Systematically higher Ki67 scores on core biopsy samples compared to corresponding resection specimen in breast cancer: a multi-operator and multi-institutional study

Modern Pathology - Tập 35 - Trang 1362-1369 - 2022
Balazs Acs1,2,3, Samuel C.Y. Leung4, Kelley M. Kidwell5, Indu Arun6, Renaldas Augulis7, Sunil S. Badve8, Yalai Bai1, Anita L. Bane9, John M.S. Bartlett10,11, Jane Bayani10, Gilbert Bigras12, Annika Blank13,14, Henk Buikema15, Martin C. Chang16, Robin L. Dietz17, Andrew Dodson18, Susan Fineberg19, Cornelia M. Focke20, Dongxia Gao4, Allen M. Gown21
1Department of Pathology, Yale University School of Medicine, New Haven, CT USA.
2Department of Oncology and Pathology, Karolinska Institutet, Stockholm, Sweden
3Department of Clinical Pathology and Cancer Diagnostics, Karolinska University Hospital, Stockholm, Sweden
4University of British Columbia, Vancouver, BC, Canada
5Department of Biostatistics, School of Public Health, University of Michigan, Ann Arbor, MI, USA
6Tata Medical Center, Kolkata, West Bengal, India
7Vilnius University Faculty of Medicine and National Center of Pathology, Vilnius University Hospital Santaros Clinics, Vilnius, Lithuania
8Department of Pathology and Laboratory Medicine, Emory University School of Medicine, Atlanta, GA, USA
9Juravinski Hospital and Cancer Centre, McMaster University, Hamilton, ON, Canada
10Ontario Institute for Cancer Research, Toronto, ON, Canada
11Edinburgh Cancer Research Centre, Western General Hospital, Edinburgh, United Kingdom
12Department of Laboratory Medicine and Pathology, University of Alberta, Edmonton, AB, Canada
13Institute of Pathology, University of Bern, Bern, Switzerland
14Institute of Pathology, Triemli Hospital Zurich, Zurich, Switzerland
15University of Groningen, University Medical Center Groningen, Groningen, the Netherlands
16Department of Pathology & Laboratory Medicine, University of Vermont Medical Center, Burlington, VT, USA
17Department of Pathology, Olive View-UCLA Medical Center, Los Angeles, CA, USA
18UK NEQAS for Immunocytochemistry and In-Situ Hybridisation, London, United Kingdom
19Montefiore Medical Center and The Albert Einstein College of Medicine, Bronx, NY, USA
20Dietrich-Bonhoeffer Medical Center, Neubrandenburg, Mecklenburg-Vorpommern, Germany
21PhenoPath Laboratories, Seattle, WA, USA

Tài liệu tham khảo

Smith I, Robertson J, Kilburn L, Wilcox M, Evans A, Holcombe C, et al. Long-term outcome and prognostic value of Ki67 after perioperative endocrine therapy in postmenopausal women with hormone-sensitive early breast cancer (POETIC): an open-label multicentre parallel-group randomised phase 3 trial. Lancet Oncol 21, 1443–1454 (2020) Nielsen TO, Leung SCY, Rimm DL, Dodson A, Acs B, Badve S, et al. Assessment of Ki67 in breast cancer: updated recommendations from the International Ki67 in Breast Cancer Working Group. J Natl Cancer Inst 113, 808–819 (2020) Harris LN, Ismaila N, McShane LM, Andre F, Collyar DE, Gonzalez-Angulo AM, et al. Use of biomarkers to guide decisions on adjuvant systemic therapy for women with early-stage invasive breast cancer: American Society of Clinical Oncology Clinical Practice Guideline. J Clin Oncol 34, 1134–1150 (2016) Andre F, Ismaila N, Henry NL, Somerfield MR, Bast RC, Barlow W, et al. Use of biomarkers to guide decisions on adjuvant systemic therapy for women with early-stage invasive breast cancer: ASCO Clinical Practice Guideline Update-Integration of Results From TAILORx. J Clin Oncol 37, 1956–1964 (2019) Acs B, Fredriksson I, Rönnlund C, Hagerling C, Ehinger A, Kovács A, et al. Variability in breast cancer biomarker assessment and the effect on oncological treatment decisions: a nationwide 5-year population-based study. Cancers (Basel) 13, 1166 (2021) Dowsett M, Nielsen TO, A'Hern R, Bartlett J, Coombes RC, Cuzick J, et al. Assessment of ki67 in breast cancer: recommendations from the international ki67 in breast cancer working group. J Natl Cancer Inst 103, 1656–1664 (2011) Polley MY, Leung SC, McShane LM, Gao D, Hugh JC, Mastropasqua MG, et al. An international Ki67 reproducibility study. J Natl Cancer Inst 105, 1897–1906 (2013) Polley MY, Leung SC, Gao D, Mastropasqua MG, Zabaglo LA, Bartlett JM, et al. An international study to increase concordance in Ki67 