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Breast Cytology

  • Gabriela Oprea-Ilies
  • Momin T. Siddiqui
Chapter
Part of the Atlas of Anatomic Pathology book series (AAP)

Abstract

Fine needle aspiration (FNA) of breast lesions represents a rapid, minimally invasive procedure to diagnose both benign and malignant conditions. In experienced hands, with the aid of immediate evaluation, this procedure reaches above 97% sensitivity and specificity in diagnosing the wide spectrum of benign and malignant breast lesions. Diagnosis by aspiration is rendered in the setting of the triple test: clinical, imaging, and cytologic data. Reporting of results should follow the guidelines issued by the NCI in 1996. The International Academy of Cytology (IAC) recently took the initiative to revise and standardize reporting of breast FNA.

The FNA specimen is not only used for making the diagnosis. Immediate evaluation improves the potential of making the correct diagnosis and determines optimum sample management by indicating the need for additional tissue and the ancillary tests to be undertaken for an accurate diagnosis, including microbiology for an inflammatory specimen, flow cytometry for a predominantly lymphoid specimen, and breast cancer markers to be performed on the formalin-fixed, paraffin-embedded specimen in cases of carcinoma. In the era of molecular testing and personalized medicine, the tissue obtained by FNA as a fresh specimen or cell block doubtless will be used for additional molecular studies.

Keywords

Fine needle aspirate (FNA) Fibroadenoma Fibrocystic disease Fat necrosis Lactational changes Granular cell tumor Lipoma Breast granuloma Breast carcinoma Lobular carcinoma Ductal carcinoma Metaplastic carcinoma Apocrine carcinoma Papillary lesion Papillary carcinoma Mucinous carcinoma Tubular carcinoma Hodgkin lymphoma Small-cell carcinoma Adenoid cystic carcinoma of breast Gynecomastia 

References

  1. 1.
    Dupont WD, Page DL. Risk factors for breast cancer in women with proliferative breast disease. N Engl J Med. 1985;312:146–51.PubMedCrossRefGoogle Scholar
  2. 2.
    London SJ, Connolly JL, Schnitt SJ, Colditz GA. A prospective study of benign breast disease and the risk of breast cancer. JAMA. 1992;267:941–4.PubMedCrossRefGoogle Scholar
  3. 3.
    Siegel R, Ward E, Brawley O, Jemal A. Cancer statistics, 2011: the impact of eliminating socioeconomic and racial disparities on premature cancer deaths. CA Cancer J Clin. 2011;61:212–36.PubMedCrossRefGoogle Scholar
  4. 4.
    Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011;61:69–90.PubMedCrossRefPubMedCentralGoogle Scholar
  5. 5.
    Kohler BA, Sherman RL, Howlader N, Jemal A, Ryerson AB, Henry KA, et al. Annual report to the nation on the status of cancer, 1975-2011, featuring incidence of breast cancer subtypes by race/ethnicity, poverty, and state. J Natl Cancer Inst. 2015;107:djv048.  https://doi.org/10.1093/jnci/djv048.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Mitra S, Dey P. Fine-needle aspiration and core biopsy in the diagnosis of breast lesions: a comparison and review of the literature. Cytojournal. 2016;13:18.PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Stewart FW. The diagnosis of tumors by aspiration. Am J Pathol. 1933;9:801–12.PubMedPubMedCentralGoogle Scholar
  8. 8.
    Silverberg SG, DeLellis RA, Frable WJ, LiVolsi VA, Wick MR, editors. Silverberg’s principles and practice of surgical pathology and cytopathology. 4th ed. New York: Churchill Livingstone Elsevier; 2006. p. 22.Google Scholar
  9. 9.
    Franzen S, Zajicek J. Aspiration biopsy in diagnosis of palpable lesions of the breast. Critical review of 3479 consecutive biopsies. Acta Radiol Ther. 1968;7:241–62.CrossRefGoogle Scholar
  10. 10.
    Fassina A, Cappellesso R, Simonato F, Lanza C, Marzari A, Fassan M. Fine needle aspiration of non-small cell lung cancer: current state and future perspective. Cytopathology. 2012;23:213–9.PubMedCrossRefGoogle Scholar
  11. 11.
    National Cancer Institute. The uniform approach to breast fine-needle aspiration biopsy. National Cancer Institute Fine-Needle Aspiration of Breast Workshop Subcommittees. Diagn Cytopathol. 1997;16:295–311.CrossRefGoogle Scholar
  12. 12.
    Layfield LJ, Mooney EE, Glasgow B, Hirschowitz S, Coogan A. What constitutes an adequate smear in fine-needle aspiration cytology of the breast? Cancer. 1997;81:16–21.PubMedCrossRefGoogle Scholar
  13. 13.
    Field AS, Schmitt F, Vielh P. IAC standardized reporting of breast fine-needle aspiration biopsy cytology. Acta Cytol. 2017;61:3–6.PubMedCrossRefGoogle Scholar
  14. 14.
    Sidawy MK, Stoler MH, Frable WF, Frost AR, Masood S, Miller TR, et al. Interobserver variability in the classification of proliferative breast lesions by fine-needle aspiration: results of the Papanicolaou Society of Cytopathology Study. Diagn Cytopathol. 1998;18:150–65.PubMedCrossRefGoogle Scholar
  15. 15.
    Amin AL, Purdy AC, Mattingly JD, Kong AL, Termuhlen PM. Benign breast disease. Surg Clin North Am. 2013;93:299–308.PubMedCrossRefGoogle Scholar
  16. 16.
    Vidal M, Peg V, Galván P, Tres A, Cortés J, Ramón y Cajal S, et al. Gene expression-based classifications of fibroadenomas and phyllodes tumours of the breast. Molec Oncol. 2015;9:1081–90.CrossRefGoogle Scholar
  17. 17.
