Central retesting of breast cancer with HER2 immunohistochemistry score of 0 or 1+ using silver-enhanced in situ hybridisation: a multicentre, prospective study in Greece

[1] Wolff AC, Hammond ME, Schwartz JN, Hagerty KL, Allred DC, Cote RJ, Dowsett M, Fitzgibbons PL, Hanna WM, Langer A, McShane LM, Paik S, Pegram MD, Perez EA, Press MF, Rhodes A, Sturgeon C, Taube SE, Tubbs R, Vance GH, van de Vijver M, Wheeler TM, Hayes DF, American Society of Clinical Oncology, College of American Pathologists (2007) American Society of Clinical Oncology/College of American Pathologists guideline recommendations for human epidermal growth factor receptor 2 testing in breast cancer. J Clin Oncol 25:118–145. doi: 10.1200/JCO.2006.09.277510.1200/JCO.2006.09.2775Search in Google Scholar

[2] Slamon DJ, Leyland-Jones B, Shak S, Fuchs H, Paton V, Bajamonde A, Fleming T, Eiermann W, Wolter J, Pegram M, Baselga J, Norton L (2001) Use of chemotherapy plus a monoclonal antibody against HER2 for metastatic breast cancer that overexpresses HER2. N Engl J Med 344:783–792. doi: 10.1056/NEJM20010315344110110.1056/NEJM200103153441101Search in Google Scholar

[3] Piccart-Gebhart MJ, Procter M, Leyland-Jones B, Goldhirsch A, Untch M, Smith I, Gianni L, Baselga J, Bell R, Jackisch C, Cameron D, Dowsett M, Barrios CH, Steger G, Huang CS, Andersson M, Inbar M, Lichinitser M, Lang I, Nitz U, Iwata H, Thomssen C, Lohrisch C, Suter TM, Ruschoff J, Suto T, Greatorex V, Ward C, Straehle C, McFadden E, Dolci MS, Gelber RD (2005) Trastuzumab after adjuvant chemotherapy in HER2-positive breast cancer. N Engl J Med 353:1659–1672. doi: 10.1056/ NEJMoa05230610.1056/NEJMoa052306Search in Google Scholar

[4] Marty M, Cognetti F, Maraninchi D, Snyder R, Mauriac L, Tubiana-Hulin M, Chan S, Grimes D, Anton A, Lluch A, Kennedy J, O’Byrne K, Conte P, Green M, Ward C, Mayne K, Extra JM (2005) Randomized phase II trial of the effcacy and safety of trastuzumab combined with docetaxel in patients with human epidermal growth factor receptor 2-positive metastatic breast cancer administered as frst-line treatment: the M77001 study group. J Clin Oncol 23:4265–4274. doi: 10.1200/ JCO.2005.04.173Search in Google Scholar

[5] Gianni L, Eiermann W, Semiglazov V, Manikhas A, Lluch A, Tjulandin S, Zambetti M, Vazquez F, Byakhow M, Lichinitser M, Climent MA, Ciruelos E, Ojeda B, Mansutti M, Bozhok A, Baronio R, Feyereislova A, Barton C, Valagussa P, Baselga J (2010) Neoadjuvant chemotherapy with trastuzumab followed by adjuvant trastuzumab versus neoadjuvant chemotherapy alone, in patients with HER2-positive locally advanced breast cancer (the NOAH trial): a randomised controlled superiority trial with a parallel HER2-negative cohort. Lancet 375:377–384. doi: 10.1016/S0140-6736(09)61964-410.1016/S0140-6736(09)61964-4Search in Google Scholar

[6] Cobleigh MA, Vogel CL, Tripathy D, Robert NJ, Scholl S, Fehrenbacher L, Wolter JM, Paton V, Shak S, Lieberman G, Slamon DJ (1999) Multinational study of the effcacy and safety of humanized anti-HER2 monoclonal antibody in women who have HER2-overexpressing metastatic breast cancer that has progressed after chemotherapy for metastatic disease. J Clin Oncol 17:2639–264810.1200/JCO.1999.17.9.263910561337Search in Google Scholar

[7] Vogel CL, Cobleigh MA, Tripathy D, Gutheil JC, Harris LN, Fehrenbacher L, Slamon DJ, Murphy M, Novotny WF, Burchmore M, Shak S, Stewart SJ, Press M (2002) Effcacy and safety of trastuzumab as a single agent in frst-line treatment of HER2-overexpressing metastatic breast cancer. J Clin Oncol 20:719–726. doi: 10.1200/JCO.20.3.71910.1200/JCO.20.3.719Search in Google Scholar

