(1):55–60.CrossRefGoogle Scholar
  2. 2.
    Siegel RL, Miller KD, Jemal A. Cancer statistics, 2017. CA Cancer J Clin. 2017;67(1):7–30.CrossRefGoogle Scholar
  3. 3.
    Doria MT, Maesaka JY, Soares de Azevedo Neto R, de Barros N, et al. Development of a model to predict invasiveness in ductal carcinoma in situ diagnosed by percutaneous biopsy-original study and critical evaluation of the literature. Clin Breast Cancer. 2018;18(5):e805–12.Google Scholar
  4. 4.
    Levinsohn E, Altman M, Chagpar AB. Controversies regarding the diagnosis and management of ductal carcinoma in situ. The Am Surg. 2018;84(1):1–6.PubMedGoogle Scholar
  5. 5.
    Pu T, Zhong X, Deng L, Li S, et al. Long term prognosis of ductal carcinoma in situ with microinvasion: a retrospective cohort study. Int J Clin Exp Pathol. 2018;11(5):2665–74.Google Scholar
  6. 6.
    Jakub JW, Murphy BL, Gonzalez AB, Conners AL, et al. A validated nomogram to predict upstaging of ductal carcinoma in situ to invasive disease. Ann Surg Oncol. 2017;24(10):2915–24.CrossRefGoogle Scholar
  7. 7.
    Fang Y, Wu J, Wang W, Fei X, et al. Biologic Behavior and long-term outcomes of breast ductal carcinoma in situ with microinvasion. Oncotarget. 2016;7(39):64182–90.CrossRefGoogle Scholar
  8. 8.
    Maffuz A, Barroso-Bravo S, Najera I, Zarco G, et al. Tumor size as a predictor of microinvasion, invasion and axillary metastasis in ductal carcinoma in situ. J Exp Clin Cancer Res. 2006;25(2):223–7.PubMedGoogle Scholar
  9. 9.
    Shatat L, Gloyeske N, Madan R, O’Neil M, et al. Microinvasive breast carcinoma carries an excellent prognosis regardless of the tumor characteristics. Hum Pathol. 2013;44(12):2684–9.CrossRefGoogle Scholar
  10. 10.
    Sue GR, Lannin DR, Killelea B, Chagpar AB. Predictors of microinvasion and its prognostic role in ductal carcinoma in situ. Am J Surg. 2013;206(4):478–81.CrossRefGoogle Scholar
  11. 11.
    Hanna MG, Jaffer S, Bleiweiss IJ, Nayak A. Re-evaluating the role of sentinel lymph node biopsy in microinvasive breast carcinoma. Mod Pathol. 2014;27(11):1489–98.CrossRefGoogle Scholar
  12. 12.
    Vieira CC, Mercado CL, Cangiarella JF, Moy L, et al. Microinvasive ductal carcinoma in situ: clinical presentation, imaging features, pathologic findings, and outcome. Eur J Radiol. 2010;73(1):102–7.CrossRefGoogle Scholar
  13. 13.
    Kim M, Kim HJ, Chung YR, Kang E, et al. Microinvasive carcinoma versus ductal carcinoma in situ: a comparison of clinicopathological features and clinical outcomes. J Breast Cancer. 2018;21(2):197–205.CrossRefGoogle Scholar
  14. 14.
    Lyons JM 3rd, Stempel M, Van Zee KJ, Cody HS 3rd. Axillary node staging for microinvasive breast cancer: is it justified? Ann Surg Oncol. 2012;19(11):3416–21.CrossRefGoogle Scholar
  15. 15.
    Magnoni F, Massari G, Santomauro G, Bagnardi V, et al. Sentinel lymph node biopsy in microinvasive ductal carcinoma in situ. Br J Surg. 2019;106(4):375–383.CrossRefGoogle Scholar
  16. 16.
    Adamovich TL, Simmons RM. Ductal carcinoma in situ with microinvasion. Am J Surg 2003;186(2):112–6.CrossRefGoogle Scholar
  17. 17.
    Lagios MD, Westdahl PR, Margolin FR, Rose MR. Duct carcinoma in situ: relationship of extent of noninvasive disease to the frequency of occult invasion, multicentricity, lymph node metastases and short-term treatment failures. Cancer. 1982;50:1309–14.CrossRefGoogle Scholar
  18. 18.
    Murphy BL, Gonzalez AB, Keeney MG, Chen B, et al. Ability of intraoperative pathologic analysis of ductal carcinoma in situ to guide selective use of sentinel lymph node surgery. Am Surg. 2018;84(4):537–542.PubMedGoogle Scholar