    Jacklin RK, Ridgway PF, Ziprin P, Healy V, Hadjiminas D, Darzi A. Optimising preoperative diagnosis in phyllodes tumor of the breast. J Clin Pathol. 2006;59:454–9.PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Liberman L, Bonaccio E, Hamele-Bena D, Abramson AF, Cohen MA, Dershaw DD. Benign and malignant phyllodes tumors: mammographic and sonographic findings. Radiology. 1996;198:121–4.PubMedCrossRefGoogle Scholar
  19. 19.
    Wurdinger S, Herzog AB, Fischer DR, Marx C, Raabe G, Schneider A, Kaiser WA. Differentiation of phyllodes breast tumors from fibroadenomas on MRI. AJR Am J Roentgenol. 2005;185:1317–21.PubMedCrossRefGoogle Scholar
  20. 20.
    Chhieng DC, Cangiarella JF, Waisman J, Fernandez G, Cohen J-M. Fine-needle aspiration cytology of spindle cell lesions of the breast. Cancer Cytol. 1999;87:359–71.CrossRefGoogle Scholar
  21. 21.
    Jayaram G, Sthaneshwar P. Fine-needle aspiration cytology of phyllodes tumors. Diagn Cytopathol. 2002;26:222–7.PubMedCrossRefGoogle Scholar
  22. 22.
    El Hag IA, Aodah A, Kollur SM, Attallah A, Mohamed AA, Al-Hussaini H. Cytological clues in the distinction between phyllodes tumor and fibroadenoma. Cancer Cytopathol. 2010;118:33–40.PubMedCrossRefGoogle Scholar
  23. 23.
    Ridgway PF, Jacklin RK, Ziprin P, Harbin L, Peck DH, Darzi AW, et al. Perioperative diagnosis of cytosarcoma phyllodes of the breast may be enhanced by MIB-1 index. J Surg Res. 2004;122:83–8.PubMedCrossRefGoogle Scholar
  24. 24.
    Bandyopadhyay R, Nag D, Mondal SK, Mukhopadhyay S, Roy S, Sinha SK. Distinction of phyllodes tumor from fibroadenoma: Cytologists' perspective. J Cytol. 2010;27:59–62.PubMedPubMedCentralCrossRefGoogle Scholar
  25. 25.
    Sabate JM, Clotet M, Torrubia S, Gomez A, Guerrero R, de las Heras P, Lerma E. Radiologic evaluation of breast disorders related to pregnancy and lactation. Radiographics. 2007;27(Suppl 1):S101–24.PubMedCrossRefGoogle Scholar
  26. 26.
    Kanal E, Borgstede JP, Barkovich AJ, Bell C, Bradley WG, Felmlee JP, et al. American College of Radiology white paper on MR safety. AJR Am J Roentgenol. 2002;178:1335–47.PubMedCrossRefGoogle Scholar
  27. 27.
    Webb JA, Thomsen HS, Morcos SK, Members of Contrast Media Safety Committee of European Society of Urogenital Radiology (ESUR). The use of iodinated and gadolinium contrast media during pregnancy and lactation. Eur Radiol. 2005;15:1234–40.PubMedCrossRefGoogle Scholar
  28. 28.
    Szabo J, Garcia D, Ciomek N, Margolies L. Spuriously aggressive features of a lactating adenoma prompting repeated biopsies. Radiol Case Rep. 2017;12:215–8.PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Saglam A, Can B. Coexistence of lactating adenoma and invasive ductal adenocarcinoma of the breast in a pregnant woman. J Clin Pathol. 2005;58:87–9.PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Peeters WJ, Nanhekhan L, Van Ongeval C, Fabré G, Vandevoort M. Fat necrosis in deep inferior epigastric perforator flaps: an ultrasound-based review of 202 cases. Plast Reconstr Surg. 2009;124:1754–8.PubMedCrossRefPubMedCentralGoogle Scholar
  31. 31.
    Lövey K, Fodor J, Major T, Szabó E, Orosz Z, Sulyok Z, et al. Fat necrosis after partial-breast irradiation with brachytherapy or electron irradiation versus standard whole-breast radiotherapy—4-year results of a randomized trial. Int J Radiat Oncol Biol Phys. 2007;69:724–31.PubMedCrossRefPubMedCentralGoogle Scholar
  32. 32.
    Trombetta M, Valakh V, Julian TB, Werts ED, Parda D. Mammary fat necrosis following radiotherapy in the conservative management of localized breast cancer: does it matter? Radiother Oncol. 2010;97:92–4.PubMedCrossRefPubMedCentralGoogle Scholar
  33. 33.
    Turner MJ, Amerasekera S, Cantwell R, Purushotham AD. An unusual case of fat necrosis of the breast. J BUON. 2002;7:281–2.PubMedPubMedCentralGoogle Scholar
  34. 34.
    Das AK. Low-molecular-weight heparin-associated fat necrosis of the breast. Age Ageing. 2005;34:193–4.PubMedCrossRefPubMedCentralGoogle Scholar
  35. 35.
    Salhab M, Al Sarakbi W, Mokbel K. Skin and fat necrosis of the breast following methylene blue dye injection for sentinel node biopsy in a patient with breast cancer. Int Semin Surg Oncol. 2005;2:26.PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    Taboada JL, Stephens TW, Krishnamurthy S, Brandt KR, Whitman GJ. The many faces of fat necrosis in the breast. AJR Am J Roentgenol. 2009;192:815–25.PubMedCrossRefPubMedCentralGoogle Scholar
  37. 37.
    Kerridge WD, Kryvenko ON, Thompson A, Shah BA. Fat necrosis of the breast: a pictorial review of the mammographic, ultrasound, CT, and MRI findings with histopathologic correlation. Radiol Res Pract. 2015;2015:613139.PubMedPubMedCentralGoogle Scholar
  38. 38.
    McClatchie S, Bremner AD. Unusual subcutaneous swellings in African patients. E Afr Med J. 1969;46:625–33.Google Scholar
  39. 39.
    Rosai J. The nature of myospherulosis of the upper respiratory tract. Am J Clin Pathol. 1978;69:475–81.PubMedCrossRefPubMedCentralGoogle Scholar
  40. 40.