[8] Boekhout AH, Beijnen JH, Schellens JH (2011) Trastuzumab. Oncologist 16:800–810. doi: 10.1634/theoncologist.2010-003510.1634/theoncologist.2010-0035322821321632460Search in Google Scholar

[9] Jackisch C (2006) HER-2-positive metastatic breast cancer: optimizing trastuzumab-based therapy. Oncologist 11 (Suppl 1):34–41. doi: 10.1634/theoncologist.11-90001-3410.1634/theoncologist.11-90001-3416971738Search in Google Scholar

[10] National Comprehensive Cancer Network (2013) NCCN Clinical Practice Guidelines in Oncology: Breast Cancer, Version 1Search in Google Scholar

[11] Mass RD, Press MF, Anderson S, Cobleigh MA, Vogel CL, Dybdal N, Leiberman G, Slamon DJ (2005) Evaluation of clinical outcomes according to HER2 detection by fuorescence in situ hybridization in women with metastatic breast cancer treated with trastuzumab. Clin Breast Cancer 6:240–246. doi: 10.3816/CBC.2005.n.02610.3816/CBC.2005.n.02616137435Search in Google Scholar

[12] Baselga J, Cortes J, Kim SB, Im SA, Hegg R, Im YH, Roman L, Pedrini JL, Pienkowski T, Knott A, Clark E, Benyunes MC, Ross G, Swain SM, CLEOPATRA Study Group (2012) Pertuzumab plus trastuzumab plus docetaxel for metastatic breast cancer. N Engl J Med 366:109–119. doi: 10.1056/ NEJMoa111321610.1056/NEJMoa1113216570520222149875Search in Google Scholar

[13] Verma S, Miles D, Gianni L, Krop IE, Welslau M, Baselga J, Pegram M, Oh D-Y, Diéras V, Guardino E, Fang L, Lu M, Olsen S and Blakwell K (2012) Trastuzumab emtansine for HER2-positive advanced breast cancer. N Engl J Med 2012;367:1783-91. doi:10.1056/ NEJMoa120912410.1056/NEJMoa1209124512525023020162Search in Google Scholar

[14] Geyer CE, Forster J, Lindquist D, Chan S, Romieu CG, Pienkowski T, Jagiello-Gruszfeld A, Crown J, Chan A, Kaufman B, Skarlos D, Campone M, Davidson N, Berger M, Oliva C, Rubin SD, Stein S, Cameron D (2006) Lapatinib plus capecitabine for HER2-positive advanced breast cancer. N Engl J Med 355:2733–2743. doi: 10.1056/NEJMoa06432010.1056/NEJMoa06432017192538Search in Google Scholar

[15] Yamauchi H, Stearns V, Hayes DF (2001) When is a tumor marker ready for prime time? A case study of c-erb B-2 as a predictive factor in breast cancer. J Clin Oncol 19:2334–235610.1200/JCO.2001.19.8.233411304787Search in Google Scholar

[16] Penault-Llorca F, Bilous M, Dowsett M, Hanna W, Osamura RY, Rüschoff J, van de Vijver M (2009) Emerging technologies for assessing HER2 amplifcation. Am J Clin Pathol 132:539–548. doi: 10.1309/AJCPV2I0HGPMGBSQ10.1309/AJCPV2I0HGPMGBSQ19762531Search in Google Scholar

[17] Dietel M, Ellis IO, Höfer H, Kreipe H, Moch H, Dankof A, Kölble K, Kristiansen G (2007) Comparison of automated silver enhanced in situ hybridisation (SISH) and fuorescence ISH (FISH) for the validation of HER2 gene status in breast carcinoma according to the guidelines of the American Society of Clinical Oncology and the College of American Pathologists. Virchows Arch 451:19–25. doi: 10.1007/s00428-007-0424-510.1007/s00428-007-0424-517562074Search in Google Scholar

[18] Bartlett JM, Campbell FM, Ibrahim M, Wencyk P, Ellis I, Kay E, Connolly Y, O’Grady A, Di Palma S, Starczynski J, Morgan JM, Jasani B, Miller K (2009) Chromogenic in situ hybridization: a multicenter study comparing silver in situ hybridization with FISH. Am J Clin Pathol 132:514–520. doi: 10.1309/ AJCPXY3MJ6GSRCYP10.1309/AJCPXY3MJ6GSRCYP19762528Search in Google Scholar

[19] Ross JS (2011) Point: Fluorescence in situ hybridization is the preferred approach over immunohistochemistry for determining HER2 status. Clin Chem 57:980–982. doi: 10.1373/ clinchem.2010.16076210.1373/clinchem.2010.16076221558455Search in Google Scholar

