Abstract
Background
Breast cancer is a heterogeneous disease with various histopathologic subtypes. Except for invasive carcinoma of no special type (NST), other subtypes are rare with limited data. The purpose of this study was to analyze the characteristics and prognosis of special histopathologic subtypes of breast cancer compared to NST.
Methods
A total of 136,140 patients were analyzed using the Korean Breast Cancer Society Registry database between January 1996 and March 2019. The clinicopathologic features and survival outcomes of special type breast carcinoma were compared with those of NST.
Results
The prevalence of special subtypes other than NST was 13.7% (n = 18,633). Compared to NST, patients with lobular, medullary, metaplastic, and micropapillary carcinoma had larger tumors (p < 0.001). Patients with mucinous, tubular, medullary, metaplastic, and cribriform carcinoma presented with less node metastasis (p < 0.001), contrary to patients with micropapillary carcinoma. Patients with lobular, mucinous, tubular, papillary, and cribriform carcinoma presented as luminal A subtype much more often (p < 0.001). Micropapillary carcinoma included more luminal B subtype (p < 0.001). Typically, medullary and metaplastic carcinoma included more triple-negative subtypes (p < 0.001). In survival analysis, only medullary (Hazard Ratio (HzR) 0.542, 95% CI 0.345 to 0.852, p = 0.008) and metaplastic carcinoma (HzR 1.655, 95% CI 1.317 to 2.080, p < 0.001) showed significantly different overall survival from NST by multivariate analysis.
Conclusion
Breast cancer had distinct clinicopathologic features according to histopathologic subtype. However, special types of breast cancer had similar survival outcomes compared to NST when adjusting for other prognostic factors, except for metaplastic carcinoma and medullary carcinoma.
Similar content being viewed by others
References
Weigelt B, Geyer FC, Reis-Filho JS (2010) Histological types of breast cancer: how special are they? Mol Oncol 4(3):192–208. https://doi.org/10.1016/j.molonc.2010.04.004
Abramson VG, Lehmann BD, Ballinger TJ, Pietenpol JA (2015) Subtyping of triple-negative breast cancer: implications for therapy. Cancer 121(1):8–16. https://doi.org/10.1002/cncr.28914
Lakhani SR, Ellis IO, Schnitt SJ, Tan PH, van de Vijver MJ (2012) WHO Classification of tumours of the breast, 4th edn. The International Agency for Research on Cancer (IARC), Lyon
Gannon LM, Cotter MB, Quinn CM (2013) The classification of invasive carcinoma of the breast. Expert Rev Anticancer Ther 13(8):941–954. https://doi.org/10.1586/14737140.2013.820577
Sinn HP, Kreipe H (2013) A brief overview of the WHO classification of breast tumors, 4th edition, focusing on issues and updates from the 3rd edition. Breast Care (Basel) 8(2):149–154. https://doi.org/10.1159/000350774
Cserni G (2020) Histological type and typing of breast carcinomas and the WHO classification changes over time. Pathologica 112(1):25–41. https://doi.org/10.32074/1591-951X-1-20
Chen AC, Paulino AC, Schwartz MR, Rodriguez AA, Bass BL, Chang JC, Teh BS (2014) Population-based comparison of prognostic factors in invasive micropapillary and invasive ductal carcinoma of the breast. Br J Cancer 111(3):619–622. https://doi.org/10.1038/bjc.2014.301
Shi WB, Yang LJ, Hu X, Zhou J, Zhang Q, Shao ZM (2014) Clinico-pathological features and prognosis of invasive micropapillary carcinoma compared to invasive ductal carcinoma: a population-based study from China. PLoS ONE 9(6):e101390. https://doi.org/10.1371/journal.pone.0101390