    Godbersen GS, Kleeberg J, Lüttges J, Werner JA [Spherulocytosis (myospherulosis) of the paranasal sinuses]. HNO. 1995;43:552–5. German.Google Scholar
  41. 41.
    Gao Y, Slanetz PJ, Eisenberg RL. Echogenic breast masses at US: to biopsy or not to biopsy? Radiographics. 2013;33:419–34.PubMedCrossRefPubMedCentralGoogle Scholar
  42. 42.
    Lanng C, Eriksen BØ, Hoffmann J. Lipoma of the breast: a diagnostic dilemma. Breast. 2004;13:408–11.PubMedCrossRefPubMedCentralGoogle Scholar
  43. 43.
    Bartuma H, Panagopoulos I, Collin A, Trombetta D, Domanski HA, Mandahl N, Mertens F. Expression levels of HMGA2 in adipocytic tumors correlate with morphologic and cytogenetic subgroups. Mol Cancer. 2009;8:36.PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    Pant R, Poh AC, Hwang SG. An unusual case of an intramuscular lipoma of the pectoralis major muscle simulating a malignant breast mass. Ann Acad Med Singapore. 2005;34:275–6.PubMedPubMedCentralGoogle Scholar
  45. 45.
    Zuska JJ, Crile G Jr, Ayres WW. Fistulas of lactiferous ducts. Am J Surg. 1951;81:312–7.PubMedCrossRefPubMedCentralGoogle Scholar
  46. 46.
    Silverman JF, Lannin DR, Unverferth M, Norris HT. Fine needle aspiration cytology of subareolar abscess of the breast. Spectrum of cytomorphologic findings and potential diagnostic pitfalls. Acta Cytol. 1986;30:413–9.PubMedPubMedCentralGoogle Scholar
  47. 47.
    Koss LG, Melamed MR, editors. Koss’ diagnostic cytology and its histopathologic bases. Philadelphia: Lippincott Williams & Wilkins; 2005.Google Scholar
  48. 48.
    Abrikossoff A. Uber Myome, ausgehend von der quergestreiften wilkuerlichen muskulatur. Virchows Arch Pathol Anat. 1926;260:215–33.CrossRefGoogle Scholar
  49. 49.
    El Aouni N, Laurent I, Terrier P, Mansouri D, Suciu V, Delaloge S, Vielh P. Granular cell tumor of the breast. Diagn Cytopathol. 2007;35:725–7.PubMedCrossRefPubMedCentralGoogle Scholar
  50. 50.
    Kontaridis MI, Swanson KD, David FS, Barford D, Neel BG. PTPN11 (Shp2) mutations in LEOPARD syndrome have dominant negative, not activating, effects. J Biol Chem. 2006;281:6785–92.PubMedCrossRefGoogle Scholar
  51. 51.
    Dolman PJ, Rootman J, Dolman CL. Infiltrating orbital granular cell tumor: a case report and literature review. Br J Ophthalmol. 1987;71:47–53.PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Al-Ahmadie H, Hasselgren PO, Yassin R, Mutema G. Colocalized granular cell tumor and infiltrating ductal carcinoma of the breast. Arch Pathol Lab Med. 2002;126:731–3.PubMedGoogle Scholar
  53. 53.
    Katz U, Molad Y, Ablin J, Ben-David D, Paran D, Gutman M, Langevitz P. Chronic idiopathic granulomatous mastitis. Ann N Y Acad Sci. 2007;1108:603–8.PubMedCrossRefGoogle Scholar
  54. 54.
    Ang LM, Brown H. Corynebacterium accolens isolated from breast abscess: possible association with granulomatous mastitis. J Clin Microbiol. 2007;45:1666–8.PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Scaranelo AM, Bukhanov K, Crystal P, Mulligan AM, O’Malley FP. Granular cell tumour of the breast: MRI findings and review of the literature. Br J Radiol. 2007;80:970–4.PubMedCrossRefPubMedCentralGoogle Scholar
  56. 56.
    Tse GM, Poon CS, Law BK, Pang LM, Chu WC, Ma TK. Fine needle aspiration cytology of granulomatous mastitis. J Clin Pathol. 2003;56:519–21.PubMedPubMedCentralCrossRefGoogle Scholar
  57. 57.
    Kumarasinghe MP. Cytology of granulomatous mastitis. Acta Cytol. 1997;41:727–30.PubMedCrossRefPubMedCentralGoogle Scholar
  58. 58.
    Shin HJ, Sneige N. Is a diagnosis of infiltrating versus in situ ductal carcinoma of the breast possible in fine-needle aspiration specimens? Cancer. 1998;84:186–91.PubMedCrossRefPubMedCentralGoogle Scholar
  59. 59.
    Cai N, Koizumi J, Vazquez M. Mammary carcinoma with osteoclast-like giant cells: a study of four cases and a review of literature. Diagn Cytopathol. 2005;33:246–51.PubMedCrossRefPubMedCentralGoogle Scholar
  60. 60.
    Shishido-Hara Y, Kurata A, Fujiwara M, Itoh H, Imoto S, Kamma H. Two cases of breast carcinoma with osteoclastic giant cells: are the osteoclastic giant cells pro-tumoural differentiation of macrophages? Diagn Pathol. 2010;5:55.PubMedPubMedCentralCrossRefGoogle Scholar
  61. 61.
    Arpino G, Bardou VJ, Clark GM, Elledge RM. Infiltrating lobular carcinoma of the breast: tumor characteristics and clinical outcome. Breast Cancer Res. 2004;6:R149.PubMedPubMedCentralCrossRefGoogle Scholar
  62. 62.
    Eheman CR, Shaw KM, Ryerson AB, Miller JW, Ajani UA, White MC. The changing incidence of in situ and invasive ductal and lobular breast carcinomas: United States, 1999-2004. Cancer Epidemiol Biomark Prev. 2009;18:1763–9.CrossRefGoogle Scholar
  63. 63.
    Lopez JK, Bassett LW. Invasive lobular carcinoma of the breast: spectrum of mammographic, US, and MR imaging findings. Radiographics. 2009;29:165–76.PubMedCrossRefGoogle Scholar
  64. 64.
