Male breast cancer precursor lesions: analysis of the EORTC 10085/TBCRC/BIG/NABCG International Male Breast Cancer Program

Shusma C. Doebar, Leen Slaets, Fatima Cardoso, Sharon H. Giordano, John MS Bartlett, Konstantinos Tryfonidis, Nizet H. Dijkstra, Caroline P. Schröder, Christi J. van Asperen, Barbro Linderholm, Kim Benstead, Winan NM Dinjens, Ronald van Marion, Paul J. van Diest, John WM Martens, Carolien HM van Deurzen

Research output: Contribution to journalArticle

Abstract

In men, data regarding breast cancer carcinogenesis are limited. The aim of our study was to describe the presence of precursor lesions adjacent to invasive male breast cancer, in order to increase our understanding of carcinogenesis in these patients. Central pathology review was performed for 1328 male breast cancer patients, registered in the retrospective joint analysis of the International Male Breast Cancer Program, which included the presence and type of breast cancer precursor lesions. In a subset, invasive breast cancer was compared with the adjacent precursor lesion by immunohistochemistry (n=83) or targeted next generation sequencing (n=7). Additionally, we correlated the presence of ductal carcinoma in situ with outcome. A substantial proportion (46.2%) of patients with invasive breast cancer also had an adjacent precursor lesion, mainly ductal carcinoma in situ (97.9%). The presence of lobular carcinoma in situ and columnar cell-like lesions were very low (<1%). In the subset of invasive breast cancer cases with adjacent ductal carcinoma in situ (n=83), a complete concordance was observed between the estrogen receptor, progesterone receptor, and HER2 status of both components. Next generation sequencing on a subset of cases with invasive breast cancer and adjacent ductal carcinoma in situ (n=4) showed identical genomic aberrations, including PIK3CA, GATA3, TP53, and MAP2K4 mutations. Next generation sequencing on a subset of cases with invasive breast cancer and an adjacent columnar cell-like lesion showed genomic concordance in two out of three patients. A multivariate Cox model for survival showed a trend that the presence of ductal carcinoma in situ was associated with a better overall survival, in particular in the Luminal B HER2+ subgroup. In conclusion, ductal carcinoma in situ is the most commonly observed precursor lesion in male breast cancer and its presence seems to be associated with a better outcome, in particular in Luminal B HER2+ cases. The rate of lobular carcinoma in situ and columnar cell-like lesions adjacent to male breast cancer is very low, but our findings support the role of columnar cell-like lesions as a precursor of male breast cancer.Modern Pathology advance online publication, 13 January 2017; doi:10.1038/modpathol.2016.229.

Original languageEnglish (US)
JournalModern Pathology
DOIs
StateAccepted/In press - Jan 13 2017
Externally publishedYes

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Male Breast Neoplasms
Carcinoma, Intraductal, Noninfiltrating
Breast Neoplasms
Carcinogenesis
Pathology
Survival
Progesterone Receptors
Proportional Hazards Models
Estrogen Receptors
Publications
Immunohistochemistry
Mutation

ASJC Scopus subject areas

  • Pathology and Forensic Medicine

Cite this

Doebar, S. C., Slaets, L., Cardoso, F., Giordano, S. H., Bartlett, J. MS., Tryfonidis, K., ... van Deurzen, C. HM. (Accepted/In press). Male breast cancer precursor lesions: analysis of the EORTC 10085/TBCRC/BIG/NABCG International Male Breast Cancer Program. Modern Pathology. https://doi.org/10.1038/modpathol.2016.229

Male breast cancer precursor lesions : analysis of the EORTC 10085/TBCRC/BIG/NABCG International Male Breast Cancer Program. / Doebar, Shusma C.; Slaets, Leen; Cardoso, Fatima; Giordano, Sharon H.; Bartlett, John MS; Tryfonidis, Konstantinos; Dijkstra, Nizet H.; Schröder, Caroline P.; van Asperen, Christi J.; Linderholm, Barbro; Benstead, Kim; Dinjens, Winan NM; van Marion, Ronald; van Diest, Paul J.; Martens, John WM; van Deurzen, Carolien HM.

In: Modern Pathology, 13.01.2017.

Research output: Contribution to journalArticle

Doebar, SC, Slaets, L, Cardoso, F, Giordano, SH, Bartlett, JMS, Tryfonidis, K, Dijkstra, NH, Schröder, CP, van Asperen, CJ, Linderholm, B, Benstead, K, Dinjens, WNM, van Marion, R, van Diest, PJ, Martens, JWM & van Deurzen, CHM 2017, 'Male breast cancer precursor lesions: analysis of the EORTC 10085/TBCRC/BIG/NABCG International Male Breast Cancer Program', Modern Pathology. https://doi.org/10.1038/modpathol.2016.229
Doebar, Shusma C. ; Slaets, Leen ; Cardoso, Fatima ; Giordano, Sharon H. ; Bartlett, John MS ; Tryfonidis, Konstantinos ; Dijkstra, Nizet H. ; Schröder, Caroline P. ; van Asperen, Christi J. ; Linderholm, Barbro ; Benstead, Kim ; Dinjens, Winan NM ; van Marion, Ronald ; van Diest, Paul J. ; Martens, John WM ; van Deurzen, Carolien HM. / Male breast cancer precursor lesions : analysis of the EORTC 10085/TBCRC/BIG/NABCG International Male Breast Cancer Program. In: Modern Pathology. 2017.
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abstract = "In men, data regarding breast cancer carcinogenesis are limited. The aim of our study was to describe the presence of precursor lesions adjacent to invasive male breast cancer, in order to increase our understanding of carcinogenesis in these patients. Central pathology review was performed for 1328 male breast cancer patients, registered in the retrospective joint analysis of the International Male Breast Cancer Program, which included the presence and type of breast cancer precursor lesions. In a subset, invasive breast cancer was compared with the adjacent precursor lesion by immunohistochemistry (n=83) or targeted next generation sequencing (n=7). Additionally, we correlated the presence of ductal carcinoma in situ with outcome. A substantial proportion (46.2{\%}) of patients with invasive breast cancer also had an adjacent precursor lesion, mainly ductal carcinoma in situ (97.9{\%}). The presence of lobular carcinoma in situ and columnar cell-like lesions were very low (<1{\%}). In the subset of invasive breast cancer cases with adjacent ductal carcinoma in situ (n=83), a complete concordance was observed between the estrogen receptor, progesterone receptor, and HER2 status of both components. Next generation sequencing on a subset of cases with invasive breast cancer and adjacent ductal carcinoma in situ (n=4) showed identical genomic aberrations, including PIK3CA, GATA3, TP53, and MAP2K4 mutations. Next generation sequencing on a subset of cases with invasive breast cancer and an adjacent columnar cell-like lesion showed genomic concordance in two out of three patients. A multivariate Cox model for survival showed a trend that the presence of ductal carcinoma in situ was associated with a better overall survival, in particular in the Luminal B HER2+ subgroup. In conclusion, ductal carcinoma in situ is the most commonly observed precursor lesion in male breast cancer and its presence seems to be associated with a better outcome, in particular in Luminal B HER2+ cases. The rate of lobular carcinoma in situ and columnar cell-like lesions adjacent to male breast cancer is very low, but our findings support the role of columnar cell-like lesions as a precursor of male breast cancer.Modern Pathology advance online publication, 13 January 2017; doi:10.1038/modpathol.2016.229.",
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