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Can additional immunohistochemistry staining replace the surgical excision for the diagnosis of papillary breast lesions classified as benign on 14-gage core needle biopsy?

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Abstract

To evaluate whether the upgrade-to-malignancy rate of benign papillary lesions on ultrasonographically (US)-guided 14-gage core needle biopsy (CNB) can be decreased using immunohistochemistry staining (IHC) for pathologic diagnosis, and to determine whether additional IHC can replace surgical excision for the diagnosis of papillary breast lesions classified as benign on 14-gage CNB. A total of 274 consecutive papillary lesions were studied, including available imaging findings, CNB specimens and surgical specimens. Two rounds of retrospective review of the pathologic slides from CNB were performed by a pathologist, including H&E staining (first round; 1R, n = 274) and IHC of the benign papillomas (second round; 2R). The upgrade-to-malignancy rate was assessed for benign papillomas with comparison between 1R and 2R. The final diagnosis was based on surgical pathology. The clinicoradiologic findings were compared between the benign and malignant papillomas at the time of final diagnosis. In 1R, 204 benign papillomas were identified. During 2R using IHC, three carcinomas and ten atypical papillomas were diagnosed. Among the 204 benign papillomas from 1R, 15 were found to be carcinomas (upgrade-to-malignancy rate, 7.4 %) at the time of final diagnosis. With 2R, the overall upgrade-to-malignancy rate was decreased to 4.7 % (9/192, p = 0.3680). Older age and upgrades made after IHC review resulted in higher upgrade-to-malignancy rates (odds ratio, 4.133, 95 % CI 1.393–12.267, p = 0.0106; 134.46, 95 % CI 17.886–infinity, p < 0.0001, respectively). The use of IHC may decrease the upgrade-to-malignancy rate for benign papillary lesions after US-guided 14-gage CNB and help to more accurately predict malignancy at the time of surgery. Despite these findings, a misdiagnosis still occurred in our study, suggesting that IHC cannot replace surgical excision for diagnosis of benign papillary lesions of the breast.

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References

  1. Tavassoli FA, Schnitt SJ (1992) Pathology of the breast. Elsevier, New York, pp 193–227

    Google Scholar 

  2. Fenoglio C, Lattes R (1974) Sclerosing papillary proliferations in the female breast. A benign lesion often mistaken for carcinoma. Cancer 33:691–700

    Article  PubMed  CAS  Google Scholar 

  3. Kraus FT, Neubecker RD (1962) The differential diagnosis of papillary tumors of the breast. Cancer 15:444–455

    Article  PubMed  CAS  Google Scholar 

  4. Liberman L, Tornos C, Huzjan R, Bartella L, Morris EA, Dershaw DD (2006) Is surgical excision warranted after benign, concordant diagnosis of papilloma at percutaneous breast biopsy? AJR Am J Roentgenol 186:1328–1334

    Article  PubMed  Google Scholar 

  5. Mercado CL, Hamele-Bena D, Oken SM, Singer CI, Cangiarella J (2006) Papillary lesions of the breast at percutaneous core-needle biopsy. Radiology 238:801–808

    Article  PubMed  Google Scholar 

  6. Puglisi F, Zuiani C, Bazzocchi M, Valent F, Aprile G, Pertoldi B, Minisini AM, Cedolini C, Londero V, Piga A, Di Loreto C (2003) Role of mammography, ultrasound and large core biopsy in the diagnostic evaluation of papillary breast lesions. Oncology 65:311–315

    Article  PubMed  Google Scholar 

  7. Liberman L, Bracero N, Vuolo MA, Dershaw DD, Morris EA, Abramson AF, Rosen PP (1999) Percutaneous large-core biopsy of papillary breast lesions. AJR Am J Roentgenol 172:331–337

    PubMed  CAS  Google Scholar 

  8. Irfan K, Brem RF (2002) Surgical and mammographic follow-up of papillary lesions and atypical lobular hyperplasia diagnosed with stereotactic vacuum-assisted biopsy. Breast J 8:230–233

    Article  PubMed  Google Scholar 

  9. Ivan D, Selinko V, Sahin AA, Sneige N, Middleton LP (2004) Accuracy of core needle biopsy diagnosis in assessing papillary breast lesions: histologic predictors of malignancy. Mod Pathol 17:165–171

    Article  PubMed  Google Scholar 

  10. Ahmadiyeh N, Stoleru MA, Raza S, Lester SC, Golshan M (2009) Management of intraductal papillomas of the breast: an analysis of 129 cases and their outcome. Ann Surg Oncol 16:2264–2269