    Jayaram G, Swain M, Chew MT, Yip CH. Cytologic appearances in invasive lobular carcinoma of the breast. A study of 21 cases. Acta Cytol. 2000;44:169–74.PubMedCrossRefGoogle Scholar
  65. 65.
    Tsuchiya S. Cytological characteristics of invasive lobular carcinoma of the human breast. Med Mol Morphol. 2008;41:121–5.PubMedCrossRefGoogle Scholar
  66. 66.
    Menet E, Becette V, Briffod M. Cytologic diagnosis of lobular carcinoma of the breast: experience with 555 patients in the Rene Huguenin Cancer Center. Cancer. 2008;114:111–7.PubMedCrossRefGoogle Scholar
  67. 67.
    Da Silva L, Parry S, Reid L, Keith P, Waddell N, Kossai M, et al. Aberrant expression of E-cadherin in lobular carcinomas of the breast. Am J Surg Pathol. 2008;32:773–83.PubMedCrossRefGoogle Scholar
  68. 68.
    Choi YJ, Pinto MM, Hao L, Riba AK. Interobserver variability and aberrant E-cadherin immunostaining of lobular neoplasia and infiltrating lobular carcinoma. Mod Pathol. 2008;21:1224–37.PubMedCrossRefGoogle Scholar
  69. 69.
    Yu J, Dabbs DJ, Shuai Y, Niemeier LA, Bhargava R. Classical-type invasive lobular carcinoma with HER2 overexpression: clinical, histologic, and hormone receptor characteristics. Am J Clin Pathol. 2011;136:88–97.PubMedCrossRefGoogle Scholar
  70. 70.
    Iorfida M, Maiorano E, Orvieto E, Maisonneuve P, Bottiglieri L, Rotmensz N, et al. Invasive lobular breast cancer: subtypes and outcome. Breast Cancer Res Treat. 2012;133:713–23.PubMedCrossRefGoogle Scholar
  71. 71.
    Weigelt B, Geyer FC, Natrajan R, Lopez-Garcia MA, Ahmad AS, Savage K, et al. The molecular underpinning of lobular histological growth pattern: a genome-wide transcriptomic analysis of invasive lobular carcinomas and grade- and molecular subtype-matched invasive ductal carcinomas of no special type. J Pathol. 2010;220:45–57.PubMedCrossRefGoogle Scholar
  72. 72.
    Sircoulomb F, Nicolas N, Ferrari A, Finetti P, Bekhouche I, Rousselet E, et al. ZNF703 gene amplification at 8p12 specifies luminal B breast cancer. EMBO Mol Med. 2011;3(3):153–66.PubMedPubMedCentralCrossRefGoogle Scholar
  73. 73.
    Simpson PT, Reis-Filho JS, Lambros MB, Jones C, Steele D, Mackay A, et al. Molecular profiling pleomorphic lobular carcinomas of the breast: evidence for a common molecular genetic pathway with classic lobular carcinomas. J Pathol. 2008;215:231–44.PubMedCrossRefGoogle Scholar
  74. 74.
    Metzger Filho O, Giobbie-Hurder A, Mallon E, Gusterson B, Viale G, Winer EP, et al. Relative effectiveness of letrozole compared with tamoxifen for patients with lobular carcinoma in the BIG 1-98 trial. J Clin Oncol. 2015;33:2772–9.PubMedPubMedCentralCrossRefGoogle Scholar
  75. 75.
    Middleton LP, Palacios DM, Bryant BR, Krebs P, Otis CN, Merino MJ. Pleomorphic lobular carcinoma: morphology, immunohistochemistry, and molecular analysis. Am J Surg Pathol. 2000;24:1650–6.PubMedCrossRefGoogle Scholar
  76. 76.
    Auger M, Huttner I. Fine-needle aspiration cytology of pleomorphic lobular carcinoma of the breast. Comparison with the classic type. Cancer. 1997;81:29–32.PubMedCrossRefGoogle Scholar
  77. 77.
    Monaco SE, Dabbs DJ, Kanbour-Shakir A. Pleomorphic lobular carcinoma in pleural fluid: diagnostic pitfall for atypical mesothelial cells. Diagn Cytopathol. 2008;36:657–61.PubMedCrossRefGoogle Scholar
  78. 78.
    Marchiò C, Sapino A, Arisio R, Bussolati G. A new vision of tubular and tubulo-lobular carcinomas of the breast, as revealed by 3-D modelling. Histopathology. 2006;48:556–62.PubMedCrossRefGoogle Scholar
  79. 79.
    Green I, McCormick B, Cranor M, Rosen PP. A comparative study of pure tubular carcinoma of the breast. Am J Surg Pathol. 1997;21:653–7.PubMedCrossRefGoogle Scholar
  80. 80.
    Liu GF, Yang Q, Haffty BG, Moran MS. Clinical-pathologic features and long-term outcomes of tubular carcinoma of the breast compared with invasive ductal carcinoma treated with breast conservation therapy. Int J Radiat Oncol Biol Phys. 2009;75:1304–8.PubMedCrossRefGoogle Scholar
  81. 81.
    Sheppard DG, Whitman GJ, Fornage BD, Stelling CB, Huynh PT, Sahin AA. Tubular carcinoma of the breast. Mammographic and sonographic features. AJR Am J Roentgenol. 2000;174:253–7.PubMedCrossRefPubMedCentralGoogle Scholar
  82. 82.
    Cangiarella J, Waisman J, Shapiro RL, Simsir A. Cytologic features of tubular adenocarcinoma of the breast by aspiration biopsy. Diagn Cytopathol. 2001;25(5):311.PubMedCrossRefGoogle Scholar
  83. 83.
    Dei Tos AP, Della Giustina D, De Martin V, Della Libera D, Bittesini L. Aspiration biopsy cytology of tubular carcinoma of the breast. Diagn Cytopathol. 1994;11:146–50.PubMedCrossRefGoogle Scholar
  84. 84.
