Micropapillary Breast Carcinoma: From Molecular Pathogenesis to Prognosis

Figures & data

Figure 1 (A–D) In low magnification, through an atrophic mammary gland a neoplastic population is recognized, infiltrating the remaining ducts (A). The cells are organized in clusters, forming small-sized glandular structures and nests, arranged in a micropapillary pattern (B). Occasionally, a small proportion of them acquire a central lumina. Fibrovascular cores are absent. (C) The neoplastic cells have a moderate amount of eosinophilic cytoplasm and small round nuclei with condensed chromatin and intermediate pleomorphism. (D). In another slide of this lesion, a lymphovascular emboli is recognized (D). The morphology is highly suggestive of invasive micropapillary carcinoma, so immunohistochemical markers are performed to establish the diagnosis.

Notes: Reproduced from: Verras GI, Mulita F, Tchabashvili L, et al. A rare case of invasive micropapillary carcinoma of the breast. Menopause Review/Przegląd Menopauzalny. 2022;21(1):1-8. doi:10.5114/pm.2022.113834.¹⁶¹ Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0) License (http://creativecommons.org/licenses/by-nc-sa/4.0/).

Figure 2 Report selection flowchart.

Table 1 Data on Tumor Size, Tumor Grade, Nodal Status and LVI from Included Studies