    Article  PubMed  Google Scholar 

  11. Al Sarakbi W, Worku D, Escobar P, Mokbel K (2006) Breast papillomas: current management with a focus on a new diagnostic and therapeutic modality. Int Semin Surg Oncol 3:1

    Article  PubMed  CAS  Google Scholar 

  12. Kim MJ, Kim EK, Kwak JY, Son EJ, Park BW, Kim SI, Oh KK (2008) Nonmalignant papillary lesions of the breast at US-guided directional vacuum-assisted removal: a preliminary report. Eur Radiol 18:1774–1783

    Article  PubMed  Google Scholar 

  13. Kim MJ, Kim SI, Youk JH, Moon HJ, Kwak JY, Park BW, Kim EK (2011) The diagnosis of non-malignant papillary lesions of the breast: comparison of ultrasound-guided automated gun biopsy and vacuum-assisted removal. Clin Radiol 66:530–535

    Article  PubMed  CAS  Google Scholar 

  14. Mercado CL, Hamele-Bena D, Singer C, Koenigsberg T, Pile-Spellman E, Higgins H, Smith SJ (2001) Papillary lesions of the breast: evaluation with stereotactic directional vacuum-assisted biopsy. Radiology 221:650–655

    Article  PubMed  CAS  Google Scholar 

  15. Sohn V, Keylock J, Arthurs Z, Wilson A, Herbert G, Perry J, Eckert M, Smith D, Groo S, Brown T (2007) Breast papillomas in the era of percutaneous needle biopsy. Ann Surg Oncol 14:2979–2984

    Article  PubMed  Google Scholar 

  16. Furuya C, Kawano H, Yamanouchi T, Oga A, Ueda J, Takahashi M (2012) Combined evaluation of CK5/6, ER, p63, and MUC3 for distinguishing breast intraductal papilloma from ductal carcinoma in situ. Pathol Int 62:381–390

    Article  PubMed  Google Scholar 

  17. Grin A, O’Malley FP, Mulligan AM (2009) Cytokeratin 5 and estrogen receptor immunohistochemistry as a useful adjunct in identifying atypical papillary lesions on breast needle core biopsy. Am J Surg Pathol 33:1615–1623

    Article  PubMed  Google Scholar 

  18. Schnitt SJ, Collins LC (2008) Biopsy interpretation of the breast. Wolters Kluwer/Lippincott Williams & Wilkins, Philadelphia

    Google Scholar 

  19. Philpotts LE, Shaheen NA, Jain KS, Carter D, Lee CH (2000) Uncommon high-risk lesions of the breast diagnosed at stereotactic core-needle biopsy: clinical importance. Radiology 216:831–837

    PubMed  CAS  Google Scholar 

  20. Rosen EL, Bentley RC, Baker JA, Soo MS (2002) Imaging-guided core needle biopsy of papillary lesions of the breast. AJR Am J Roentgenol 179:1185–1192

    PubMed  Google Scholar 

  21. Agoff SN, Lawton TJ (2004) Papillary lesions of the breast with and without atypical ductal hyperplasia: can we accurately predict benign behavior from core needle biopsy? Am J Clin Pathol 122:440–443

    Article  PubMed  Google Scholar 

  22. Bode MK, Rissanen T, Apaja-Sarkkinen M (2009) Ultrasonography-guided core needle biopsy in differential diagnosis of papillary breast tumors. Acta Radiol 50:722–729

    Article  PubMed  CAS  Google Scholar 

  23. Chang JM, Moon WK, Cho N, Han W, Noh DY, Park IA, Jung EJ (2010) Risk of carcinoma after subsequent excision of benign papilloma initially diagnosed with an ultrasound (US)-guided 14-gauge core needle biopsy: a prospective observational study. Eur Radiol 20:1093–1100

    Article  PubMed  Google Scholar 

  24. Chang JM, Moon WK, Cho N, Han W, Noh DY, Park IA, Jung EJ (2011) Management of ultrasonographically detected benign papillomas of the breast at core needle biopsy. AJR Am J Roentgenol 196:723–729

    Article  PubMed  Google Scholar 

  25. Ko ES, Cho N, Cha JH, Park JS, Kim SM, Moon WK (2007) Sonographically-guided 14-gauge core needle biopsy for papillary lesions of the breast. Korean J Radiol 8:206–211

    Article  PubMed  Google Scholar 

  26. Sydnor MK, Wilson JD, Hijaz TA, Massey HD, Shaw de Paredes ES (2007) Underestimation of the presence of breast carcinoma in papillary lesions initially diagnosed at core-needle biopsy. Radiology 242:58–62