    Waldman FM, Hwang ES, Etzell J, Eng C, DeVries S, Bennington J, Thor A. Genomic alterations in tubular breast carcinomas. Hum Pathol. 2001;32:222–6.PubMedCrossRefGoogle Scholar
  85. 85.
    Gupta RK, Dowle CS. Fine needle aspiration cytology of tubular carcinoma of the breast. Acta Cytol. 1997;41:1139–43.PubMedCrossRefGoogle Scholar
  86. 86.
    Dahlstrom JE, Tait N, Cranney BG, Jain S. Fine needle aspiration cytology and core biopsy histology in infiltrating syringomatous adenoma of the breast. A case report. Acta Cytol. 1999;43:303–7.PubMedCrossRefGoogle Scholar
  87. 87.
    de la Torre M, Lindholm K, Lindgren L. Fine needle aspiration cytology of tubular breast carcinoma and radial scar. Acta Cytol. 1994;38:884–90.PubMedGoogle Scholar
  88. 88.
    Nayar R, De Frias DV, Bourtsos EP, Sutton V, Bedrossian C. Cytologic differential diagnosis of papillary pattern in breast aspirates: correlation with histology. Ann Diagn Pathol. 2001;5:34–42.PubMedCrossRefGoogle Scholar
  89. 89.
    Di Saverio S, Gutierrez J, Avisar E. A retrospective review with long term follow up of 11,400 cases of pure mucinous breast carcinoma. Breast Cancer Res Treat. 2008;111:541–7.PubMedCrossRefGoogle Scholar
  90. 90.
    Memis A, Ozdemir N, Parildar M, Ustun EE, Erhan Y. Mucinous (colloid) breast cancer: mammographic and US features with histologic correlation. Eur J Radiol. 2000;35:39–43.PubMedCrossRefGoogle Scholar
  91. 91.
    Wilson TE, Helvie MA, Oberman HA, Joynt LK. Pure and mixed mucinous carcinoma of the breast: pathologic basis for differences in mammographic appearance. AJR Am J Roentgenol. 1995;165:285–9.PubMedCrossRefGoogle Scholar
  92. 92.
    Dawson AE, Mulford DK. Fine needle aspiration of mucinous (colloid) breast carcinoma. Nuclear grading and mammographic and cytologic findings. Acta Cytol. 1998;42:668–72.PubMedCrossRefGoogle Scholar
  93. 93.
    Sharma S, Bansal R, Khare A, Agrawal N. Mucinous carcinoma of breast: cytodiagnosis of a case. J Cytol. 2011;28:42–4.PubMedPubMedCentralCrossRefGoogle Scholar
  94. 94.
    Capella C, Eusebi V, Mann B, Azzopardi JG. Endocrine differentiation in mucoid carcinoma of the breast. Histopathology. 1980;4:613–30.PubMedCrossRefGoogle Scholar
  95. 95.
    Weigelt B, Geyer FC, Horlings HM, Kreike B, Halfwerk H, Reis-Filho JS. Mucinous and neuroendocrine breast carcinomas are transcriptionally distinct from invasive ductal carcinomas of no special type. Mod Pathol. 2009;22:1401–14.PubMedCrossRefGoogle Scholar
  96. 96.
    Laucirica R, Bentz JS, Khalbuss WE, Clayton AC, Souers RJ, Moriarty AT. Performance characteristics of mucinous (colloid) carcinoma of the breast in fine-needle aspirates: observations from the College of American Pathologists Interlaboratory Comparison Program in Nongynecologic Cytopathology. Arch Pathol Lab Med. 2011;135:1533–8.PubMedCrossRefGoogle Scholar
  97. 97.
    Meyer JE, Amin E, Lindfors KK, Lipman JC, Stomper PC, Genest D. Medullary carcinoma of the breast: mammographic and US appearance. Radiology. 1989;170:79–82.PubMedCrossRefGoogle Scholar
  98. 98.
    Jeong SJ, Lim HS, Lee JS, Park MH, Yoon JH, Park JG, Kanh HK. Medullary carcinoma of the breast: MRI findings. AJR Am J Roentgenol. 2012;198:W482–7.PubMedCrossRefGoogle Scholar
  99. 99.
    Akbulut M, Zekioglu O, Kapkac M, Ozdemir N. Fine needle aspiration cytologic features of medullary carcinoma of the breast: a study of 20 cases with histologic correlation. Acta Cytol. 2009;53:165–73.PubMedCrossRefGoogle Scholar
  100. 100.
    Bertucci F, Finetti P, Cervera N, Charafe-Jauffret E, Mamessier E, Adélaïde J, et al. Gene expression profiling shows medullary breast cancer is a subgroup of basal breast cancers. Cancer Res. 2006;66:4636–44.PubMedCrossRefGoogle Scholar
  101. 101.
    Takeuchi H, Tsuji K, Ueo H, Kano T, Maehara Y. Clinicopathological feature and long-term prognosis of apocrine carcinoma of the breast in Japanese women. Breast Cancer Res Treat. 2004;88:49–54.PubMedCrossRefGoogle Scholar
  102. 102.
    Unal E, Firat A, Gunes P, Kilicogly G, Gulkilik A, Titiz I. Apocrine carcinoma of the breast: clinical, radiologic, and pathologic correlation. Breast J. 2007;13(6):617–8.PubMedCrossRefGoogle Scholar
  103. 103.
    Gaurish S, Khandeparkar S, Deshmukh SD, Bhayekar PD. A rare case of apocrine carcinoma of the breast: cytopathological and immunohistopathological study. J Cytol. 2014;31:96–8.CrossRefGoogle Scholar
  104. 104.
    Honma N, Saji S, Kurabayashi R, Aida J, Arai T, Horii R, et al. Oestrogen receptor-beta1 but not oestrogen receptor-betacx is of prognostic value in apocrine carcinoma of the breast. APMIS. 2008;116:923–30.PubMedCrossRefGoogle Scholar
  105. 105.
    Celis JE, Cabezón T, Moreira JM, Gromov P, Gromova I, Timmermans-Wielenga V, et al. Molecular characterization of apocrine carcinoma of the breast: validation of an apocrine protein signature in a well-defined cohort. Mol Oncol. 2009;3:220–37.PubMedPubMedCentralCrossRefGoogle Scholar
  106. 106.