Study	Study Type	Tumor Size in IMPC Patients	Histological Tumor Grade in IMPC Patients	Nodal Status of IMPC Patients	LVI Status of IMPC Patients	Comparison with Other Histological Subtypes
Stranix et al (2015)^Citation4	Literature Review	–	–	LN positivity in 71.2% (1267/1280 patients)	LVI observed in 73.7% (638/866 patients)	–
Vingiani et al (2013)^Citation6	Case–Control Study	T3-T4 in 12.2% of the patients	Grade III in 32.7% of the patients	LN positivity in 69.4% of the patients	LVI observed in 61.2% of the patients	Tumor size, nodal positivity and LVI rates was higher in IMPC patients compared to IDC patients (5.3%, 47.3% and 61.2%, respectively)
Tang et al (2017)^Citation13	Case–Control Study	T3-T4 in 9.2% of the patients	–	LN positivity in 64.9% of the patients	LVI observed in 14.7% of the patients	Nodal positivity and LVI differed significantly in IMPC patients compared to IDC patients (46.8% and 0.1%, respectively) No difference in tumor size
Cui et al (2014)^Citation14	Case Series Study	–	–	LN positivity in 80% of the patients	LVI observed in 44% of the patients	–
Hashmi et al (2018)^Citation15	Case–Control Study	T3 in 11.1% of the patients	Grade III in 26.7% of the patients	LN positivity in 55.6% of the patients	LVI observed in 77.8% of the patients	LVI differed significantly in IMPC patients compared to IDC patients (24.8%) No difference in tumor size, tumor grade or nodal invasion
Pettinato et al (2002)^Citation16	Case Series Study	–	–	LN positivity in 90% of the patients	LVI in 72% of the patients	–
Chen et al (2017)^Citation23	Case-Control Study	T3-T4 in 10.2% of the patients	Grade III in 22.6% of the patients	LN positivity in 51.3% of the patients	–	No observed difference in tumor size, grade or LN positivity when compared with IMPC patients
Yu et al (2015)^Citation28	Case–Control Study	T3 in 5.2% of the patients	Grade III in 40.1% of the patients	LN positivity in 69.3% of the patients	LVI in 61.8% of the patients	LVI differed significantly in IMPC patients compared to IDC patients (43.4%) No difference in tumor size, tumor grade or nodal invasion
Zekioglou et al (2004)^Citation30	Case–Control Study	–	Grade III in 82% of the patients	LN positivity in 69% of the patients	LVI in 75.5% of the patients	Tumor grade, nodal positivity and LVI differed were significantly higher in IMPC compared to IDC patients.
Chen et al (2014)^Citation32	Case–Control Study	T3-T4 in 10% of the patients	Grade III in 40% of the patients	LN positivity in in 52% of the patients	–	Tumor size, tumor grade and LN positivity were significantly higher in IMPC compared to IDC patients.
Gokce et al (2013)^Citation33	Case-Control Study	–	Grade III in 40.8% of the patients	LN positivity in 59.3% of the patients	LVI in 94.7% of the patients	Nodal positivity and LVI were seen significantly more frequently in IMPC patients than IDC patients
Akdeniz et al (2020)^Citation38	Case Series Study	T3-T4 in 33.3% of the patients	–	LN positivity in 79.2% of the patients	–	–
Lewis et al (2019)^Citation41	Case Series Study	–	Grade III in 34.7% of the patients	–	–	–
Ye et al (2018)^Citation42	Case Series Study	–	Grade III in 37.17% of the patients	LN positivity in 50.46% of the patients	–	–
Paterakos et al (1999)^Citation43	Case-Control Study	–	–	LN positivity in 94% of the patients	–	Nodal positivity and number of infiltrated lymph nodes were higher in IMPC patients compared to IDC patients.
Hao et al (2019)^Citation44	Case–Control Study	T3-T4 in 59% of the patients	–	LN positivity in 69.1% of the patients	LVI in 71.3% of the patients	No difference in nodal positivity and LVI after matching, for IMPC patients and IDC patients
De La Cruz et al (2004)^Citation46	Case–Control Study	–	Grade III in 81.3% of the patients	LN positivity in 92.9% of the patients	–	Higher grade tumors and LN positivity were higher in IMPC compared to IDC patients
Chen et al (2013)^Citation47	Case Series Study	T3-T4 in 12% of the patients	Grade III in 38% of the patients	LN positivity in 53% of the patients	–	–
