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Published in: Virchows Archiv 1/2017

01-07-2017 | Original Article

Invasive lobular carcinoma with extracellular mucin production—a novel pattern of lobular carcinomas of the breast. Clinico-pathological description of eight cases

Authors: Gábor Cserni, Giuseppe Floris, Nektarios Koufopoulos, Anikó Kovács, Afroditi Nonni, Peter Regitnig, Anders Stahls, Zsuzsanna Varga

Published in: Virchows Archiv | Issue 1/2017

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Abstract

Invasive lobular carcinoma of the breast is known to produce intracellular mucin and has been recognized in single-case reports to show extracellular mucin production, as well. This latter morphology is not only rare but must also be under- or misdiagnosed. The aim was to better characterize this entity. Cases of lobular cancers demonstrating extracellular mucin formation were identified in a multi-institutional effort and their clinical and morphologic features were assessed. Immunohistochemistry was used to characterize the E-cadherin-membrane complex, neuroendocrine differentiation, and to some extent, mucin formation. All but one of the eight cases occurred in postmenopausal patients. Extracellular mucin production was present in 5 to 50% of the tumour samples and rarely also appeared in nodal and distant metastases. The tumours were completely E-cadherin negative and showed cytoplasmic p120 positivity. The majority (n = 6/8) was also completely negative for β-catenin, but two tumours displayed focal β-catenin positivity in the mucinous area. MUC1 and MUC2 expression was observed in all and 7/8 tumours, respectively; neuroendocrine differentiation was present in only one. Invasive lobular carcinoma with extracellular mucin formation is a rare morphologic variant of lobular carcinoma prone to be misdiagnosed and warranting further studies.
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Literature
1.
2.
go back to reference Fechner RE (1975) Histologic variants of infiltrating lobular carcinoma of the breast. Hum Pathol 6:373–378CrossRefPubMed Fechner RE (1975) Histologic variants of infiltrating lobular carcinoma of the breast. Hum Pathol 6:373–378CrossRefPubMed
3.
go back to reference Steinbrecher JS, Silverberg SG (1976) Signet-ring cell carcinoma of the breast. The mucinous variant of infiltrating lobular carcinoma? Cancer 37:828–840CrossRefPubMed Steinbrecher JS, Silverberg SG (1976) Signet-ring cell carcinoma of the breast. The mucinous variant of infiltrating lobular carcinoma? Cancer 37:828–840CrossRefPubMed
4.
go back to reference Fisher ER, Gregorio RM, Redmond C, Fisher B (1977) Tubulolobular invasive breast cancer: a variant of lobular invasive cancer. Hum Pathol 8:679–683CrossRefPubMed Fisher ER, Gregorio RM, Redmond C, Fisher B (1977) Tubulolobular invasive breast cancer: a variant of lobular invasive cancer. Hum Pathol 8:679–683CrossRefPubMed
5.
go back to reference Martinez V, Azzopardi JG (1979) Invasive lobular carcinoma of the breast: incidence and variants. Histopathology 3:467–488CrossRefPubMed Martinez V, Azzopardi JG (1979) Invasive lobular carcinoma of the breast: incidence and variants. Histopathology 3:467–488CrossRefPubMed
6.
go back to reference Page DL, Anderson TJ, eds (1987) Diagnostic histopathology of the breast. Churchill Livingstone, Edinburgh Page DL, Anderson TJ, eds (1987) Diagnostic histopathology of the breast. Churchill Livingstone, Edinburgh
7.
go back to reference Weidner N, Semple JP (1992) Pleomorphic variant of invasive lobular carcinoma of the breast. Hum Pathol 23:1167–1171CrossRefPubMed Weidner N, Semple JP (1992) Pleomorphic variant of invasive lobular carcinoma of the breast. Hum Pathol 23:1167–1171CrossRefPubMed
8.
go back to reference Eusebi V, Magalhaes F, Azzopardi JG (1992) Pleomorphic lobular carcinoma of the breast: an aggressive tumor showing apocrine differentiation. Hum Pathol 23:655–662CrossRefPubMed Eusebi V, Magalhaes F, Azzopardi JG (1992) Pleomorphic lobular carcinoma of the breast: an aggressive tumor showing apocrine differentiation. Hum Pathol 23:655–662CrossRefPubMed
9.