[20] Cuadros M, Villegas R (2009) Systematic review of HER2 breast cancer testing. Appl Immunohistochem Mol Morphol 17:1–7. doi: 10.1097/PAI.0b013e318169fc1c10.1097/PAI.0b013e318169fc1c18685491Search in Google Scholar

[21] Papadopoulos S, Kouvatseas G, Skarlos D, Malamos N, Delliou E, Saratsiotou I, Ardavanis A, Mavroudis D, Skarpidi E, Arapantoni P, Karyda I, Patakioyta F, Aravantinos G, Razis E, Fountzilas G, Kosmidis P (2007) Comparison of HER2 detection methods between central and regional laboratories in Greece. Clin Breast Cancer 7:784–790. doi: 10.3816/CBC.2007.n.04010.3816/CBC.2007.n.04018021480Search in Google Scholar

[22] Vergara-Lluri ME, Moatamed NA, Hong E, Apple SK (2012) High concordance between HercepTest immunohistochemistry and ERBB2 fuorescence in situ hybridization before and after implementation of American Society of Clinical Oncology/College of American Pathology 2007 guidelines. Mod Pathol 25:1326–1332. doi: 10.1038/modpathol.2012.9310.1038/modpathol.2012.9322699517Search in Google Scholar

[23] Agresti A, Coull BA (1998) Approximate is better than “exact” for interval estimation of binomial proportions. Am Stat 52:119–126Search in Google Scholar

[24] Press MF, Slamon DJ, Flom KJ, Park J, Zhou JY, Bernstein L (2002) Evaluation of HER-2/neu gene amplifcation and overexpression: comparison of frequently used assay methods in a molecularly characterized cohort of breast cancer specimens. J Clin Oncol 20:3095–3105. doi: 10.120/ JCO.2002.09.094Search in Google Scholar

[25] Lal P, Salazar PA, Hudis CA, Ladanyi M, Chen B (2004) HER-2 testing in breast cancer using immunohistochemical analysis and fuorescence in situ hybridization: a single-institution experience of 2,279 cases and comparison of dual-color and single-color scoring. Am J Clin Pathol 121:631– 636. doi: 10.1309/VE78-62V2-646B-R6EX10.1309/VE78-62V2-646B-R6EX15151202Search in Google Scholar

[26] Perez EA, Suman VJ, Davidson NE, Martino S, Kaufman PA, Lingle WL, Flynn PJ, Ingle JN, Visscher D, Jenkins RB (2006) HER2 testing by local, central, and reference laboratories in specimens from the North Central Cancer Treatment Group N9831 intergroup adjuvant trial. J Clin Oncol 24:3032–3038. doi: 10.1200/JCO.2005.03.474410.1200/JCO.2005.03.474416809727Search in Google Scholar

[27] Paik S, Bryant J, Tan-Chiu E, Romond E, Hiller W, Park K, Brown A, Yothers G, Anderson S, Smith R, Wickerham DL, Wolmark N (2002) Real-world performance of HER2 testing-National Surgical Adjuvant Breast and Bowel Project experience. J Natl Cancer Inst 94:852–854. doi: 10.1093/ jnci/94.11.85210.1093/jnci/94.11.85212048273Search in Google Scholar

[28] Roche PC, Suman VJ, Jenkins RB, Davidson NE, Martino S, Kaufman PA, Addo FK, Murphy B, Ingle JN, Perez EA (2002) Concordance between local and central laboratory HER2 testing in the Breast Intergroup trial N9831. J Natl Cancer Inst 94:855–857. doi: 10.1093/jnci/94.11.85510.1093/jnci/94.11.85512048274Search in Google Scholar

[29] Reddy JC, Reimann JD, Anderson SM, Klein PM (2006) Concordance between central and local laboratory HER2 testing from a community-based clinical study. Clin Breast Cancer 7:153–157. doi: 10.3816/CBC.2006.n.02510.3816/CBC.2006.n.02516800975Search in Google Scholar

[30] Larsimont D, Colpaert C, Salgado R, Vermeesen N, D’hondt V, De Celle T (2011) Results of a Belgian multicenter retrospective study to determine the incidence of HER2 gene amplifcation in patients scored as immunohistochemistry 0 or 1+. J Clin Oncol 29:abstr 549Search in Google Scholar

[31] Reiner-Concin AM, Lax S, Regitnig P, Kronberger C, Jasarevic Z, Bogner S (2011) Should HER-2 score 0/1+ breast cancer cases be retested by in-situ hybridisation? Results of a multicenter retesting study. Cancer Res 71:P5-11-15. doi: 10.1158/0008-5472.SABCS11-P5-11-1510.1158/0008-5472.SABCS11-P5-11-15Search in Google Scholar

