Abstract
Fine needle aspiration (FNA) is increasingly being supplanted by core needle biopsy. However, breast surgeons continue to rely on FNA at our institution. This retrospective study evaluated breast FNA for its diagnostic accuracy and breast cancer biomarker testing utility. All breast FNAs performed at Massachusetts General Hospital 2009–2015 were reviewed. Cytology diagnoses were compared with subsequent tissue or clinical diagnoses. Immunohistochemistry and fluorescence in situ hybridization (FISH) results using formalin-fixed paraffin-embedded (FFPE) cell blocks and histologic tissue blocks were compared. 1654 consecutive breast FNAs were included. Breast FNA demonstrated the following diagnostic performance: positive predictive value of malignant cytology diagnosis 100 %, negative predictive value of benign cytology diagnosis 97.5 %, complete sensitivity 91.6 %, and specificity 95.5 %. Concordance rates for estrogen receptor, progesterone receptor, and human epidermal growth factor receptor 2 (HER2) immunohistochemistry, and HER2 FISH were 98.2 % (κ = 0.95, p < 0.001), 100.0 % (κ = 1.000, p < 0.001), 83.1 % (κ = 0.69, p < 0.001), and 93.5 % (κ = 0.785, p < 0.001), respectively. Review of consecutive breast FNAs in a large cohort confirmed the excellent accuracy of this biopsy technique for breast lesion diagnosis. FNA FFPE cell blocks collected in the course of routine clinical care are adequate, practical, and reliable for breast cancer biomarker testing.
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References
Dixon JM, Anderson TJ, Lamb J, Nixon SJ, Forrest AP (1984) Fine needle aspiration cytology, in relationships to clinical examination and mammography in the diagnosis of a solid breast mass. Br J Surg 71(8):593–596
Sneige N (1993) Fine-needle aspiration of the breast: a review of 1,995 cases with emphasis on diagnostic pitfalls. Diagn Cytopathol 9(1):106–112
Ariga R, Bloom K, Reddy VB, Kluskens L, Francescatti D, Dowlat K, Siziopikou P, Gattuso P (2002) Fine-needle aspiration of clinically suspicious palpable breast masses with histopathologic correlation. Am J Surg 184(5):410–413
Kurita T, Tsuchiya S, Watarai Y, Yamamoto Y, Harada O, Yanagihara K, Iida S, Yamashita K, Haga SS, Uchida E (2012) Roles of fine-needle aspiration and core needle biopsy in the diagnosis of breast cancer. Breast Cancer 19(1):23–29. doi:10.1007/s12282-010-0251-4
Nagar S, Iacco A, Riggs T, Kestenberg W, Keidan R (2012) An analysis of fine needle aspiration versus core needle biopsy in clinically palpable breast lesions: a report on the predictive values and a cost comparison. Am J Surg 204(2):193–198. doi:10.1016/j.amjsurg.2011.10.018
Nassar A (2011) Core needle biopsy versus fine needle aspiration biopsy in breast–a historical perspective and opportunities in the modern era. Diagn Cytopathol 39(5):380–388. doi:10.1002/dc.21433
Simsir A, Cangiarella J (2012) Challenging breast lesions: pitfalls and limitations of fine-needle aspiration and the role of core biopsy in specific lesions. Diagn Cytopathol 40(3):262–272. doi:10.1002/dc.21630
National Comprehensive Cancer Network (2016) NCCN Clinical Practice Guidelines in Oncology. Accessed 10 June 2016
Hermansen C, Skovgaard Poulsen H, Jensen J, Langfeldt B, Steenskov V, Frederiksen P, Jensen OM (1987) Diagnostic reliability of combined physical examination, mammography, and fine-needle puncture (“triple-test”) in breast tumors a prospective study. Cancer 60(8):1866–1871
Vetto J, Pommier R, Schmidt W, Wachtel M, DuBois P, Jones M, Thurmond A (1995) Use of the “triple test” for palpable breast lesions yields high diagnostic accuracy and cost savings. Am J Surg 169(5):519–522. doi:10.1016/S0002-9610(99)80209-8
Lau SK, McKee GT, Weir MM, Tambouret RH, Eichhorn JH, Pitman MB (2004) The negative predicative value of breast fine-needle aspiration biopsy: the Massachusetts General Hospital experience. Breast J 10(6):487–491. doi:10.1111/j.1075-122X.2004.21496.x
Abati A, National Cancer Institute Conference (1997) The uniform approach to breast fine-needle aspiration biopsy. Am J Surg 174(4):371–385
Singh N, Wells CA (2001) Assessment of accuracy in breast cytology. Cytopathology 12(4):211–218