  19. 19.
    Gumus H, Mills P, Fish D, Gumus M, et al. Predictive factors for invasive cancer in surgical specimens following an initial diagnosis of ductal carcinoma in situ after stereotactic vacuum-assisted breast biopsy in microcalcification-only lesions. Diagn Interv Radiol. 2016;22(1):29–34.CrossRefGoogle Scholar
  20. 20.
    Goyal A, Douglas-Jones A, Monypenny I, Sweetland H, et al. Is there a role of sentinel lymph node biopsy in ductal carcinoma in situ? Analysis of 587 cases. Breast Cancer Res Treat. 2006;98(3):311–4.CrossRefGoogle Scholar
  21. 21.
    Yen TW, Hunt KK, Ross MI, Mirza NQ, et al. Predictors of invasive breast cancer in patients with an initial diagnosis of ductal carcinoma in situ: a guide to selective use of sentinel lymph node biopsy in management of ductal carcinoma in situ. J Am Coll Surg. 2005;200(4):516–26.CrossRefGoogle Scholar
  22. 22.
    Lyman. GH, Giuliano AE, Somerfield MR, Benson AB 3rd, et al. American Society of Clinical Oncology guideline recommendations for sentinel lymph node biopsy in early-stage breast cancer. J Clin Oncol. 2005;23(30):7703–20.CrossRefGoogle Scholar
  23. 23.
    Lyman GH, Somerfield MR, Bosserman LD, Perkins CL, et al. Sentinel lymph node biopsy for patients with early-stage breast cancer: American Society of Clinical oncology clinical practice guideline update. J Clin Oncol. 2017;35(5):561–4.CrossRefGoogle Scholar
  24. 24.
    Miller ME, Kyrillos A, Yao K, Kantor O, et al. Utilization of axillary surgery for patients with ductal carcinoma in situ: a report from the national cancer data base. Ann Surg Oncol. 2016;23(10):3337–46.CrossRefGoogle Scholar
  25. 25.
    Fortunato L, Santoni M, Drago S, Gucciardo G, et al. Sentinel lymph node biopsy in women with pT1a or “microinvasive” breast cancer. Breast. 2008;17(4):395–400.CrossRefGoogle Scholar
  26. 26.
    Zahoor S, Haji A, Battoo A, Qurieshi M, et al. Sentinel lymph node biopsy in breast cancer: a clinical review and update. J Breast Cancer. 2017;20(3):217–227.CrossRefGoogle Scholar
  27. 27.
    Lagios MD, Silverstein MJ. Sentinel node biopsy for patients with DCIS: a dangerous and unwarranted direction. Ann Surg Oncol. 2001;8(4):275–7.CrossRefGoogle Scholar
  28. 28.
    Yu KD, Wu LM, Liu GY, Wu J, et al. Different distribution of breast cancer subtypes in breast ductal carcinoma in situ (DCIS), DCIS with microinvasion, and DCIS with invasion component. Ann Surg Oncol. 2011;18(5):1342–8.CrossRefGoogle Scholar
  29. 29.
    Murphy CD, Jones JL, Javid SH, Michaelson JS, et al. Do sentinel node micrometastases predict recurrence risk in ductal carcinoma in situ and ductal carcinoma in situ with microinvasion? Am J Surg. 2008;196(4):566–8.CrossRefGoogle Scholar
  30. 30.
    Lillemoe TJ, Tsai ML, Swenson KK, Susnik B, et al. Clinicopathologic analysis of a large series of microinvasive breast cancers. Breast J. 2018;24(4):574–9.CrossRefGoogle Scholar
  31. 31.
    Kapoor NS, Shamonki J, Sim MS, Chung CT, et al. Impact of multifocality and lymph node metastasis on the prognosis and management of microinvasive breast cancer. Ann Surg Oncol. 2013;20(8):2576–81.CrossRefGoogle Scholar
  32. 32.
    Sopik V, Sun P, Narod SA. Impact of microinvasion on breast cancer mortality in women with ductal carcinoma in situ. Breast Cancer Res Treat. 2018;167(3):787–795.CrossRefGoogle Scholar
  33. 33.