    Lininger RA, Zhuang Z, Man Y, Park WS, Emmert-Buck M, Tavassoli FA. Loss of heterozygosity is detected at chromosomes 1p35-36 (NB), 3p25 (VHL), 16p13 (TSC2/PKD1), and 17p13 (TP53) in microdissected apocrine carcinomas of the breast. Mod Pathol. 1999;12:1083–9.PubMedGoogle Scholar
  107. 107.
    Vranic S, Feldman R, Gatalica Z. Apocrine carcinoma of the breast: a brief update on the molecular features and targetable biomarkers. Bosn J Basic Med Sci. 2017;17:9–11.PubMedPubMedCentralGoogle Scholar
  108. 108.
    Vranic S, Tawfik O, Palazzo J, Bilalovic N, Eyzaguirre E, Lee LM, et al. EGFR and HER-2/neu expression in invasive apocrine carcinoma of the breast. Mod Pathol. 2010;23:644–53.PubMedCrossRefGoogle Scholar
  109. 109.
    Moritani S, Ichihara S, Hasegawa M, Endo T, Oiwa M, Shiraiwa M, et al. Intracytoplasmic lipid accumulation in apocrine carcinoma of the breast evaluated with adipophilin immunoreactivity: a possible link between apocrine carcinoma and lipid-rich carcinoma. Am J Surg Pathol. 2011;35:861–7.PubMedCrossRefGoogle Scholar
  110. 110.
    Huvos AG, Lucas JC Jr, Foote FW Jr. Metaplastic breast carcinoma. Rare form of mammary cancer. NY State J Med. 1973;73:1078–82.Google Scholar
  111. 111.
    Tavassoli FA, Devilee P, editors. World Health Organization classification of tumours. Pathology and genetics of tumours of the breast and female genital organs. 3rd ed. Lyon: IARC Press; 2003.Google Scholar
  112. 112.
    Rayson D, Adjei AA, Suman VJ, Wold LE, Ingle JN. Metaplastic breast cancer: prognosis and response to systemic therapy. Ann Oncol. 1999;10:413–9.PubMedCrossRefGoogle Scholar
  113. 113.
    Velasco M, Santamaría G, Ganau S, Farrús B, Zanón G, Romagosa C, Fernández PL. MRI of metaplastic carcinoma of the breast. AJR Am J Roentgenol. 2005;184:1274–8.PubMedCrossRefGoogle Scholar
  114. 114.
    Park JM, Han BK, Moon WK, Choe YH, Ahn SH, Gong G. Metaplastic carcinoma of the breast: mammographic and sonographic findings. J Clin Ultrasound. 2000;28:179–86.PubMedCrossRefGoogle Scholar
  115. 115.
    Joshi D, Singh P, Zonunfawni Y, Gangane N. Metaplastic carcinoma of the breast: cytological diagnosis and diagnostic pitfalls. Acta Cytol. 2011;55:313–8.PubMedCrossRefGoogle Scholar
  116. 116.
    Lui PC, Tse GM, Tan PH, Jayaram G, Putti TC, Chaiwun B, et al. Fine-needle aspiration cytology of metaplastic carcinoma of the breast. J Clin Pathol. 2007;60:529–33.PubMedCrossRefGoogle Scholar
  117. 117.
    van de Rijn M, Perou CM, Tibshirani R, Haas P, Kallioniemi O, Kononen J, et al. Expression of cytokeratins 17 and 5 identifies a group of breast carcinomas with poor clinical outcome. Am J Pathol. 2002;161(6):1991.PubMedPubMedCentralCrossRefGoogle Scholar
  118. 118.
    Carey LA, Perou CM, Livasy CA, Dressler LG, Cowan D, Conway K, et al. Race, breast cancer subtypes, and survival in the Carolina Breast Cancer Study. JAMA. 2006;295:2492–502.PubMedCrossRefGoogle Scholar
  119. 119.
    Koker MM, Kleer CG. p63 Expression in breast cancer. A highly sensitive and specific marker of metaplastic carcinoma. Am J Surg Pathol. 2004;28:1506–12.PubMedCrossRefGoogle Scholar
  120. 120.
    Leibl S, Moinfar F. Metaplastic breast carcinomas are negative for Her-2 but frequently express EGFR (Her-1): potential relevance to adjuvant treatment with EGFR tyrosine kinase inhibitors? J Clin Pathol. 2005;58:700–4.PubMedPubMedCentralCrossRefGoogle Scholar
  121. 121.
    Gilbert JA, Goetz MP, Reynolds CA, Ingle JN, Giordano KF, Suman VJ, et al. Molecular analysis of metaplastic breast carcinoma: high EGFR copy number via aneusomy. Mol Cancer Ther. 2008;7:944–51.PubMedPubMedCentralCrossRefGoogle Scholar
  122. 122.
    Reis-Filho JS, Pinheiro C, Lambros MB, Milanezi F, Carvalho S, Savage K, et al. EGFR amplification and lack of activating mutations in metaplastic breast carcinomas. J Pathol. 2006;209:445–53.PubMedCrossRefGoogle Scholar
  123. 123.
    Lien HC, Hsiao YH, Lin YS, Yao YT, Juan HF, Kuo WH, et al. Molecular signatures of metaplastic carcinoma of the breast by large-scale transcriptional profiling: identification of genes potentially related to epithelial–mesenchymal transition. Oncogene. 2007;26:7859–71.PubMedCrossRefGoogle Scholar
  124. 124.
    Korsching E, Packeisen J, Liedtke C, Hungermann D, Wülfing P, van Diest PJ, et al. The origin of vimentin expression in invasive breast cancer: epithelial–mesenchymal transition, myoepithelial histogenesis or histogenesis from progenitor cells with bilinear differentiation potential? J Pathol. 2005;206:451–7.PubMedCrossRefGoogle Scholar
  125. 125.