Kaya et al (2018)^Citation48	Case Series Study	T3-T4 in 5.3% of the patients	Grade III in 42.1% of the patients	LN positivity in 68% of the patients	LVI in 84.2% of the patients	Nodal positivity and LVI were higher in tumors with >75% micropapillary component
Walsh et al (2001)^Citation52	Case Series Study	T3 in 7.5% of the patients	Grade III in 67.5% of the patients	LN positivity in 72.3% of the patients	LVI in 62.5% of the patients	–
Kim et al (2020)^Citation58	Case–Control Study	T3-T4 in 11% of the patients	Grade III in 34% of the patients	LN positivity in 67.4% of the patients	LVI in 67.2% of the patients	Tumor size, nodal positivity, LVI and grade were higher in IMPC patients compared to IDC patients
Lee et al (2011)^Citation98	Case Series Study	T3-T4 in 43% of the patients	Grade III in 55% of the patients	–	–	–
Guan et al (2020)^Citation101	Case–Control Study	T3-T4 in 1.5% of the patients	–	LN positivity in 60.8% of the patients	LVI in 78.9% of the patients	Nodal positivity and LVI were significantly higher in tumors with IMPC component, compared to DCIS component
Kim et al (2005)^Citation102	Case–Control Study	T3-T4 in 18.4% of the patients	Grade III in 44.7% of the patients	LN positivity in 78.9% of the patients	LVI in 60.5% of the patients
Collins et al (2017)^Citation108	Case Series Study	T3-T4 in 21% of the patients	Grade III in 21% of the patients	LN positivity in 42.8% of the patients	LVI in 21.4% of the patients	–
Yoon et al (2019)^Citation124	Case–Control Study	–	Grade III in 37.7% of the patients	LN positivity in 63.6% of the patients	LVI in 52% of the patients	After propensity matching, nodal status, Histological grade, and LVI rates did not differ between IMPC and IDC patients
Kim et al (2010)^Citation128	Case–Control Study	T3 in 8.3% of the patients	Grade III in 41% of the patients	LN positivity in 70.5% of the patients	LVI in 75.4% of the patients	Nodal positivity, histological grade and LVI were significantly higher in tumors with IMPC component, compared to DCIS component
Chen et al (2018)^Citation143	Case–Control Study	T3 in 22.1% of the patients	–	LN positivity in 72.6% of the patients	LVI in 51.65 of the patients	Tumor size, nodal positivity and LVI rates were higher in IMPC patients compared to TN-IDC patients
Li et al (2019)^Citation144	Case–Control Study	T3-T4 in 11.79% of the patients	Grade III in 62.71% of the patients	LN positivity in 51.5% of the patients	–	Tumor size and nodal positivity rates were higher compared to IDC patients
Li et al (2016)^Citation147	Case–Control Study	T3-T4 in 24.2% of the patients	–	LN positivity in 79.8% of the patients	LVI in 18.2% of the patients	Nodal positivity and LVI rates were higher in IMPC than IDC patients
Lewis et al (2019)^Citation148	Case Series Study	T3-T4 in 8% of the patients	Grade III in 36.5% of the patients	LN positivity in 53.3% of the patients	–	–
Liu et al (2014)^Citation149	Case–Control Study	T3 in 5.88% of the patients	Grade III in 49.02% of the patients	LN positivity in 69.6% of the patients	LVI in 52.94% of the patients	LVI rates were higher compared to IDC patients
Liu et al (2015)^Citation151	Case–Control Study	–	Grade III in 16.4% of the patients	LN positivity in 80.8% of the patients	LVI in 82.9% of the patients	Histological grade, nodal positivity, and LVI rates were higher compared to the mucinous carcinoma group
Kuroda et al (2004)^Citation153	Case Series Study	T3-T4 in 33.3% of the patients	–	LN positivity in 66.6% of the patients	LVI in 88.8% of the patients	–
Shi et al (2014)^Citation154	Case–Control Study	T3-T4 in 9.6% of the patients	–	LN positivity in 73.4% of the patients	LVI in 75.4% of the patients	Tumor size, nodal positivity and LVI rates were higher in IMPC patients compared to IDC patients
Meng et al (2021)^Citation155	Case Series Study	T3-T4 in 6.96% of the patients	Grade III in 14.95% of the patients	LN positivity in 30.4% of the patients	LVI in 42.27% of the patients	–