Park I, Kim J, Kim M, Bae SY, Lee SK, Kil WH, Lee JE, Nam SJ (2013) Comparison of the characteristics of medullary breast carcinoma and invasive ductal carcinoma. J Breast Cancer 16(4):417–425. https://doi.org/10.4048/jbc.2013.16.4.417
Huober J, Gelber S, Goldhirsch A, Coates AS, Viale G, Ohlschlegel C, Price KN, Gelber RD, Regan MM, Thurlimann B (2012) Prognosis of medullary breast cancer: analysis of 13 International Breast Cancer Study Group (IBCSG) trials. Ann Oncol 23(11):2843–2851. https://doi.org/10.1093/annonc/mds105
Bae SY, Lee SK, Koo MY, Hur SM, Choi MY, Cho DH, Kim S, Choe JH, Lee JE, Kim JH, Kim JS, Nam SJ, Yang JH (2011) The prognoses of metaplastic breast cancer patients compared to those of triple-negative breast cancer patients. Breast Cancer Res Treat 126(2):471–478. https://doi.org/10.1007/s10549-011-1359-8
Vranic S, Schmitt F, Sapino A, Costa JL, Reddy S, Castro M, Gatalica Z (2013) Apocrine carcinoma of the breast: a comprehensive review. Histol Histopathol 28(11):1393–1409. https://doi.org/10.14670/HH-28.1393
Zhao S, Ma D, Xiao Y, Jiang YZ, Shao ZM (2018) Clinicopathologic features and prognoses of different histologic types of triple-negative breast cancer: a large population-based analysis. Eur J Surg Oncol 44(4):420–428. https://doi.org/10.1016/j.ejso.2017.11.027
Ahn SH, Son BH, Kim SW, Kim SI, Jeong J, Ko SS, Han W, Korean Breast Cancer S (2007) Poor outcome of hormone receptor-positive breast cancer at very young age is due to tamoxifen resistance: nationwide survival data in Korea—a report from the Korean Breast Cancer Society. J Clin Oncol 25(17):2360–2368. https://doi.org/10.1200/JCO.2006.10.3754
Hammond ME, Hayes DF, Dowsett M, Allred DC, Hagerty KL, Badve S, Fitzgibbons PL, Francis G, Goldstein NS, Hayes M, Hicks DG, Lester S, Love R, Mangu PB, McShane L, Miller K, Osborne CK, Paik S, Perlmutter J, Rhodes A, Sasano H, Schwartz JN, Sweep FC, Taube S, Torlakovic EE, Valenstein P, Viale G, Visscher D, Wheeler T, Williams RB, Wittliff JL, Wolff AC (2010) American Society of Clinical Oncology/College Of American Pathologists guideline recommendations for immunohistochemical testing of estrogen and progesterone receptors in breast cancer. J Clin Oncol 28(16):2784–2795. https://doi.org/10.1200/JCO.2009.25.6529
Allred DC, Harvey JM, Berardo M, Clark GM (1998) Prognostic and predictive factors in breast cancer by immunohistochemical analysis. Mod Pathol 11(2):155–168
Hoon Tan P, Ellis I, Allison K, Brogi E, Fox SB, Lakhani S, Lazar AJ, Morris EA, Sahin A, Salgado R, Sapino A, Sasano H, Schnitt S, Sotiriou C, van Diest P, White VA, Lokuhetty D, Cree IA, Board WHOCoTE (2020) The 2019 WHO classification of tumours of the breast. Histopathology. https://doi.org/10.1111/his.14091
Lee JH, Park S, Park HS, Park BW (2010) Clinicopathological features of infiltrating lobular carcinomas comparing with infiltrating ductal carcinomas: a case control study. World J Surg Oncol 8:34. https://doi.org/10.1186/1477-7819-8-34
Ko SS, Korean Breast Cancer S (2008) Chronological changing patterns of clinical characteristics of Korean breast cancer patients during 10 years (1996–2006) using nationwide breast cancer registration on-line program: biannual update. J Surg Oncol 98(5):318–323. https://doi.org/10.1002/jso.21110
Kang SY, Kim YS, Kim Z, Kim HY, Lee SK, Jung KW, Youn HJ, Korean Breast Cancer S (2018) Basic findings regarding breast cancer in Korea in 2015: data from a breast cancer registry. J Breast Cancer 21(1):1–10. https://doi.org/10.4048/jbc.2018.21.1.1
Arpino G, Bardou VJ, Clark GM, Elledge RM (2004) Infiltrating lobular carcinoma of the breast: tumor characteristics and clinical outcome. Breast Cancer Res 6(3):R149–156. https://doi.org/10.1186/bcr767