go back to reference Amendoeira I, Apostolikas N, Bellocq JP et al (2006) Quality assurance guidelines for pathology. In: Perry N, Broeders M, de Wolf C, Törnberg S, Holland R, von Karsa L (eds) European guidelines for quality assurance in breast cancer screening and diagnosis, 4th edn. European Comission, Luxemburg, pp 219–311 Amendoeira I, Apostolikas N, Bellocq JP et al (2006) Quality assurance guidelines for pathology. In: Perry N, Broeders M, de Wolf C, Törnberg S, Holland R, von Karsa L (eds) European guidelines for quality assurance in breast cancer screening and diagnosis, 4th edn. European Comission, Luxemburg, pp 219–311
10.
go back to reference Lakhani SR, Ellis IO, Schnitt SJ, Tan PH, van de Vijver MJ (eds) (2012) WHO classification of tumours of the breast. International Agency for Research on Cancer, Lyon Lakhani SR, Ellis IO, Schnitt SJ, Tan PH, van de Vijver MJ (eds) (2012) WHO classification of tumours of the breast. International Agency for Research on Cancer, Lyon
11.
go back to reference Tavassoli FA, Eusebi V (2009) Tumors of the mammary gland. Armed Forces Institute of Pathology Atlas of tumor pathology, Series 4. American Registry of Pathology, Washington, DC Tavassoli FA, Eusebi V (2009) Tumors of the mammary gland. Armed Forces Institute of Pathology Atlas of tumor pathology, Series 4. American Registry of Pathology, Washington, DC
12.
go back to reference Cserni G (1999) Reproducibility of a diagnosis of invasive lobular carcinoma. J Surg Oncol 70:217–221CrossRefPubMed Cserni G (1999) Reproducibility of a diagnosis of invasive lobular carcinoma. J Surg Oncol 70:217–221CrossRefPubMed
13.
go back to reference Acs G, Lawton TJ, Rebbeck TR, LiVolsi VA, Zhang PJ (2001) Differential expression of E-cadherin in lobular and ductal neoplasms of the breast and its biologic and diagnostic implications. Am J Clin Pathol 115:85–98CrossRefPubMed Acs G, Lawton TJ, Rebbeck TR, LiVolsi VA, Zhang PJ (2001) Differential expression of E-cadherin in lobular and ductal neoplasms of the breast and its biologic and diagnostic implications. Am J Clin Pathol 115:85–98CrossRefPubMed
14.
go back to reference Kovács A, Dhillon J, Walker RA (2003) Expression of P-cadherin, but not E-cadherin or N-cadherin, relates to pathological and functional differentiation of breast carcinomas. Mol Pathol 56:318–322CrossRefPubMedPubMedCentral Kovács A, Dhillon J, Walker RA (2003) Expression of P-cadherin, but not E-cadherin or N-cadherin, relates to pathological and functional differentiation of breast carcinomas. Mol Pathol 56:318–322CrossRefPubMedPubMedCentral
15.
go back to reference Rakha EA, Abd El Rehim D, Pinder SE, Lewis SA, Ellis IO (2005) E-cadherin expression in invasive non-lobular carcinoma of the breast and its prognostic significance. Histopathology 46:685–693CrossRefPubMed Rakha EA, Abd El Rehim D, Pinder SE, Lewis SA, Ellis IO (2005) E-cadherin expression in invasive non-lobular carcinoma of the breast and its prognostic significance. Histopathology 46:685–693CrossRefPubMed
16.
go back to reference Da Silva L, Parry S, Reid L, Keith P, Waddell N, Kossai M, Clarke C, Lakhani SR, Simpson PT (2008) Aberrant expression of E-cadherin in lobular carcinomas of the breast. Am J Surg Pathol 32:773–783CrossRefPubMed Da Silva L, Parry S, Reid L, Keith P, Waddell N, Kossai M, Clarke C, Lakhani SR, Simpson PT (2008) Aberrant expression of E-cadherin in lobular carcinomas of the breast. Am J Surg Pathol 32:773–783CrossRefPubMed
17.
go back to reference Rakha EA, Teoh TK, Lee AH, Nolan CC, Ellis IO, Green AR (2013) Further evidence that E-cadherin is not a tumour suppressor gene in invasive ductal carcinoma of the breast: an immunohistochemical study. Histopathology 62:695–701CrossRefPubMed Rakha EA, Teoh TK, Lee AH, Nolan CC, Ellis IO, Green AR (2013) Further evidence that E-cadherin is not a tumour suppressor gene in invasive ductal carcinoma of the breast: an immunohistochemical study. Histopathology 62:695–701CrossRefPubMed
18.
go back to reference Canas-Marques R, Schnitt SJ (2016) E-cadherin immunohistochemistry in breast pathology: uses and pitfalls. Histopathology 68:57–69CrossRefPubMed Canas-Marques R, Schnitt SJ (2016) E-cadherin immunohistochemistry in breast pathology: uses and pitfalls. Histopathology 68:57–69CrossRefPubMed