Table 2 Data on Hormone Receptor and HER-2 Status of IMPC Patients from Included Studies

Study	Study Type	HR Status of IMPC Tumors	PR Status of IMPC Tumors	HER-2 Status of IMPC Tumors	Comparison with Other Histological Subtypes
Stranix et al (2015)^Citation4	Literature Review	Positive in 73.4% of the patients	Positive in 62.5% of the patients	Positive in 40.5% of the patients	–
Vingiani et al (2013)^Citation6	Case–Control Study	Positive in 87.8% of the patients	Positive in 69.4% of the patients	Positive in 18.4% of the patients	No observed differences compared to IDC patients.
Tang et al (2017)^Citation13	Case–Control Study	Positive in 83.5% of the patients	Positive in 78.2% of the patients	Positive in 34% of the patients	HR, PR and HER-2 positivity was observed more frequently in IMPC patients compared to IDC patients.
Cui et al (2014)^Citation14	Clinicopathological Study	Positive in 88% of the patients	Positive in 64% of the patients	Positive in 84% of the patients	–
Hashmi et al (2018)^Citation15	Case–Control Study	Positive in 86.7% of the patients	Positive in 73.3% of the patients	Positive in 60% of the patients	HR and PR positivity were seen more frequently in IMPC, compared to IDC patients
Pettinato et al (2002)^Citation16	Case Series Study	Positive in 36% of the patients	Positive in 27% of the patients	Positive in 72% of the patients	–
Yu et al (2015)^Citation28	Case–Control Study	Positive in 66.3% of the patients	Positive in 66.3% of the patients	Positive in 28.8% of the patients	HER2 positivity was observed more frequently in IMPC patients compared to IDC patients
Zekioglou et al (2004)^Citation30	Case–Control Study	Positive in 68% of the patients	Positive in 61% of the patients	Positive in 54% of the patients	HR and PR positivity were seen more frequently in IMPC compared to IDC patients
Chen et al (2014)^Citation32	Case–Control Study	Positive in 84.1% of the patients	Positive in 70.2% of the patients	–	HR and PR positivity were seen more frequently in IMPC compared to IDC patients
Gokce et al (2013)^Citation33	Case–Control Study	Positive in 70.3% of the patients	Positive in 77.3% of the patients	Positive in 52.5% of the patients	No observed differences compared to IDC patients
Akdeniz et al (2020)^Citation38	Case Series Study	Positive in 66.7% of the patients	Positive in 66.7% of the patients	Positive in 45.8% of the patients	–
Ye et al (2018)^Citation42	Case Series Study	Positive in 89.48% of the patients	Positive in 77.83% of the patients	Positive in 12.15% of the patients	–
Paterakos et al (1999)^Citation43	Case–Control Study	Positive in 61% of the patients	–	Positive in 77% of the patients	HER2 positivity was observed more frequently in IMPC patients compared to IDC patients
Hao et al (2019)^Citation44	Case–Control Study	Positive in 84.3% of the patients	Positive in 84.3% of the patients	Positive in 33% of the patients	No observed differences compared to IDC patients.
De La Cruz et al (2004)^Citation46	Case–Control Study	Positive in 50% of the patients	Positive in 31.2% of the patients	Positive in 50% of the patients	HR, PR and HER-2 positivity were seen more frequently in IMPC compared to IDC patients
Chen et al (2013)^Citation47	Case Series Study	Positive in 85% of the patients	Positive in 70% of the patients	–	–
Kuroda et al (2004)^Citation51	Case–Control Study	Positive in 70.3% of the patients	Positive in 55.5% of the patients	Positive in 25.9% of the patients	No observed differences compared to IDC patients
Walsh et al (2001)^Citation52	Case Series Study	Positive in 90.6% of the patients	Positive in 70.3% of the patients	–	–
Kim et al (2020)^Citation58	Case–Control Study	Positive in 75.8% of the patients	Positive in 63.2% of the patients	Positive in 33.3% of the patients	HR, PR and HER-2 positivity were seen more frequently in IMPC compared to IDC patients
Perron et al (2021)^Citation62	Case Series Study	Positive in 94% of the patients	Positive in 80.5% of the patients	Positive in 22.5% of the patients	–
Lee et al (2011)^Citation98	Case Series Study	Positive in 83% of the patients	Positive in 67% of the patients	Positive in 7% of the patients	–
Guan et al (2020)^Citation101	Case–Control Study	Positive in 82.3% of the patients	Positive in 56.2% of the patients	Positive in 30% of the patients	HR and HER2 positivity were seen more frequently in IMPC patients, compared to IDC patients. PR positivity was more frequent in IDC patients
Kim et al (2005)^Citation102	Case–Control Study	Positive in 19.4% of the patients	Positive in 19.4% of the patients	Positive in 38.9% of the patients	No observed differences compared to non-IMPC patients
Collins et al (2017)^Citation108	Case Series Study	Positive in 100% of the patients	Positive in 85.7% of the patients	Positive in 14.2% of the patients	–
Yoon et al (2019)^Citation124	Case–Control Study	Positive in 79.2% of the patients	Positive in 60.7% of the patients	Positive in 38% of the patients	After propensity score matching, HER-2 positivity was significantly higher in IMPC patients compared to IDC patients. No observed difference in ER or PR positivity
Kim et al (2010)^Citation140	Case–Control Study	Positive in 77% of the patients	Positive in 73.8% of the patients	Positive in 39.3% of the patients	No observed difference between IMPC and IDC patients
Chen et al (2018)^Citation143	Case–Control Study	Positive in 83.2% of the patients	Positive in 74.7% of the patients	Positive in 21.1% of the patients	–
Li et al (2019)^Citation144	Case–Control Study	Positive in 88.69% of the patients	Positive in 78.75% of the patients	–	ER and PR positivity rates were higher in IMPC patients, compared to IDC patients
Li et al (2016)^Citation147	Case–Control Study	Positive in 81.8% of the patients	Positive in 75.8% of the patients	Positive in 18.8% of the patients	ER positivity rates were significantly higher compared to IDC patients
Lewis et al (2019)^Citation148	Case Series Study	Positive in 87.5% of the patients	Positive in 79.4% of the patients	Positive in 14.9% of the patients	–
Liu et al (2014)^Citation149	Case–Control Study	Positive in 84.31% of the patients	Positive in 72.5% of the patients	Positive in 15.69% of the patients	ER positivity rates were significantly higher compared to IDC patients
Liu et al (2015)^Citation151	Case–Control Study	Positive in 83.3% of the patients	Positive in 74% of the patients	Positive in 28.8% of the patients	HR, PR and HER-2 positivity were seen more frequently in tumors with micropapillary histology, compared to pure mucinous histology
Shi et al (2014)^Citation154	Case–Control Study	Positive in 85.1% of the patients	Positive in 78.2% of the patients	Positive in 29.9% of the patients	ER and PR positivity rates were higher in IMPC patients compared to IDC patients
Meng et al (2021)^Citation155	Case Series Study	Positive in 78.09% of the patients	Positive in 65.46% of the patients	Positive in 33.99% of the patients	–