    Dunne B, Lee AH, Pinder SE, Bell JA, Ellis IO. An immunohistochemical study of metaplastic spindle cell carcinoma, phyllodes tumor and fibromatosis of the breast. Hum Pathol. 2003;34:1009–15.PubMedCrossRefGoogle Scholar
  126. 126.
    Mardi K, Sharma J. Matrix-producing mammary carcinoma: a rare breast tumor. Indian J Pathol Microbiol. 2008;51:263–4.PubMedCrossRefGoogle Scholar
  127. 127.
    Cook SS, DeMay R. Adenocarcinoma of the breast with osseous metaplasia. Report of a case with needle aspiration cytology. Acta Cytol. 1984;28:317–20.PubMedGoogle Scholar
  128. 128.
    Ng WK. Fine needle aspiration cytology of fibroadenoma with multinucleated stromal giant cells. A review of cases in a six-year period. Acta Cytol. 2002;46:535–9.PubMedCrossRefGoogle Scholar
  129. 129.
    Pal SK, Lau SK, Kruper L, Nwoye U, Garberoglio C, Gupta RK, et al. Papillary carcinoma of the breast: an overview. Breast Cancer Res Treat. 2010;122:637–45.PubMedPubMedCentralCrossRefGoogle Scholar
  130. 130.
    Eiada R, Chong J, Kulkarni S, Goldberg F, Muradali D. Papillary lesions of the breast: MRI, ultrasound, and mammographic appearances. AJR Am J Roentgenol. 2012;198:264–71.PubMedCrossRefGoogle Scholar
  131. 131.
    Lingamfelter D, Chen Y, Kure K, Lankachandra K. Infiltrating myoepithelial carcinoma of the breast, a case report and cytologic-histologic correlation. Diagn Pathol. 2008;3:7.PubMedPubMedCentralCrossRefGoogle Scholar
  132. 132.
    Agrawal G, Su MY, Nalcioglu O, Feig SA, Chen JH. Significance of breast lesion descriptors in the ACR BI-RADS MRI lexicon. Cancer. 2009;115:1363–80.PubMedPubMedCentralCrossRefGoogle Scholar
  133. 133.
    Rizzo M, Lund MJ, Oprea G, Schniederjan M, Wood WC, Mosunjac M. Surgical follow-up and clinical presentation of 142 breast papillary lesions diagnosed by ultrasound-guided core-needle biopsy. Ann Surg Oncol. 2008;15:1040–7.PubMedCrossRefGoogle Scholar
  134. 134.
    East EG, Zhao L, Pang JC, Jorns JM. Characteristics of a breast pathology consultation practice. Arch Pathol Lab Med. 2017;141:578–84.PubMedCrossRefGoogle Scholar
  135. 135.
    Naran S, Simpson J, Gupta RK. Cytologic diagnosis of papillary carcinoma of the breast in needle aspirates. Diagn Cytopathol. 1988;4:33–7.PubMedCrossRefGoogle Scholar
  136. 136.
    Dei Tos AP, Della Giustina D, Bittesini L. Aspiration biopsy cytology of malignant papillary breast neoplasms. Diagn Cytopathol. 1992;8:580–4.PubMedCrossRefGoogle Scholar
  137. 137.
    Bardales RH, Suhrland MJ, Stanley MW. Papillary neoplasms of the breast: fine-needle aspiration findings in cystic and solid cases. Diagn Cytopathol. 1994;10:336–41.PubMedCrossRefPubMedCentralGoogle Scholar
  138. 138.
    Gomez-Aracil V, Mayayo E, Azua J, Arraiza A. Papillary neoplasms of the breast: clues in fine needle aspiration cytology. Cytopathology. 2002;13:22–30.PubMedCrossRefGoogle Scholar
  139. 139.
    Haji BE, Das DK, Al-Ayadhy B, Pathan SK, George SG, Mallik MK, Abdeen SM. Fine-needle aspiration cytologic features of four special types of breast cancers: mucinous, medullary, apocrine, and papillary. Diagn Cytopathol. 2007;35:408–16.PubMedCrossRefPubMedCentralGoogle Scholar
  140. 140.
    Di Cristofano C, Mrad K, Zavaglia K, Bertacca G, Aretini P, Cipollini G, et al. Papillary lesions of the breast: a molecular progression? Breast Cancer Res Treat. 2005;90:71–6.PubMedCrossRefPubMedCentralGoogle Scholar
  141. 141.
    Troxell ML, Levine J, Beadling C, Warrick A, Dunlap J, Presnell A, et al. High prevalence of PIK3CA/AKT pathway mutations in papillary neoplasms of the breast. Mod Pathol. 2010;23:27–37.PubMedCrossRefGoogle Scholar
  142. 142.
    Khoury T, Hu Q, Liu S, Wang J. Intracystic papillary carcinoma of breast: interrelationship with in situ and invasive carcinoma and a proposal of pathogenesis: array comparative genomic hybridization study of 14 cases. Mod Pathol. 2014;27:194–203.PubMedCrossRefPubMedCentralGoogle Scholar
  143. 143.
    Wei S. Papillary lesions of the breast. An update. Arch Pathol Lab Med. 2016;140:628–43.PubMedCrossRefPubMedCentralGoogle Scholar
  144. 144.
    Ghabach B, Anderson WF, Curtis RE, Huycke MM, Lavigne JA, Dores GM. Adenoid cystic carcinoma of the breast in the United States (1977 to 2006): a population-based cohort study. Breast Cancer Res. 2010;12:R54.PubMedPubMedCentralCrossRefGoogle Scholar
  145. 145.
    Glazebrook KN, Reynolds C, Smith RL, Gimenez EI, Boughey JC. Adenoid cystic carcinoma of the breast. AJR Am J Roentgenol. 2010;194:1391–6.PubMedCrossRefGoogle Scholar
  146. 146.
    Gupta RK, Green C, Naran S, Lallu S, Fauck R, Dowle C, Simpson J. Fine-needle aspiration cytology of adenoid cystic carcinoma of the breast. Diagn Cytopathol. 1999;20:82–4.PubMedCrossRefGoogle Scholar
  147. 147.