19.
go back to reference Rosa M, Mohammadi A, Masood S (2009) Lobular carcinoma of the breast with extracellular mucin: new variant of mucin-producing carcinomas? Pathol Int 59:405–409CrossRefPubMed Rosa M, Mohammadi A, Masood S (2009) Lobular carcinoma of the breast with extracellular mucin: new variant of mucin-producing carcinomas? Pathol Int 59:405–409CrossRefPubMed
20.
go back to reference Yu J, Bhargava R, Dabbs DJ (2010) Invasive lobular carcinoma with extracellular mucin production and HER-2 overexpression: a case report and further case studies. Diagn Pathol 5:36CrossRefPubMedPubMedCentral Yu J, Bhargava R, Dabbs DJ (2010) Invasive lobular carcinoma with extracellular mucin production and HER-2 overexpression: a case report and further case studies. Diagn Pathol 5:36CrossRefPubMedPubMedCentral
21.
go back to reference Haltas H, Bayrak R, Yenidunya S, Kosehan D, Sen M, Akin K (2012) Invasive lobular carcinoma with extracellular mucin as a distinct variant of lobular carcinoma: a case report. Diagn Pathol 7:91CrossRefPubMedPubMedCentral Haltas H, Bayrak R, Yenidunya S, Kosehan D, Sen M, Akin K (2012) Invasive lobular carcinoma with extracellular mucin as a distinct variant of lobular carcinoma: a case report. Diagn Pathol 7:91CrossRefPubMedPubMedCentral
22.
go back to reference Bari VB, Bholay SU, Sane KC (2015) Invasive lobular carcinoma of the breast with extracellular mucin. A new rare variant J Clin Diagn Res 9:ED05–ED06PubMed Bari VB, Bholay SU, Sane KC (2015) Invasive lobular carcinoma of the breast with extracellular mucin. A new rare variant J Clin Diagn Res 9:ED05–ED06PubMed
23.
go back to reference Gomez Macias GS, Pérez Saucedo JE, Cardona Huerta S, Garza Montemayor M, Villarreal Garza C, Garcia Hernandez I (2016) Invasive lobular carcinoma of the breast with extracellular mucin: a case report. Int J Surg Case Rep 25:33–36CrossRefPubMedPubMedCentral Gomez Macias GS, Pérez Saucedo JE, Cardona Huerta S, Garza Montemayor M, Villarreal Garza C, Garcia Hernandez I (2016) Invasive lobular carcinoma of the breast with extracellular mucin: a case report. Int J Surg Case Rep 25:33–36CrossRefPubMedPubMedCentral
24.
go back to reference Hammond ME, Hayes DF, Dowsett M et al (2010) American Society of ClinicalOncology/College of American Pathologists guideline recommendations for immunohistochemical testing of estrogen and progesterone receptors in breast cancer. Arch Pathol Lab Med 134:e48–e72PubMed Hammond ME, Hayes DF, Dowsett M et al (2010) American Society of ClinicalOncology/College of American Pathologists guideline recommendations for immunohistochemical testing of estrogen and progesterone receptors in breast cancer. Arch Pathol Lab Med 134:e48–e72PubMed
25.
go back to reference Wolff AC, Hammond ME, Hicks DG et al (2014) Recommendations for human epidermal growth factor receptor 2 testing in breast cancer: American Society of Clinical Oncology/College of American Pathologists Clinical Practice Guideline Update. Arch Pathol Lab Med 138:241–256CrossRefPubMed Wolff AC, Hammond ME, Hicks DG et al (2014) Recommendations for human epidermal growth factor receptor 2 testing in breast cancer: American Society of Clinical Oncology/College of American Pathologists Clinical Practice Guideline Update. Arch Pathol Lab Med 138:241–256CrossRefPubMed
26.
go back to reference Tot T (2007) Clinical relevance of the distribution of the lesions in 500 consecutive breast cancer cases documented in large-format histologic sections. Cancer 110:2551–2560CrossRefPubMed Tot T (2007) Clinical relevance of the distribution of the lesions in 500 consecutive breast cancer cases documented in large-format histologic sections. Cancer 110:2551–2560CrossRefPubMed
27.
go back to reference Bratthauer GL, Moinfar F, Stamatakos MD et al (2002) Combined E-cadherin and high molecular weight cytokeratin immunoprofile differentiates lobular, ductal, and hybrid mammary intraepithelial neoplasias. Hum Pathol 33:620–627CrossRefPubMed Bratthauer GL, Moinfar F, Stamatakos MD et al (2002) Combined E-cadherin and high molecular weight cytokeratin immunoprofile differentiates lobular, ductal, and hybrid mammary intraepithelial neoplasias. Hum Pathol 33:620–627CrossRefPubMed