Figure 3 (A) Preoperative and pre-treatment MRI image of IMPC. White arrow indicates the central mass of the lesion along with mass and non-mass enhancement. (B) MRI findings post-PST consistent with complete pathologic response. White arrow indicates local scarring in the mass area after PST. Although imaging indicated complete pathological response, residual disease was still found in the scarring area when examined under a microscope, and complete mastectomy was deemed appropriate.

Table 3 Data on Local Recurrence, Distant Metastasis, and Survival from the Included Studies

Study	Study Type	Local Recurrence Rate of IMPC Patients	Rate of Distant Metastases of IMPC Patients	Survival of IMPC Patients	Comparison with Other Histological Subtypes.
Stranix et al (2015)^Citation4	Literature Review	6–80% of the patients (study-dependent)	1–49% of the patients	20–95% of the patients	–
Vingiani et al (2013)^Citation6	Case–Control Study	6.1% of the patients	8.2% of the patients	89.8% of the patients	Local recurrence rates and 10-year mortality were higher in IMPC patients compared to IDC patients. No observed difference in distant metastases
Wu et al (2017)^Citation7	Meta-Analysis	Locoregional relapse-free survival OR compared to IDC was 2.82	Distant metastasis-free survival OR compared to IDC was 0.95.	Overall survival OR compared to IDC was 0.90	IMPC patients have a higher incidence of locoregional relapse compared to IDC patients. Survival of IMPC and IDC patients did not differ.
Tang et al (2017)^Citation13	Case–Control Study	Locoregional recurrence in 4.2% of the IMPC patients	Distant metastasis in 8.2% of the IMPC patients	10-year Overall survival of 84.3% for IMPC patients	Regional and distant relapse-free survival was worse, compared to IDC patients
Cui et al (2014)^Citation14	Clinicopathological Study	Locoregional recurrence in 4% of the patients	Distant metastasis in 8% of the IMPC patients	92% of the patients with an average of 36.5 months of follow-up	–
Pettinato et al (2002)^Citation16	Case Series Study	Locoregional recurrence in 36% of the patients	Distant metastasis in 45% of the IMPC patients	55% of the patients with an average of 28 months of follow-up	–
Chen et al (2017)^Citation23	Case–Control Study	–	–	Overall survival HR compared to IDC was 0.67. Breast Cancer Specific Survival compared to IDC was 0.628.	Compared to IDC patients, IMPC patients had more favorable survival. IMPC histology was an indpendent prognostic factor for survival.
Yu et al (2015)^Citation28	Case–Control Study	Locoregional recurrence free	–	10-year Overall Survival of 92.4% of the IMPC patients. Survival HR compared to IDC was 2.56	Compared to IDC patients, IMPC patients had more favorable locoregional recurrence free survival. IMPC histology was an independent prognostic factor for survival.
Zekioglou et al (2004)^Citation30	Case–Control Study	Locoregional recurrence in 22.2% of the patients	Distant metastasis in 25% of the IMPC patients	72% of the patients with an average of 56.5 months of follow-up	–
Chen et al (2014)^Citation32	Case–Control Study	–	–	5-year DSS survival was 91.8% and OS was 82.9% of the patients on average	No difference was found in OS or DSS of IMPC patients compared to IDC patients
Gokce et al (2013)^Citation33	Case–Control Study	Locoregional recurrence in 6.9% of the patients	Distant metastasis in 23% of the IMPC patients	75.9% of the patients with an average of 64.7 months of follow-up	No difference was found in OS of IMPC patients compared to IDC patients
Hao et al (2019)^Citation44	Case–Control Study	Locoregional recurrence in 15.4% of the patients	Distant metastasis in 13.6% of the IMPC patients	85% of the patients with an average of 80 months of follow-up	No difference in OS or DFS between IMPC and IDC patients.
Ye et al (2020)^Citation45	Meta-Analysis	Locoregional recurrence OR was 3.60 compared to IDC	–	Overall survival OR compared to IDC was 0.87	No difference in OS between IMPC and IDC patients. Higher locoregional recurrence rates of IMPC patients compared to IDC patients.
Chen et al (2013)^Citation47	Case Series Study	–	Distant metastasis in 4.1% of the IMPC patients	5-year DS survival was at 91.9% and OS at 83.8%	–
Kaya et al (2018)^Citation48	Case Series Study	Locoregional recurrence in 15.8% of the patients	Distant metastasis in 5.3% of the patients	95.7% of the patients with an average of 48.87 months of follow-up	No difference in recurrence rates or survival, between patients with low or high percentage of micropapillary pattern
Kim et al (2020)^Citation58	Case–Control Study	–	–	–	No difference in overall survival between IMPC and NST patients, in multivariate analysis
Guan et al (2020)^Citation101	Case–Control Study	Locoregional recurrence in 3.1% of the patients	Distant metastasis in 20% of the patients	HR for OS for patients with IMPC component was 1.677 when compared to IDC patients	Locoregional recurrence was lower for IMPC patients compared to IDC patients. OS was better for IMPC patients. Distant metastasis rates were higher for IMPC patients
Kim et al (2005)^Citation102	Case–Control Study	Locoregional recurrence in 10.5% of the patients	Distant metastasis in 34.2% of the patients	–	Locoregional recurrence and distant metastasis rates did not differ between IMPC and non-IMPC patients.
Yoon et al (2019)^Citation124	Case–Control Study	Local recurrence HR was 2.86 compared to IDC patients	Distant metastasis HR was 1.85 compared to IDC patients	HR for death in IMPC patients compared to IDC patients was 1.30	Local and distant recurrence rates were significantly higher in IMPC patients, compared to IDC patients. No observed difference in overall survival.
Kim et al (2010)^Citation139	Case–Control Study	Locoregional recurrence in 13.1% of the patients	–	–	No significant difference in recurrence rates between IMPC and IDC patients. IMPC histology was not independently associated with recurrence
Chen et al (2018)^Citation142	Case–Control Study	5-year Locoregional recurrence in 28.6% of the patients	5-year Distant metastasis in 20.2% of the patients	5-year OS 81.9% for IMPC patients	Locoregional recurrence was associated with LN positivity, and was more frequent in IMPC patients. No difference in metastasis rates or OS, compared to TN-IDC patients.
Li et al (2019)^Citation143	Case–Control Study	–	–	3-year, 5-year and 10-year survival of 95.9%, 92.3% and 82.1% of the patients respectively	IMPC patients had better OS rates when compared to IDC patients, after propensity score matching
Li et al (2016)^Citation146	Case–Control Study	Locoregional recurrence in 5.1% of the patients after a mean of 39 months of follow-up	Distant metastasis in 9.1% of the patients after a mean of 39 months of follow-up	97% of the patients after a mean of 39 months of follow-up	No observed difference in survival or recurrence rates, compared to IDC patients
Lewis et al (2019)^Citation147	Case Series Study	–	–	5-year OS of 87.5%	–
Liu et al (2015)^Citation150	Case–Control Study	Micropapillary features in histological examination had an HR for RFS of 21.23	–	Micropapillary features in histological examination had no efffect on OS	Mucinous carcinoma with micropapillary features had worse RFS, but non-inferior OS compared to pure mucinous carcinoma
Kuroda et al (2004)^Citation152	Case Series Study	–	–	6-year OS of 41.2%	–
Shi et al (2014)^Citation153	Case–Control Study	5-year RFS of 67.1%	–	5-year BCSS of 75.9%	Recurrence and death rates were higher for IMPC patients compared to IDC patients
Meng et al (2021)^Citation154	Case Series Study	Locoregional recurrence in 18.5% of the patients after 59-month average follow-up	–	–	–