    Azoulay S, Laé M, Fréneaux P, Merle S, Al Ghuzlan A, Chnecker C, et al. KIT is highly expressed in adenoid cystic carcinoma of the breast, a basal-like carcinoma associated with a favorable outcome. Mod Pathol. 2005;18:1623–31.PubMedCrossRefGoogle Scholar
  148. 148.
    Arpino G, Clark GM, Mohsin S, Bardou VJ, Elledge RM. Adenoid cystic carcinoma of the breast: molecular markers, treatment, and clinical outcome. Cancer. 2002;94:2119–27.PubMedCrossRefGoogle Scholar
  149. 149.
    Miyai K, Schwartz MR, Divatia MK, Anton RC, Park YW, Ayala AG, Ro JY. Adenoid cystic carcinoma of breast: recent advances. World J Clin Cases. 2014;2:732–41.PubMedPubMedCentralCrossRefGoogle Scholar
  150. 150.
    Weigelt B, Geyer FC, Reis-Filho JS. Histological types of breast cancer: how special are they? Mol Oncol. 2010;4:192–208.PubMedPubMedCentralCrossRefGoogle Scholar
  151. 151.
    Ilkay TM, Gozde K, Ozgur S, Dilaver D. Diagnosis of adenoid cystic carcinoma of the breast using fine-needle aspiration cytology: a case report and review of the literature. Diagn Cytopathol. 2015;43:722–6.PubMedCrossRefGoogle Scholar
  152. 152.
    Park J, Rizzo M, Jackson S, Bates SR, Green V, Oprea-Ilies G. Reed-Sternberg cells in breast FNA of a patient with left breast mass. Diagn Cytopathol. 2010;38:663–8.PubMedCrossRefGoogle Scholar
  153. 153.
    Zarnescu NO, Iliesiu A, Procop A, Tampa M, Matei C, Sajin M, et al. A challenging case of primary breast Hodgkin’s lymphoma. Maedica (Buchar). 2015;10:44–7.Google Scholar
  154. 154.
    Kitakata H, Yasumoto K, Sudo Y, Minato H, Takahashi Y. A case of primary small cell carcinoma of the breast. Breast Cancer. 2007;14:414–9.PubMedCrossRefGoogle Scholar
  155. 155.
    Wei B, Ding T, Xing Y, Wei W, Tian Z, Tang F, et al. Invasive neuroendocrine carcinoma of the breast. A distinctive subtype of aggressive mammary carcinoma. Cancer. 2010;116:4463–73.PubMedCrossRefPubMedCentralGoogle Scholar
  156. 156.
    Ersahin C, Bandyopadhyay S, Bhargava R. Thyroid transcription factor-1 and “basal marker”—expressing small cell carcinoma of the breast. Int J Surg Pathol. 2009;17:368–72.PubMedCrossRefPubMedCentralGoogle Scholar
  157. 157.
    Yamaguchi R, Tanaka M, Otsuka H, Yamaguchi M, Kaneko Y, Fukushima T, et al. Neuroendocrine small cell carcinoma of the breast: report of a case. Med Mol Morphol. 2009;42:58–61.PubMedCrossRefPubMedCentralGoogle Scholar
  158. 158.
    Hoang MP, Maitra A, Gazdar AF, Albores-Saavedra J. Primary mammary small-cell carcinoma: a molecular analysis of 2 cases. Hum Pathol. 2001;32(7):753.PubMedCrossRefPubMedCentralGoogle Scholar
  159. 159.
    Kinoshita S, Hirano A, Komine K, Kobayashi S, Kyoda S, Takeyama H, et al. Primary small-cell neuroendocrine carcinoma of the breast: report of a case. Surg Today. 2008;38(8):734.PubMedCrossRefPubMedCentralGoogle Scholar
  160. 160.
    Mosunjac MB, Kochhar R, Mosunjac MI, Lau SK. Primary small bowel carcinoid tumor with bilateral breast metastases. Report of 2 cases with different clinical presentations. Arch Pathol Lab Med. 2004;128:292–7.PubMedPubMedCentralGoogle Scholar
  161. 161.
    Cho YR, Jones S, Gosain AK. Neurofibromatosis: a cause of prepubertal gynecomastia. Plast Reconstr Surg. 2008;121:34e–0.PubMedCrossRefPubMedCentralGoogle Scholar
  162. 162.
    Morrone N, Morrone N Jr, Braz AG, Maia JA. Gynecomastia: a rare adverse effect of isoniazid. J Bras Pneumol. 2008;34:978–81.PubMedCrossRefGoogle Scholar
  163. 163.
    Abe K, Mitsuka T, Kanamori S, Yamashita K, Yamaoka A. Gynecomastia associated with low-dose methotrexate therapy for rheumatoid arthritis. Mod Rheumatol. 2007;17:511–3.PubMedCrossRefPubMedCentralGoogle Scholar
  164. 164.
    Henley DV, Lipson N, Korach KS, Bloch CA. Prepubertal gynecomastia linked to lavender and tea tree oils. N Engl J Med. 2007;356:479–85.PubMedCrossRefPubMedCentralGoogle Scholar
  165. 165.
    Nguyen C, Kettler MD, Swirsky ME, Miller VI, Scott C, Krause R, Hadro JA. Male breast disease: pictorial review with radiologic-pathologic correlation. Radiographics. 2013;33:763–79.PubMedCrossRefPubMedCentralGoogle Scholar
  166. 166.
    Amrikachi M, Green LK, Rone R, Ramzy I. Gynecomastia. Cytologic features and diagnostic pitfalls in fine needle aspirates. Acta Cytol. 2001;45:948–52.PubMedCrossRefPubMedCentralGoogle Scholar
  167. 167.
    Chen L, Chantra PK, Larsen LH, Barton P, Rohitopakarn M, Zhu EQ, Bassett LW. Imaging characteristics of malignant lesions of the male breast. Radiographics. 2006;26:993–1006.PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of PathologyEmory University School of MedicineAtlantaUSA
  2. 2.Weill Cornell MedicineNew YorkUSA

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