[32] Hanna W, Barnes PJ, Chang MC, Gilks B, Magliocco A, Rees H, Robertson S, SenGupta SK, Nofech-Mozes S (2012) The incidence of false negative of HER2/Neu status in primary breast cancer in the era of standardized testing: a Canadian prospective study. Cancer Res 72:P2-10-09. doi: 10.1158/0008-5472. SABCS12-P2-10-09Search in Google Scholar

[33] Lee M, Cho S, Kim D, Lee K, Lee J, Kwon H, Lee H, Lee S (2012) Concordance between immunohistochemistry and FISH (fuorescence in situ hybridization) & SISH (silver in situ hybridization) for assessment of the HER2. Cancer Res 72:PD02-06. doi: 10.1158/0008-5472.SABCS12-PD02-0610.1158/0008-5472.SABCS12-PD02-06Search in Google Scholar

[34] Slamon DJ, Godolphin W, Jones LA, Holt JA, Wong SG, Keith DE, Levin WJ, Stuart SG, Udove J, Ullrich A (1989) Studies of the HER-2/ neu proto-oncogene in human breast and ovarian cancer. Science 244:707–712. doi: 10.1126/ science.247015210.1126/science.24701522470152Search in Google Scholar

[35] Press MF, Hung G, Godolphin W, Slamon DJ (1994) Sensitivity of HER-2/neu antibodies in archival tissue samples: potential source of error in immunohistochemical studies of oncogene expression. Cancer Res 54:2771–2777Search in Google Scholar

[36] van der Vegt B, de Bock GH, Bart J, Zwartjes NG, Wesseling J (2009) Validation of the 4B5 rabbit monoclonal antibody in determining Her2/neu status in breast cancer. Mod Pathol 22:879-886. doi: 10.1038/modpathol.2009.3710.1038/modpathol.2009.3719305385Search in Google Scholar

[37] Marchiò C, Lambros MB, Gugliotta P, Di Cantogno LV, Botta C, Pasini B, Tan DS, Mackay A, Fenwick K, Tamber N, Bussolati G, Ashworth A, Reis-Filho JS, Sapino A (2009) Does chromosome 17 centromere copy number predict polysomy in breast cancer? A fuorescence in situ hybridization and microarray-based CGH analysis. J Pathol 219:16–24. doi: 10.1002/path.257410.1002/path.257419670217Search in Google Scholar

[38] Grimm EE, Schmidt RA, Swanson PE, Dintzis SM, Allison KH (2010) Achieving 95% cross-methodological concordance in HER2 testing: causes and implications of discordant cases. Am J Clin Pathol 134:284–292. doi: 10.1309/ AJCPUQB18XZOHHBJ10.1309/AJCPUQB18XZOHHBJ20660333Search in Google Scholar

[39] Paik S, Kim C, Wolmark N (2008) HER2 status and beneft from adjuvant trastuzumab in breast cancer. N Engl J Med 358:1409–1411. doi: 10.1056/ NEJMc0801440Search in Google Scholar

[40] Perez EA, Reinholz MM, Hillman DW, Tenner KS, Schroeder MJ, Davidson NE, Martino S, Sledge GW, Harris LN, Gralow JR, Dueck AC, Ketterling RP, Ingle JN, Lingle WL, Kaufman PA, Visscher DW, Jenkins RB (2010) HER2 and chromosome 17 effect on patient outcome in the N9831 adjuvant trastuzumab trial. J Clin Oncol 28:4307–4315. doi: 10.1200/JCO.2009.26.215410.1200/JCO.2009.26.2154295413220697084Search in Google Scholar

[41] Rossi V, Sarotto I, Maggiorotto F, Berchialla P, Kubatzki F, Tomasi N, Redana S, Martinello R, Valabrega G, Aglietta M, Ponzone R, Montemurro F (2012) Moderate immunohistochemical expression of HER-2 (2+) without HER-2 gene amplifcation is a negative prognostic factor in early breast cancer. Oncologist 17:1418–1425. doi: 10.1634/ theoncologist.2012-0194Search in Google Scholar

[42] Nitta H, Kelly BD, Padilla M, Wick N, Brunhoeber P, Bai I, Singh S, Ranger-Moore J, Bieniarz C, Tsuda H, Grogan TM (2012) A gene-protein assay for human epidermal growth factor receptor 2 (HER2): brightfeld tricolor visualization of HER2 protein, the HER2 gene, and chromosome 17 centromere (CEN17) in formalin-fxed, paraffn-embedded breast cancer tissue sections. Diagn Pathol 7:60-1596-7-60. doi: 10.1186/1746-1596-7-6010.1186/1746-1596-7-60348781022647525Search in Google Scholar