Verras GI, Mulita F, Tchabashvili L, et al. A rare case of invasive micropapillary carcinoma of the breast. Menopause Review/Przegląd Menopauzalny. 2022;21(1):1-8. doi:10.5114/pm.2022.113834

 Google Scholar

Stranix JT, Kwa MJ, Shapiro RL, Speyer JL. Invasive micropapillary carcinoma of the male breast: case report and review of the literature. Cancer Treat Commun. 2015;3:44–49. doi:10.1016/j.ctrc.2014.12.001

 Google Scholar

Vingiani A, Maisonneuve P, Dell’Orto P, et al. The clinical relevance of micropapillary carcinoma of the breast: a case-control study. Histopathology. 2013;63:217–224. doi:10.1111/his.12147

 PubMed Web of Science ®Google Scholar

Tang S-L, Yang J-Q, Du Z-G, et al. Clinicopathologic study of invasive micropapillary carcinoma of the breast. Oncotarget. 2017;8:42455–42465. doi:10.18632/oncotarget.16405

 PubMedGoogle Scholar

Cui Z-Q, Feng J-H, Zhao Y-J. Clinicopathological features of invasive micropapillary carcinoma of the breast. Oncol Lett. 2015;9:1163–1166. doi:10.3892/ol.2014.2806

 PubMed Web of Science ®Google Scholar

Hashmi AA, Aijaz S, Mahboob R, et al. Clinicopathologic features of invasive metaplastic and micropapillary breast carcinoma: comparison with invasive ductal carcinoma of breast. BMC Res Notes. 2018;11:1–7. doi:10.1186/s13104-018-3623-z

 PubMedGoogle Scholar

Pettinato G, Pambuccian SE, Di Prisco B, Manivel JC. Fine needle aspiration cytology of invasive micropapillary (pseudopapillary) carcinoma of the breast: report of 11 cases with clinicopathologic findings. Acta Cytol. 2002;46:1088–1094. doi:10.1159/000327112

 PubMed Web of Science ®Google Scholar

Chen H, Wu K, Wang M, Wang F, Zhang M, Zhang P. Invasive micropapillary carcinoma of the breast has a better long-term survival than invasive ductal carcinoma of the breast in spite of its aggressive clinical presentations: a comparison based on large population database and case–control analysis. Cancer Med. 2017;6:2775–2786. doi:10.1002/cam4.1227

 PubMed Web of Science ®Google Scholar

Yu JI, Choi DH, Huh SJ, et al. Differences in prognostic factors and failure patterns between invasive micropapillary carcinoma and carcinoma with micropapillary component versus invasive Ductal carcinoma of the breast: retrospective multicenter case-control study (KROG 13-06). Clin Breast Cancer. 2015;15:353–361.e2. doi:10.1016/j.clbc.2015.01.008

 PubMed Web of Science ®Google Scholar

Zekioglu O, Erhan Y, Çiris M, Bayramoglu H, Özdemir N. Invasive micropapillary carcinoma of the breast: high incidence of lymph node metastasis with extranodal extension and its immunohistochemical profile compared with invasive ductal carcinoma. Histopathology. 2004;44:18–23. doi:10.1111/j.1365-2559.2004.01757.x

 PubMed Web of Science ®Google Scholar

Chen AC, Paulino AC, Schwartz MR, et al. Population-based comparison of prognostic factors in invasive micropapillary and invasive ductal carcinoma of the breast. Br J Cancer. 2014;111:619–622. doi:10.1038/bjc.2014.301

 PubMed Web of Science ®Google Scholar

Gokce H, Durak MG, Akin MM, et al. Invasive micropapillary carcinoma of the breast: a clinicopathologic study of 103 cases of an unusual and highly aggressive variant of breast carcinoma. Breast J. 2013;19:374–381. doi:10.1111/tbj.12128

 PubMed Web of Science ®Google Scholar

Akdeniz N, Kaplan MA, Küçüköner M, et al. Rare breast cancer types: a study about characteristics, outcomes, and peculiarities. J Oncol Sci. 2020;6:164–172. doi:10.37047/jos.2020-78231

 Google Scholar

Lewis GD, Xing Y, Haque W, et al. The impact of molecular status on survival outcomes for invasive micropapillary carcinoma of the breast. Breast J. 2019;25:1171–1176. doi:10.1111/tbj.13432

 PubMed Web of Science ®Google Scholar

Ye F-G, Xia C, Ma D, Lin P-Y, Hu X, Shao Z-M. Nomogram for predicting preoperative lymph node involvement in patients with invasive micropapillary carcinoma of breast: a SEER population-based study. BMC Cancer. 2018;18. doi:10.1186/s12885-018-4982-5