scoring. Mod Pathol 28, 778–786 (2015) Leung SCY, Nielsen TO, Zabaglo L, Arun I, Badve SS, Bane AL, et al. Analytical validation of a standardized scoring protocol for Ki67: phase 3 of an international multicenter collaboration. NPJ Breast Cancer 2, 16014 (2016) Leung SCY, Nielsen TO, Zabaglo LA, Arun I, Badve SS, Bane AL, et al. Analytical validation of a standardised scoring protocol for Ki67 immunohistochemistry on breast cancer excision whole sections: an international multicentre collaboration. Histopathology 75, 225–235 (2019) Bankhead P, Loughrey MB, Fernandez JA, Dombrowski Y, McArt DG, Dunne PD, et al. QuPath: Open source software for digital pathology image analysis. Sci Rep 7, 16878 (2017) Acs B, Pelekanou V, Bai Y, Martinez-Morilla S, Toki M, Leung SCY, et al. Ki67 reproducibility using digital image analysis: an inter-platform and inter-operator study. Lab Invest 99, 107–117 (2019) Aung TN, Acs B, Warrell J, Bai Y, Gaule P, Martinez-Morilla S, et al. A new tool for technical standardization of the Ki67 immunohistochemical assay. Mod Pathol 34, 1261–1270 (2021) Malpica N, de Solorzano CO, Vaquero JJ, Santos A, Vallcorba I, Garcia-Sagredo JM, et al. Applying watershed algorithms to the segmentation of clustered nuclei. Cytometry 28, 289–297 (1997) Kos Z, Dabbs DJ. Biomarker assessment and molecular testing for prognostication in breast cancer. Histopathology 68, 70–85 (2016) Kayser K, Gortler J, Borkenfeld S, Kayser G. How to measure diagnosis-associated information in virtual slides. Diagn Pathol 6, Suppl 1 S9 (2011) Robertson S, Azizpour H, Smith K, Hartman J. Digital image analysis in breast pathology-from image processing techniques to artificial intelligence. Transl Res 194, 19–35 (2018) Wienert S, Heim D, Kotani M, Lindequist B, Stenzinger A, Ishii M, et al. CognitionMaster: an object-based image analysis framework. Diagn Pathol 8, 34 (2013) Laurinavicius A, Plancoulaine B, Laurinaviciene A, Herlin P, Meskauskas R, Baltrusaityte I, et al. A methodology to ensure and improve accuracy of Ki67 labelling index estimation by automated digital image analysis in breast cancer tissue. Breast Cancer Res 16, R35 (2014) Klauschen F, Wienert S, Schmitt WD, Loibl S, Gerber B, Blohmer JU, et al. Standardized Ki67 diagnostics using automated scoring-clinical validation in the gepartrio breast cancer study. Clin Cancer Res 21, 3651–3657 (2015) Stalhammar G, Fuentes Martinez N, Lippert M, Tobin N,P Molholm I, Kis L, et al. Digital image analysis outperforms manual biomarker assessment in breast cancer. Mod Pathol 29, 318–329 (2016) Acs B, Madaras L, Kovacs KA, Micsik T, Tokes AM, Gyorffy B, et al. Reproducibility and prognostic potential of Ki-67 proliferation index when comparing digital-image analysis with standard semi-quantitative evaluation in breast cancer. Pathol Oncol Res 24, 115–127 (2018) Zhong F, Bi R, Yu B, Yang F, Yang W, Shui R. A comparison of visual assessment and automated digital image analysis of Ki67 labeling index in breast cancer. PLoS One 11, e0150505 (2016) Stalhammar G, Robertson S, Wedlund L, Lippert M, Rantalainen M, Bergh J, et al. Digital image analysis of Ki67 in hot spots is superior to both manual Ki67 and mitotic counts in breast cancer. Histopathology 72, 974–989 (2018) Rimm DL, Leung SCY, McShane LM, Bai Y, Bane AL, Bartlett JMS, et al. An international multicenter study to evaluate reproducibility of automated scoring for assessment of Ki67 in breast cancer. Mod Pathol 32, 59–69 (2019) Robertson S, Acs B, Lippert M, Hartman J. Prognostic potential of automated Ki67 evaluation in breast cancer: different hot spot definitions versus true global score. Breast Cancer Res Treat 183, 161–175 (2020) Koopman T, Buikema HJ, Hollema H, de Bock GH, van der Vegt B. Digital image analysis of Ki67 proliferation index in breast cancer using virtual dual staining on whole tissue sections: clinical validation and inter-platform agreement. Breast Cancer Res Treat 169, 33–42 (2018) Plancoulaine B, Laurinaviciene A, Herlin P, Besusparis J, Meskauskas R, Baltrusaityte I, et al. A methodology for comprehensive breast cancer Ki67 labeling index with intra-tumor heterogeneity appraisal based on hexagonal tiling of digital image analysis data. Virchows Arch 467, 711–722 (2015) Arima