Wasif N, Maggard MA, Ko CY, Giuliano AE (2010) Invasive lobular vs. ductal breast cancer: a stage-matched comparison of outcomes. Ann Surg Oncol 17(7):1862–1869. https://doi.org/10.1245/s10434-010-0953-z
Pestalozzi BC, Zahrieh D, Mallon E, Gusterson BA, Price KN, Gelber RD, Holmberg SB, Lindtner J, Snyder R, Thurlimann B, Murray E, Viale G, Castiglione-Gertsch M, Coates AS, Goldhirsch A, International Breast Cancer Study Group (2008) Distinct clinical and prognostic features of infiltrating lobular carcinoma of the breast: combined results of 15 International Breast Cancer Study Group clinical trials. J Clin Oncol 26(18):3006–3014. https://doi.org/10.1200/JCO.2007.14.9336
Cao AY, Huang L, Wu J, Lu JS, Liu GY, Shen ZZ, Shao ZM, Di GH (2012) Tumor characteristics and the clinical outcome of invasive lobular carcinoma compared to infiltrating ductal carcinoma in a Chinese population. World J Surg Oncol 10:152. https://doi.org/10.1186/1477-7819-10-152
Truin W, Vugts G, Roumen RM, Maaskant-Braat AJ, Nieuwenhuijzen GA, van der Heiden-van der Loo M, Tjan-Heijnen VC, Voogd AC (2016) Differences in response and surgical management with neoadjuvant chemotherapy in invasive lobular versus ductal breast cancer. Ann Surg Oncol 23(1):51–57. https://doi.org/10.1245/s10434-015-4603-3
Fisher ER, Anderson S, Redmond C, Fisher B (1993) Pathologic findings from the national surgical adjuvant breast project protocol B-06. 10-year pathologic and clinical prognostic discriminants. Cancer 71(8):2507–2514. https://doi.org/10.1002/1097-0142(19930415)71:8<2507:aid-cncr2820710813>3.0.co;2-0
Colleoni M, Rotmensz N, Maisonneuve P, Mastropasqua MG, Luini A, Veronesi P, Intra M, Montagna E, Cancello G, Cardillo A, Mazza M, Perri G, Iorfida M, Pruneri G, Goldhirsch A, Viale G (2012) Outcome of special types of luminal breast cancer. Ann Oncol 23(6):1428–1436. https://doi.org/10.1093/annonc/mdr461
National Comprehensive Cancer Network (2019) Breast Cancer (Version 2. 2019). https://www.nccn.org/professionals/physician_gls/pdf/breast.pdf. Accessed 18 July 2019
Liu XY, Jiang YZ, Liu YR, Zuo WJ, Shao ZM (2015) Clinicopathological characteristics and survival outcomes of invasive cribriform carcinoma of breast: a SEER population-based study. Medicine (Baltimore) 94(31):e1309. https://doi.org/10.1097/MD.0000000000001309
Zheng YZ, Hu X, Shao ZM (2016) Clinicopathological characteristics and survival outcomes in invasive papillary carcinoma of the breast: a SEER population-based study. Sci Rep 6:24037. https://doi.org/10.1038/srep24037
Ong CT, Campbell BM, Thomas SM, Greenup RA, Plichta JK, Rosenberger LH, Force J, Hall A, Hyslop T, Hwang ES, Fayanju OM (2018) Metaplastic breast cancer treatment and outcomes in 2500 Patients: a retrospective analysis of a national oncology database. Ann Surg Oncol 25(8):2249–2260. https://doi.org/10.1245/s10434-018-6533-3
Nelson RA, Guye ML, Luu T, Lai LL (2015) Survival outcomes of metaplastic breast cancer patients: results from a US population-based analysis. Ann Surg Oncol 22(1):24–31. https://doi.org/10.1245/s10434-014-3890-4
Tzanninis IG, Kotteas EA, Ntanasis-Stathopoulos I, Kontogianni P, Fotopoulos G (2016) Management and outcomes in metaplastic breast cancer. Clin Breast Cancer 16(6):437–443. https://doi.org/10.1016/j.clbc.2016.06.002
Liao HY, Zhang WW, Sun JY, Li FY, He ZY, Wu SG (2018) The clinicopathological features and survival outcomes of different histological subtypes in triple-negative breast cancer. J Cancer 9(2):296–303. https://doi.org/10.7150/jca.22280