    Article  PubMed  Google Scholar 

  27. Tseng HS, Chen YL, Chen ST, Wu YC, Kuo SJ, Chen LS, Wu HK, Chen DR (2009) The management of papillary lesion of the breast by core needle biopsy. Eur J Surg Oncol 35:21–24

    Article  PubMed  CAS  Google Scholar 

  28. Youk JH, Kim EK, Kwak JY, Son EJ, Park BW, Kim SI (2011) Benign papilloma without atypia diagnosed at US-guided 14-gauge core-needle biopsy: clinical and US features predictive of upgrade to malignancy. Radiology 258:81–88

    Article  PubMed  Google Scholar 

  29. Chang JM, Han W, Moon WK, Cho N, Noh DY, Park IA, Jung EJ (2011) Papillary lesions initially diagnosed at ultrasound-guided vacuum-assisted breast biopsy: rate of malignancy based on subsequent surgical excision. Ann Surg Oncol 18:2506–2514

    Article  PubMed  Google Scholar 

  30. Cheng TY, Chen CM, Lee MY, Lin KJ, Hung CF, Yang PS, Yu BL, Yang CE, Tsai TJ, Lin CW (2009) Risk factors associated with conversion from nonmalignant to malignant diagnosis after surgical excision of breast papillary lesions. Ann Surg Oncol 16:3375–3379

    Article  PubMed  Google Scholar 

  31. Kil WH, Cho EY, Kim JH, Nam SJ, Yang JH (2008) Is surgical excision necessary in benign papillary lesions initially diagnosed at core biopsy? Breast 17:258–262

    Article  PubMed  Google Scholar 

  32. Rizzo M, Linebarger J, Lowe MC, Pan L, Gabram SG, Vasquez L, Cohen MA, Mosunjac M (2012) Management of papillary breast lesions diagnosed on core-needle biopsy: clinical pathologic and radiologic analysis of 276 cases with surgical follow-up. J Am Coll Surg 214:280–287

    Article  PubMed  Google Scholar 

  33. Plantade R, Gerard F, Hammou JC (2006) Management of non malignant papillary lesions diagnosed on percutaneous biopsy. J Radiol 87:299–305

    Article  PubMed  CAS  Google Scholar 

  34. Skandarajah AR, Field L, Yuen Larn Mou A, Buchanan M, Evans J, Hart S, Mann GB (2008) Benign papilloma on core biopsy requires surgical excision. Ann Surg Oncol 15:2272–2277

    Article  PubMed  Google Scholar 

  35. Bernik SF, Troob S, Ying BL, Simpson SA, Axelrod DM, Siegel B, Moncrief RM, Mills C, Aziz M (2009) Papillary lesions of the breast diagnosed by core needle biopsy: 71 cases with surgical follow-up. Am J Surg 197:473–478

    Article  PubMed  Google Scholar 

  36. Collins LC, Schnitt SJ (2008) Papillary lesions of the breast: selected diagnostic and management issues. Histopathology 52:20–29

    Article  PubMed  CAS  Google Scholar 

  37. Jakate K, De Brot M, Goldberg F, Muradali D, O’Malley FP, Mulligan AM (2012) Papillary lesions of the breast: impact of breast pathology subspecialization on core biopsy and excision diagnoses. Am J Surg Pathol 36:544–551

    Article  PubMed  Google Scholar 

  38. Tan PH, Aw MY, Yip G, Bay BH, Sii LH, Murugaya S, Tse GM (2005) Cytokeratins in papillary lesions of the breast: is there a role in distinguishing intraductal papilloma from papillary ductal carcinoma in situ? Am J Surg Pathol 29:625–632

    Article  PubMed  Google Scholar 

  39. Shah VI, Flowers CI, Douglas-Jones AG, Dallimore NS, Rashid M (2006) Immunohistochemistry increases the accuracy of diagnosis of benign papillary lesions in breast core needle biopsy specimens. Histopathology 48:683–691

    Article  PubMed  CAS  Google Scholar 

  40. Koo JS, Kim MJ, Kim EK, Park BW (2012) Comparison of immunohistochemical staining in breast papillary neoplasms of cytokeratin 5/6 and p63 in core needle biopsies and surgical excisions. Appl Immunohistochem Mol Morphol 20:108–115

    Article  PubMed  CAS  Google Scholar 

  41. Pathmanathan N, Albertini AF, Provan PJ, Milliken JS, Salisbury EL, Bilous AM, Byth K, Balleine RL (2010) Diagnostic evaluation of papillary lesions of the breast on core biopsy. Mod Pathol 23:1021–1028