 Web of Science ®Google Scholar

Paterakos M, Watkin WG, Edgerton SM, et al. Invasive micropapillary carcinoma of the breast: a prognostic study. Hum Pathol. 1999;30:1459–1463. doi:10.1016/S0046-8177(99)90168-5

 PubMed Web of Science ®Google Scholar

Hao S, Zhao Y, Peng J, et al. Invasive micropapillary carcinoma of the breast had no difference in prognosis compared with invasive ductal carcinoma: a propensity-matched analysis. Sci Rep. 2019;9:1–8. doi:10.1038/s41598-018-36362-8

 PubMed Web of Science ®Google Scholar

De La Cruz C, Moriya T, Endoh M, et al. Invasive micropapillary carcinoma of the breast: clinicopathological and immunohistochemical study. Pathol Int. 2004;54:90–96. doi:10.1111/j.1440-1827.2004.01590.x

 PubMed Web of Science ®Google Scholar

Chen AC, Paulino AC, Schwartz MR, et al. Prognostic markers for invasive micropapillary carcinoma of the breast: a population-based analysis. Clin Breast Cancer. 2013;13:133–139. doi:10.1016/j.clbc.2012.10.001

 PubMed Web of Science ®Google Scholar

Kaya C, Uçak R, Bozkurt E, et al. The impact of micropapillary component ratio on the prognosis of patients with invasive micropapillary breast carcinoma. J Investig Surg. 2020;33:31–39. doi:10.1080/08941939.2018.1474302

 PubMed Web of Science ®Google Scholar

Walsh MM, Bleiweiss IJ. Invasive micropapillary carcinoma of the breast: eighty cases of an underrecognized entity. Hum Pathol. 2001;32:583–589. doi:10.1053/hupa.2001.24988

 PubMed Web of Science ®Google Scholar

Kim J, Kim JY, Lee H-B, 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. 2020;184:527–542. doi:10.1007/s10549-020-05861-6

 PubMed Web of Science ®Google Scholar

Lee YS, Mathew J, Dogan BE, Resetkova E, Huo L, Yang WT. Imaging features of micropapillary DCIS: correlation with clinical and histopathological findings. Acad Radiol. 2011;18:797–803. doi:10.1016/j.acra.2011.01.022

 PubMed Web of Science ®Google Scholar

Guan X, Xu G, Shi A, et al. Comparison of clinicopathological characteristics and prognosis among patients with pure invasive ductal carcinoma, invasive ductal carcinoma coexisted with invasive micropapillary carcinoma, and invasive ductal carcinoma coexisted with ductal carcinoma. Medicine (Baltimore). 2020;99:e23487. doi:10.1097/MD.0000000000023487

 PubMed Web of Science ®Google Scholar

Kim M-J, Gong G, Joo HJ, Ahn S-H, Ro JY. Immunohistochemical and clinicopathologic characteristics of invasive ductal carcinoma of breast with micropapillary carcinoma component. Arch Pathol Lab Med. 2005;129:1277–1282. doi:10.5858/2005-129-1277-IACCOI

 PubMed Web of Science ®Google Scholar

Collins K, Ricci A. Micropapillary variant of mucinous breast carcinoma: a distinct subtype. Breast J. 2018;24:339–342. doi:10.1111/tbj.12935

 PubMed Web of Science ®Google Scholar

Yoon GY, Cha JH, Kim HH, Shin HJ, Chae EY, Choi WJ. Comparison of invasive micropapillary and invasive ductal carcinoma of the breast: a matched cohort study. Acta Radiol. 2019;60:1405–1413. doi:10.1177/0284185119834689

 PubMed Web of Science ®Google Scholar

Jones KN, Guimaraes LS, Reynolds CA, Ghosh K, Degnim AC, Glazebrook KN. Invasive micropapillary carcinoma of the breast: imaging features with clinical and pathologic correlation. Am J Roentgenol. 2013;200:689–695. doi:10.2214/AJR.12.8512

 PubMed Web of Science ®Google Scholar

Li D, Zhong C, Cheng YY, et al. A competing nomogram to predict survival outcomes in invasive micropapillary breast cancer. J Cancer. 2019;10:6801–6812. doi:10.7150/jca.27955

 PubMed Web of Science ®Google Scholar

Deman F, Punie K, Laenen A, et al. Assessment of stromal tumor infiltrating lymphocytes and immunohistochemical features in invasive micropapillary breast carcinoma with long-term outcomes. Breast Cancer Res Treat. 2020;184:985–998. doi:10.1007/s10549-020-05913-x

 PubMed Web of Science ®Google Scholar

Lewis GD, Xing Y, Haque W, et al. Prognosis of lymphotropic invasive micropapillary breast carcinoma analyzed by using data from the National Cancer Database. Cancer Commun. 2019;39:1–9. doi:10.1186/s40880-019-0406-4

 Web of Science ®Google Scholar

Liu Y, Huang X, Bi R, Yang W, Shao Z. Similar prognoses for invasive micropapillary breast carcinoma and pure invasive ductal carcinoma: a retrospectively matched cohort study in China. PLoS One. 2014;9. doi:10.1371/journal.pone.0106564

 Web of Science ®Google Scholar

Guo X-J, Chen L, Lang R-G, Fan Y, Fu L. Relationship between lymph node metastasis and pathologic features of invasive micropapillary carcinoma of breast. Chin J Pathol. 2006;35:8–12.