Mills MN, Yang GQ, Oliver DE, Liveringhouse CL, Ahmed KA, Orman AG, Laronga C, Hoover SJ, Khakpour N, Costa RLB, Diaz R (2018) Histologic heterogeneity of triple negative breast cancer: a national cancer centre database analysis. Eur J Cancer 98:48–58. https://doi.org/10.1016/j.ejca.2018.04.011
Loi S, Drubay D, Adams S, Pruneri G, Francis PA, Lacroix-Triki M, Joensuu H, Dieci MV, Badve S, Demaria S, Gray R, Munzone E, Lemonnier J, Sotiriou C, Piccart MJ, Kellokumpu-Lehtinen PL, Vingiani A, Gray K, Andre F, Denkert C, Salgado R, Michiels S (2019) Tumor-infiltrating lymphocytes and prognosis: a pooled individual patient analysis of early-stage triple-negative breast cancers. J Clin Oncol 37(7):559–569. https://doi.org/10.1200/JCO.18.01010
Miyai K, Schwartz MR, Divatia MK, Anton RC, Park YW, Ayala AG, Ro JY (2014) Adenoid cystic carcinoma of breast: recent advances. World J Clin Cases 2(12):732–741. https://doi.org/10.12998/wjcc.v2.i12.732
Kulkarni N, Pezzi CM, Greif JM, Suzanne Klimberg V, Bailey L, Korourian S, Zuraek M (2013) Rare breast cancer: 933 adenoid cystic carcinomas from the National Cancer Data Base. Ann Surg Oncol 20(7):2236–2241. https://doi.org/10.1245/s10434-013-2911-z
Collins LC, Carlo VP, Hwang H, Barry TS, Gown AM, Schnitt SJ (2006) Intracystic papillary carcinomas of the breast: a reevaluation using a panel of myoepithelial cell markers. Am J Surg Pathol 30(8):1002–1007
Guo S, Wang Y, Rohr J, Fan C, Li Q, Li X, Wang Z (2016) Solid papillary carcinoma of the breast: a special entity needs to be distinguished from conventional invasive carcinoma avoiding over-treatment. Breast 26:67–72. https://doi.org/10.1016/j.breast.2015.12.015
Stamatakos M, Stefanaki C, Stasinou T, Papantoni E, Alexiou I, Kontzoglou K (2011) Intracystic papillary carcinoma of the breast in males. In search of the optimal treatment for this rare disease. Breast Care (Basel) 6(5):399–403. https://doi.org/10.1159/000331386
Horowitz DP, Sharma CS, Connolly E, Gidea-Addeo D, Deutsch I (2012) Secretory carcinoma of the breast: results from the survival, epidemiology and end results database. Breast 21(3):350–353. https://doi.org/10.1016/j.breast.2012.02.013
Pareja F, Geyer FC, Marchio C, Burke KA, Weigelt B, Reis-Filho JS (2016) Triple-negative breast cancer: the importance of molecular and histologic subtyping, and recognition of low-grade variants. NPJ Breast Cancer 2:16036. https://doi.org/10.1038/npjbcancer.2016.36
McDivitt RW, Stewart FW (1966) Breast carcinoma in children. JAMA 195(5):388–390
Hull MT, Seo IS, Battersby JS, Csicsko JF (1980) Signet-ring cell carcinoma of the breast: a clinicopathologic study of 24 cases. Am J Clin Pathol 73(1):31–35. https://doi.org/10.1093/ajcp/73.1.31
Bartosch C, Mendes N, Rios E, Rodrigues M, Eloy C, Reis CA, Amendoeira I (2015) Morphological features and mucin expression profile of breast carcinomas with signet-ring cell differentiation. Pathol Res Pract 211(8):588–595. https://doi.org/10.1016/j.prp.2015.05.003
Acknowledgements
This article was supported by the Korean Breast Cancer Society.
Author information
Authors and Affiliations
Consortia
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflicts of interest.
Ethical approval
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.
Informed consent
For this type of study, informed consent was not required.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Kim, J., Kim, J.Y., Lee, HB. et al. Characteristics and prognosis of 17 special histologic subtypes of invasive breast cancers according to World Health Organization classification: comparative analysis to invasive carcinoma of no special type. Breast Cancer Res Treat 184, 527–542 (2020). https://doi.org/10.1007/s10549-020-05861-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10549-020-05861-6