    Orzalesi L, Casella D, Criscenti V, Gjondedaj U, et al. Microinvasive breast cancer: pathological parameters, cancer subtypes distribution, and correlation with axillary lymph nodes invasion. Results of a large single-institution series. Breast Cancer. 2016;23(4):640–8.Google Scholar
  34. 34.
    Ko BS, Lim WS, Kim HJ, Yu JH, et al. Risk factor for axillary lymph node metastases in microinvasive breast cancer. Ann Surg Oncol. 2012;19(1):212–6.CrossRefGoogle Scholar
  35. 35.
    Matsen CB, Hirsch A, Eaton A, Stempel M, et al. Extent of microinvasion in ductal carcinoma in situ is not associated with sentinel lymph node metastases. Ann Surg Oncol. 2014;21(10):3330–5.CrossRefGoogle Scholar
  36. 36.
    Parikh RR, Haffty BG, Lannin D, Moran MS. Ductal carcinoma in situ with microinvasion: prognostic implications, long-term outcomes, and role of axillary evaluation. Int J Radiat Oncol Biol Phys. 2012;82(1):7–13.CrossRefGoogle Scholar
  37. 37.
    Gojon H, Fawunmi D, Valachis A. Sentinel lymph node biopsy in patients with microinvasive breast cancer: a systematic review and meta-analysis. Eur J Surg Oncol. 2014;40(1):5–11.CrossRefGoogle Scholar
  38. 38.
    Klauber-DeMore N, Tan LK, Liberman L, Kaptain S, et al. Sentinel lymph node biopsy: is it indicated in patients with high-risk ductal carcinoma-in-situ and ductal carcinoma-in-situ with microinvasion? Ann Surg Oncol. 2000;7(9):636–642.CrossRefGoogle Scholar
  39. 39.
    Wang W, Zhu W, Du F, Luo Y, et al. The Demographic features, clinicopathological characteristics and cancer-specific outcomes for patients with microinvasive breast cancer: a SEER database analysis. Sci Rep. 2017;7:42045.CrossRefGoogle Scholar
  40. 40.
    Sparano JA, Gray RJ, Makower DF, Pritchard KI, et al. Adjuvant chemotherapy guided by a 21-gene expression assay in breast cancer. N Engl J Med. 2018;379(2):111–121.CrossRefGoogle Scholar
  41. 41.
    Mittendorf EA, King TA. Routine use of oncotype DX recurrence score testing in node-positive hormone receptor-positive HER2-negative breast cancer: the time has come. Ann Surg Oncol. 2019;26(5):1173–5.CrossRefGoogle Scholar
  42. 42.
    Wang M, Wu K, Zhang P, Zhang M, et al. The prognostic significance of the oncotype DX recurrence score in T1-2N1M0 estrogen receptor-positive HER2-negative breast cancer based on the prognostic stage in the updated AJCC 8th edition. Ann Surg Oncol. 2019;26(5):1227–35.Google Scholar
  43. 43.
    Wang M, Wu K, Chen H. ASO Author reflections: oncotype DX RS complementing the prognostic stage in the updated AJCC 8th edition for T1-2N1M0 ER-positive HER2-negative breast cancer. Ann Surg Oncol. 2019;26(5):1236–7.Google Scholar
  44. 44.
    Bevilacqua JL, Kattan MW, Fey JV, Cody HS 3rd, et al. Doctor, what are my chances of having a positive sentinel node? A validated nomogram for risk estimation. J Clin Oncol. 2007;25(24):3670–9.CrossRefGoogle Scholar

Copyright information

© Society of Surgical Oncology 2019

Authors and Affiliations

  • Jessica C. Gooch
    • 1
    • 2
  • Freya Schnabel
    • 1
  • Jennifer Chun
    • 1
  • Elizabeth Pirraglia
    • 3
  • Andrea B. Troxel
    • 3
  • Amber Guth
    • 1
  • Richard Shapiro
    • 1
  • Deborah Axelrod
    • 1
  • Daniel Roses
    • 1
    Email author
  1. 1.Division of Breast Surgery, Department of Surgery, Perlmutter Comprehensive Cancer CenterNew York University Langone HealthNew YorkUSA
  2. 2.Division of Surgical Oncology, Department of SurgeryUniversity of Rochester Medical CenterRochesterUSA
  3. 3.Department of Population Health, Division of BiostatisticsNew York University Langone HealthNew YorkUSA

Personalised recommendations