Yamaguchi R, Tsuchiya S, Koshikawa T, Ishihara A, Masuda S, Maeda I, Takimoto M, Kawamoto M, Satoh H, Narita M, Itoh H, Kitamura T, Tsuda Y, Ogane N, Abe E, Ikeda K, Nakamura T, Kamaguchi H, Tokoro Y (2012) Diagnostic accuracy of fine-needle aspiration cytology of the breast in Japan: report from the working group on the accuracy of breast fine-needle aspiration cytology of the Japanese Society of Clinical Cytology. Oncol Rep 28(5):1606–1612. doi:10.3892/or.2012.2014
Fung AD, Collins JA, Campassi C, Ioffe OB, Staats PN (2014) Performance characteristics of ultrasound-guided fine-needle aspiration of axillary lymph nodes for metastatic breast cancer employing rapid on-site evaluation of adequacy: analysis of 136 cases and review of the literature. Cancer Cytopathol 122(4):282–291. doi:10.1002/cncy.21384
Monaco SE, Wu Y, Teot LA, Cai G (2013) Assessment of estrogen receptor (ER), progesterone receptor (PR), and human epidermal growth factor receptor 2 (HER2) status in the fine needle aspirates of metastatic breast carcinomas. Diagn Cytopathol 41(4):308–315. doi:10.1002/dc.21841
Kinsella MD, Birdsong GG, Siddiqui MT, Cohen C, Hanley KZ (2013) Immunohistochemical detection of estrogen receptor, progesterone receptor and human epidermal growth factor receptor 2 in formalin-fixed breast carcinoma cell block preparations: correlation of results to corresponding tissue block (needle core and excision) samples. Diagn Cytopathol 41(3):192–198. doi:10.1002/dc.21815
Masood S, Rosa M, Kraemer DF, Smotherman C, Mohammadi A (2015) Comparative cost-effectiveness of fine needle aspiration biopsy versus image-guided biopsy, and open surgical biopsy in the evaluation of breast cancer in the era of Affordable Care Act: a changing landscape. Diagn Cytopathol 43(8):605–612. doi:10.1002/dc.23270
Ly A, Ono JC, Hughes KS, Pitman MB, Balassanian R (2016) Fine-needle aspiration biopsy of palpable breast masses: patterns of clinical use and patient experience. J Natl Compr Cancer Netw 14(5):527–536
Beatty BG, Bryant R, Wang W, Ashikaga T, Gibson PC, Leiman G, Weaver DL (2004) HER-2/neu detection in fine-needle aspirates of breast cancer: fluorescence in situ hybridization and immunocytochemical analysis. Am J Clin Pathol 122(2):246–255. doi:10.1309/N82C-TQ1J-0XEV-EFQB
Gong Y, Booser DJ, Sneige N (2005) Comparison of HER-2 status determined by fluorescence in situ hybridization in primary and metastatic breast carcinoma. Cancer 103(9):1763–1769. doi:10.1002/cncr.20987
Hanley KZ, Birdsong GG, Cohen C, Siddiqui MT (2009) Immunohistochemical detection of estrogen receptor, progesterone receptor, and human epidermal growth factor receptor 2 expression in breast carcinomas: comparison on cell block, needle-core, and tissue block preparations. Cancer 117(4):279–288. doi:10.1002/cncy.20034
Shabaik A, Lin G, Peterson M, Hasteh F, Tipps A, Datnow B, Weidner N (2011) Reliability of Her2/neu, estrogen receptor, and progesterone receptor testing by immunohistochemistry on cell block of FNA and serous effusions from patients with primary and metastatic breast carcinoma. Diagn Cytopathol 39(5):328–332. doi:10.1002/dc.21389
Bueno Angela SP, Viero RM, Soares CT (2013) Fine needle aspirate cell blocks are reliable for detection of hormone receptors and HER-2 by immunohistochemistry in breast carcinoma. Cytopathology 24(1):26–32. doi:10.1111/j.1365-2303.2011.00934.x
Acs B, Szekely N, Szasz AM, Lotz G, Szekely T, Istok R, Szekely E, Madaras L, Kulka J, Jaray B (2016) Reliability of immunocytochemistry and fluorescence in situ hybridization on fine-needle aspiration cytology samples of breast cancers: a comparative study. Diagn Cytopathol. doi:10.1002/dc.23463
Lakhani SR, Ellis IO, Schnitt SJ, Tan PH, van de Vijver MJ (2012) WHO classification of tumours of the breast. World Health Organization classification of tumours, 4th edn. International Agency for Research on Cancer, Lyon
Hammond ME, Hayes DF, Dowsett M, Allred DC, Hagerty KL, Badve S, Fitzgibbons PL, Francis G, Goldstein NS, Hayes M, Hicks DG, Lester S, Love R, Mangu PB, McShane L, Miller K, Osborne CK, Paik S, Perlmutter J, Rhodes A, Sasano H, Schwartz JN, Sweep FC, Taube S, Torlakovic EE, Valenstein P, Viale G, Visscher D, Wheeler T, Williams RB, Wittliff JL, Wolff AC (2010) American Society of Clinical Oncology/College Of American Pathologists guideline recommendations for immunohistochemical testing of estrogen and progesterone receptors in breast cancer. J Clin Oncol 28(16):2784–2795. doi:10.1200/JCO.2009.25.6529