    Article  PubMed  Google Scholar 

  42. Tse GM, Tan PH, Moriya T (2009) The role of immunohistochemistry in the differential diagnosis of papillary lesions of the breast. J Clin Pathol 62:407–413

    Article  PubMed  CAS  Google Scholar 

  43. Tse GM, Tan PH, Lacambra MD, Jara-Lazaro AR, Chan SK, Lui PC, Ma TK, Vong JS, Ng DC, Shi HJ, Lam WW (2010) Papillary lesions of the breast—accuracy of core biopsy. Histopathology 56:481–488

    Article  PubMed  Google Scholar 

  44. Tse GM, Tan PH, Lui PC, Gilks CB, Poon CS, Ma TK, Law BK, Lam WW (2007) The role of immunohistochemistry for smooth-muscle actin, p63, CD10 and cytokeratin 14 in the differential diagnosis of papillary lesions of the breast. J Clin Pathol 60:315–320

    Article  PubMed  CAS  Google Scholar 

  45. Douglas-Jones A, Shah V, Morgan J, Dallimore N, Rashid M (2005) Observer variability in the histopathological reporting of core biopsies of papillary breast lesions is reduced by the use of immunohistochemistry for CK5/6, calponin and p63. Histopathology 47:202–208

    Article  PubMed  CAS  Google Scholar 

  46. Elston CW, Sloane JP, Amendoeira I, Apostolikas N, Bellocq JP, Bianchi S, Boecker W, Bussolati G, Coleman D, Connolly CE, Dervan P, Drijkoningen M, Eusebi V, Faverly D, Holland R, Jacquemier J, Lacerda M, Martinez-Penuela J, de Miguel C, Mossi S, Munt C, Peterse JL, Rank F, Reiner A, Sylvan M, Wells CA, Zafrani B (2000) Causes of inconsistency in diagnosing and classifying intraductal proliferations of the breast. European Commission Working Group on Breast Screening Pathology. Eur J Cancer 36:1769–1772

    Article  PubMed  CAS  Google Scholar 

  47. Jain RK, Mehta R, Dimitrov R, Larsson LG, Musto PM, Hodges KB, Ulbright TM, Hattab EM, Agaram N, Idrees MT, Badve S (2011) Atypical ductal hyperplasia: interobserver and intraobserver variability. Mod Pathol 24:917–923

    Article  PubMed  Google Scholar 

  48. Wen X, Cheng W (2012) Nonmalignant breast papillary lesions at core-needle biopsy: a meta-analysis of underestimation and influencing factors. Ann Surg Oncol 20:94–101

    Google Scholar 

  49. Carder PJ, Khan T, Burrows P, Sharma N (2008) Large volume “mammotome” biopsy may reduce the need for diagnostic surgery in papillary lesions of the breast. J Clin Pathol 61:928–933

    Article  PubMed  CAS  Google Scholar 

  50. Zografos GC, Zagouri F, Sergentanis TN, Nonni A, Michalopoulos NV, Kontogianni P, Koulocheri D, Dimitriadis IE, Bramis J, Patsouris E (2008) Diagnosing papillary lesions using vacuum-assisted breast biopsy: should conservative or surgical management follow? Onkologie 31:653–656

    PubMed  Google Scholar 

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Acknowledgments

This study was supported by a BumSuk Academic Research fund of 2009.

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Authors and Affiliations

  1. Department of Pathology, Yonsei University College of Medicine, Seoul, South Korea

    Ja Seung Koo

  2. Biostatistics Collaboration Unit, Yonsei University College of Medicine, Seoul, South Korea

    Kyunghwa Han

  3. Department of Radiology, Research Institute of Radiological Science, Severance Hospital, Yonsei University College of Medicine, 50 Yonsei-ro, Seodaemun-gu, Seoul, South Korea

    Min Jung Kim, Hee Jung Moon & Eun-Kyung Kim

  4. Department of Surgery, Yonsei University College of Medicine, Seoul, South Korea

    Byeong-Woo Park

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  1. Ja Seung Koo
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  2. Kyunghwa Han
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Correspondence to Min Jung Kim.

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Koo, J.S., Han, K., Kim, M.J. et al. Can additional immunohistochemistry staining replace the surgical excision for the diagnosis of papillary breast lesions classified as benign on 14-gage core needle biopsy?. Breast Cancer Res Treat 137, 797–806 (2013). https://doi.org/10.1007/s10549-012-2403-z

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  • DOI: https://doi.org/10.1007/s10549-012-2403-z

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