 Google Scholar

Wilson PC, Chagpar AB, Cicek AF, et al. Breast cancer histopathology is predictive of low-risk Oncotype Dx recurrence score. Breast J. 2018;24:976–980. doi:10.1111/tbj.13117

 PubMed Web of Science ®Google Scholar

Shi W-B, Yang L-J, Hu X, Zhou J, Zhang Q, Shao Z-M. Clinico-pathological features and prognosis of invasive micropapillary carcinoma compared to invasive ductal carcinoma: a population-based study from China. PLoS One. 2014;9. doi:10.1371/journal.pone.0101390

 Web of Science ®Google Scholar

Meng X, Ma H, Yin HH, et al. Nomogram predicting the risk of locoregional recurrence after mastectomy for invasive micropapillary carcinoma of the breast. Clin Breast Cancer. 2021;21(4):e368–e376. doi:10.1016/j.clbc.2020.12.003

 PubMed Web of Science ®Google Scholar

Song Y, Sun H, Wu K, et al. sLex expression in invasive micropapillary breast carcinoma is associated with poor prognosis and can be combined with MUC1/EMA as a supplementary diagnostic indicator. Cancer Biol Med. 2021;18:477–489. doi:10.20892/j.issn.2095-3941.2020.0422

 PubMed Web of Science ®Google Scholar

Kuroda H, Sakamoto G, Ohnisi K, Itoyama S. Overexpression of her2/neu, estrogen and progesterone receptors in invasive micropapillary carcinoma of the breast. Breast Cancer. 2004;11:301–305. doi:10.1007/BF02984553

 PubMedGoogle Scholar

Perron M, Wen HY, Hanna MG, Brogi E, Ross DS. HER2 immunohistochemistry in invasive micropapillary breast carcinoma: complete assessment of an incomplete pattern. Arch Pathol Lab Med. 2020. doi:10.5858/arpa.2020-0288-oa

 Web of Science ®Google Scholar

Simonetti S, Dominguez N, Elguezabal A, et al. Analysis of programmed death-ligand 1 expression, stromal tumor-infiltrating lymphocytes, and mismatch repair deficiency in invasive micropapillary carcinoma of the breast. J Immunother Precis Oncol. 2019;2:130–136. doi:10.4103/JIPO.JIPO_17_19

 Google Scholar

Wu Y, Zhang N, Yang Q. The prognosis of invasive micropapillary carcinoma compared with invasive ductal carcinoma in the breast: a meta-analysis. BMC Cancer. 2017;17:1–9. doi:10.1186/s12885-017-3855-7

 PubMed Web of Science ®Google Scholar

Ye F, Yu P, Li N, et al. Prognosis of invasive micropapillary carcinoma compared with invasive ductal carcinoma in breast: a meta-analysis of PSM studies. Breast. 2020;51:11–20. doi:10.1016/j.breast.2020.01.041

 PubMed Web of Science ®Google Scholar

Kim SH, Hur SM, Lee SK, et al. Characteristics of invasive micropapillary carcinoma of the breast: in comparison with invasive ductal carcinoma. J Breast Cancer. 2010;13:174–179. doi:10.4048/jbc.2010.13.2.174

 Web of Science ®Google Scholar

Chen H, Liang H-L, Ding A. Comparison of invasive micropapillary and triple negative invasive ductal carcinoma of the breast. Breast. 2015;24:723–731. doi:10.1016/j.breast.2015.09.001

 PubMed Web of Science ®Google Scholar

Li G, Yang S, Yao J, et al. Invasive micropapillary carcinoma of the breast had poor clinical characteristics but showed no difference in prognosis compared with invasive ductal carcinoma. World J Surg Oncol. 2016;14. doi:10.1186/s12957-016-0960-z

 Web of Science ®Google Scholar

Liu F, Yang MM, Li Z, et al. Invasive micropapillary mucinous carcinoma of the breast is associated with poor prognosis. Breast Cancer Res Treat. 2015;151:443–451. doi:10.1007/s10549-015-3413-4

 PubMed Web of Science ®Google Scholar

Kuroda H, Sakamoto G, Ohnisi K, Itoyama S. Clinical and pathologic features of invasive micropapillary carcinoma. Breast Cancer. 2004;11:169–174. doi:10.1007/BF02968297

 PubMedGoogle Scholar