Wolff AC, Hammond ME, Hicks DG, Dowsett M, McShane LM, Allison KH, Allred DC, Bartlett JM, Bilous M, Fitzgibbons P, Hanna W, Jenkins RB, Mangu PB, Paik S, Perez EA, Press MF, Spears PA, Vance GH, Viale G, Hayes DF, American Society of Clinical O, College of American P (2013) 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. J Clin Oncol 31(31):3997–4013. doi:10.1200/JCO.2013.50.9984
Shin SJ, Chen B, Hyjek E, Vazquez M (2007) Immunocytochemistry and fluorescence in situ hybridization in HER-2/neu status in cell block preparations. Acta Cytol 51(4):552–557
Stalhammar G, Rosin G, Fredriksson I, Bergh J, Hartman J (2014) Low concordance of biomarkers in histopathological and cytological material from breast cancer. Histopathology 64(7):971–980. doi:10.1111/his.12344
Sauer T, Ebeltoft K, Pedersen MK, Karesen R (2010) Liquid based material from fine needle aspirates from breast carcinomas offers the possibility of long-time storage without significant loss of immunoreactivity of estrogen and progesterone receptors. Cytojournal 7:24. doi:10.4103/1742-6413.75665
Williams SL, Birdsong GG, Cohen C, Siddiqui MT (2009) Immunohistochemical detection of estrogen and progesterone receptor and HER2 expression in breast carcinomas: comparison of cell block and tissue block preparations. Int J Clin Exp Pathol 2(5):476–480
Domanski AM, Monsef N, Domanski HA, Grabau D, Ferno M (2013) Comparison of the oestrogen and progesterone receptor status in primary breast carcinomas as evaluated by immunohistochemistry and immunocytochemistry: a consecutive series of 267 patients. Cytopathology 24(1):21–25. doi:10.1111/j.1365-2303.2012.00997.x
Aurilio G, Disalvatore D, Pruneri G, Bagnardi V, Viale G, Curigliano G, Adamoli L, Munzone E, Sciandivasci A, De Vita F, Goldhirsch A, Nole F (2014) A meta-analysis of oestrogen receptor, progesterone receptor and human epidermal growth factor receptor 2 discordance between primary breast cancer and metastases. Eur J Cancer 50(2):277–289. doi:10.1016/j.ejca.2013.10.004
Aker F, Gumrukcu G, Onomay BC, Erkan M, Gurleyik G, Kilicoglu G, Karagullu H (2015) Accuracy of fine-needle aspiration cytology in the diagnosis of breast cancer a single-center retrospective study from Turkey with cytohistological correlation in 733 cases. Diagn Cytopathol 43(12):978–986. doi:10.1002/dc.23380
Dueber J, Pang JC, Lew M, Jing X, Heider A, Davenport R, Bernacki KD, Kantola S, Roh MH (2015) Value of ultrasound guidance in cytopathologist-performed fine-needle aspirations of palpable lesions. J Am Soc Cytopathol 5(4):195–202
Boerner S, Sneige N (1998) Specimen adequacy and false-negative diagnosis rate in fine-needle aspirates of palpable breast masses. Cancer 84(6):344–348
Ljung BM, Drejet A, Chiampi N, Jeffrey J, Goodson WH 3rd, Chew K, Moore DH 2nd, Miller TR (2001) Diagnostic accuracy of fine-needle aspiration biopsy is determined by physician training in sampling technique. Cancer 93(4):263–268
Vetto JT, Pommier RF, Shih RL, Campagna J, Robbins D, Schmidt WA (2005) Breast fine-needle aspirates with scant cellularity are clinically useful. Am J Surg 189 (5):621–625; discussion 625–626. doi:10.1016/j.amjsurg.2005.01.040
Abdel-Hadi M, Abdel-Hamid GF, Abdel-Razek N, Fawzy RK (2010) Should fine-needle aspiration cytology be the first choice diagnostic modality for assessment of all nonpalpable breast lesions? The experience of a breast cancer screening center in Alexandria. Egypt. Diagn Cytopathol 38(12):880–889. doi:10.1002/dc.21305
Daramola AO, Odubanjo MO, Obiajulu FJ, Ikeri NZ, Banjo AA (2015) Correlation between fine-needle aspiration cytology and histology for palpable breast masses in a Nigerian Tertiary Health Institution. Int J Breast Cancer 2015:742573. doi:10.1155/2015/742573
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Jianyu Dong and Amy Ly contributed equally to this work.
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Dong, J., Ly, A., Arpin, R. et al. Breast fine needle aspiration continues to be relevant in a large academic medical center: experience from Massachusetts General Hospital. Breast Cancer Res Treat 158, 297–305 (2016). https://doi.org/10.1007/s10549-016-3886-9
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DOI: https://doi.org/10.1007/s10549-016-3886-9