29.
go back to reference Eusebi V, Azzopardi JG (1980) Lobular endocrine neoplasia in fibroadenoma of the breast. Histopathology 4:413–428CrossRefPubMed Eusebi V, Azzopardi JG (1980) Lobular endocrine neoplasia in fibroadenoma of the breast. Histopathology 4:413–428CrossRefPubMed
30.
go back to reference Sapino A, Righi L, Cassoni P, Papotti M, Pietribiasi F, Bussolati G (2000) Expression of the neuroendocrine phenotype in carcinomas of the breast. Semin Diagn Pathol 17:127–137PubMed Sapino A, Righi L, Cassoni P, Papotti M, Pietribiasi F, Bussolati G (2000) Expression of the neuroendocrine phenotype in carcinomas of the breast. Semin Diagn Pathol 17:127–137PubMed
31.
go back to reference Capella C, Eusebi V, Mann B, Azzopardi JG (1980) Endocrine differentiation in mucoid carcinoma of the breast. Histopathology 4:613–630CrossRefPubMed Capella C, Eusebi V, Mann B, Azzopardi JG (1980) Endocrine differentiation in mucoid carcinoma of the breast. Histopathology 4:613–630CrossRefPubMed
32.
go back to reference Tan PH, Schnitt SJ, van de Vijver MJ, Ellis IO, Lakhani SR (2015) Papillary and neuroendocrine breast lesions: the WHO stance. Histopathology 66:761–770CrossRefPubMed Tan PH, Schnitt SJ, van de Vijver MJ, Ellis IO, Lakhani SR (2015) Papillary and neuroendocrine breast lesions: the WHO stance. Histopathology 66:761–770CrossRefPubMed
33.
go back to reference Wargotz ES, Norris HJ (1989) Metaplastic carcinomas of the breast. I. Matrix-producing carcinoma. Hum Pathol 20:628–635CrossRefPubMed Wargotz ES, Norris HJ (1989) Metaplastic carcinomas of the breast. I. Matrix-producing carcinoma. Hum Pathol 20:628–635CrossRefPubMed
34.
go back to reference Asioli S, Marucci G, Ficarra G, Stephens M, Foschini MP, Ellis IO, Eusebi V (2006) Polymorphous adenocarcinoma of the breast. Report of three cases. Virchows Arch 448:29–34CrossRefPubMed Asioli S, Marucci G, Ficarra G, Stephens M, Foschini MP, Ellis IO, Eusebi V (2006) Polymorphous adenocarcinoma of the breast. Report of three cases. Virchows Arch 448:29–34CrossRefPubMed
35.
go back to reference Petersson F, Putti TC (2010) Multifocal matrix-producing mammary carcinoma mimicking lobular carcinoma on core biopsy - a case with long survival reported. Pathol Res Pract 206:527–531CrossRefPubMed Petersson F, Putti TC (2010) Multifocal matrix-producing mammary carcinoma mimicking lobular carcinoma on core biopsy - a case with long survival reported. Pathol Res Pract 206:527–531CrossRefPubMed
36.
go back to reference Nicol KK, Iskandar SS (2000) Lobular carcinoma of the breast metastatic to the oral cavity mimicking polymorphous low-grade adenocarcinoma of the minor salivary glands. Arch Pathol Lab Med 124:157–159PubMed Nicol KK, Iskandar SS (2000) Lobular carcinoma of the breast metastatic to the oral cavity mimicking polymorphous low-grade adenocarcinoma of the minor salivary glands. Arch Pathol Lab Med 124:157–159PubMed
37.
go back to reference Jambal P, Badtke MM, Harrell JC, Borges VF, Post MD, Sollender GE, Spillman MA, Horwitz KB, Jacobsen BM (2013) Estrogen switches pure mucinous breast cancer to invasive lobular carcinoma with mucinous features. Breast Cancer Res Treat 137:431–448CrossRefPubMed Jambal P, Badtke MM, Harrell JC, Borges VF, Post MD, Sollender GE, Spillman MA, Horwitz KB, Jacobsen BM (2013) Estrogen switches pure mucinous breast cancer to invasive lobular carcinoma with mucinous features. Breast Cancer Res Treat 137:431–448CrossRefPubMed
Metadata
Title
Invasive lobular carcinoma with extracellular mucin production—a novel pattern of lobular carcinomas of the breast. Clinico-pathological description of eight cases
Authors
Gábor Cserni
Giuseppe Floris
Nektarios Koufopoulos
Anikó Kovács
Afroditi Nonni
Peter Regitnig
Anders Stahls
Zsuzsanna Varga
Publication date
01-07-2017
Publisher
Springer Berlin Heidelberg
Published in
Virchows Archiv / Issue 1/2017
Print ISSN: 0945-6317
Electronic ISSN: 1432-2307
DOI
https://doi.org/10.1007/s00428-017-2147-6

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