N, Nishimura R, Osako T, Nishiyama Y, Fujisue M, Okumura Y, et al. The importance of tissue handling of surgically removed breast cancer for an accurate assessment of the Ki-67 index. J Clin Pathol 69, 255–259 (2016) Mengel M, von Wasielewski R, Wiese B, Rüdiger T, Müller-Hermelink HK, Kreipe H. Inter-laboratory and inter-observer reproducibility of immunohistochemical assessment of the Ki-67 labelling index in a large multi-centre trial. J Pathol 198, 292–299 (2002) Benini E, Rao S, Daidone MG, Pilotti S, Silvestrini R. Immunoreactivity to MIB-1 in breast cancer: methodological assessment and comparison with other proliferation indices. Cell Prolif 30, 107–115 (1997) Kalvala J, Parks RM, Green AR, Cheung KL. Concordance between core needle biopsy and surgical excision specimens for Ki-67 in breast cancer - a systematic review of the literature. Histopathology 80, 468–484 (2022) Janeva S, Parris TZ, Nasic S, De Lara S, Larsson K, Audisio RA, et al. Comparison of breast cancer surrogate subtyping using a closed-system RT-qPCR breast cancer assay and immunohistochemistry on 100 core needle biopsies with matching surgical specimens. BMC Cancer 21, 439 (2021). Greer LT, Rosman M, Mylander WC, Hooke J, Kovatich A, Sawyer K, et al. Does breast tumor heterogeneity necessitate further immunohistochemical staining on surgical specimens? J Am Coll Surg 216, 239–251 (2013) Chen X, Sun L, Mao Y, Zhu S, Wu J, Huang O, et al. Preoperative core needle biopsy is accurate in determining molecular subtypes in invasive breast cancer. BMC Cancer 13, 390 (2013) Chen X, Zhu S, Fei X, Garfield DH, Wu J, Huang O, et al. Surgery time interval and molecular subtype may influence Ki67 change after core needle biopsy in breast cancer patients. BMC Cancer 15, 822 (2015) Kalkman S, Bulte JP, Halilovic, A Bult P, van Diest PJ. Brief fixation does not hamper the reliability of Ki67 analysis in breast cancer core-needle biopsies: a double-centre study. Histopathology 66, 380–387 (2015) Al Nemer A. The performance of Ki-67 labeling index in different specimen categories of invasive ductal carcinoma of the breast using 2 scoring methods. Appl Immunohistochem Mol Morphol 25, 86–90 (2017) Pölcher M, Braun M, Tischitz M, Hamann M, Szeterlak N, Kriegmair A, et al. Concordance of the molecular subtype classification between core needle biopsy and surgical specimen in primary breast cancer. Arch Gynecol Obstet 304, 783–790 (2021) Liu M, Tang SX, Tsang JYS, Shi YJ, Ni YB, Law BKB, et al. Core needle biopsy as an alternative to whole section in IHC4 score assessment for breast cancer prognostication. J Clin Pathol 71, 1084–1089 (2018) You K, Park S, Ryu JM, Kim I, Lee SK, Yu J, et al. Comparison of core needle biopsy and surgical specimens in determining intrinsic biological subtypes of breast cancer with immunohistochemistry. J Breast Cancer 20, 297–303 (2017) Chen J, Wang Z, Lv Q, Du Z, Tan Q, Zhang D, et al. Comparison of core needle biopsy and excision specimens for the accurate evaluation of breast cancer molecular markers: a report of 1003 cases. Pathol Oncol Res 23, 769-775 (2017) Focke CM, Decker T, van Diest PJ. Reliability of the Ki67-labelling index in core needle biopsies of luminal breast cancers is unaffected by biopsy volume. Ann Surg Oncol 24, 1251–1257 (2017) Meattini I, Bicchierai G, Saieva C, De Benedetto D, Desideri I, Becherini C, et al. Impact of molecular subtypes classification concordance between preoperative core needle biopsy and surgical specimen on early breast cancer management: Single-institution experience and review of published literature. Eur J Surg Oncol 43, 642–648 (2017) Robertson S, Rönnlund C, de Boniface J, Hartman J. Re-testing of predictive biomarkers on surgical breast cancer specimens is clinically relevant. Breast Cancer Res Treat 174, 795–805 (2019) Clark BZ, Onisko A, Assylbekova B, Li X, Bhargava R, Dabbs DJ. Breast cancer global tumor biomarkers: a quality assurance study of intratumoral heterogeneity. Mod Pathol 32, 354–366 (2019) Ekholm M, Grabau D, Bendahl PO, Bergh J, Elmberger G, Olsson H, et al. Highly reproducible results of breast cancer biomarkers when analysed in accordance with national guidelines - a Swedish survey with central re-assessment. Acta Oncol 54, 1040–1048 (2015)