Journal Article
. 2013 Sep;14(11).
doi: 10.1016/S1470-2045(13)70387-5.

Prediction of late distant recurrence in patients with oestrogen-receptor-positive breast cancer: a prospective comparison of the breast-cancer index (BCI) assay, 21-gene recurrence score, and IHC4 in the TransATAC study population

Dennis C Sgroi 1 Ivana Sestak 2 Jack Cuzick 2 Yi Zhang 3 Catherine A Schnabel 3 Brock Schroeder 3 Mark G Erlander 3 Anita Dunbier 4 Kally Sidhu 5 Elena Lopez-Knowles 5 Paul E Goss 6 Mitch Dowsett 7 
Affiliations
  • PMID: 24035531
  •     30 References
  •     116 citations

Abstract

Background: Biomarkers to improve the risk-benefit of extended adjuvant endocrine therapy for late recurrence in patients with oestrogen-receptor-positive breast cancer would be clinically valuable. We compared the prognostic ability of the breast-cancer index (BCI) assay, 21-gene recurrence score (Oncotype DX), and an immunohistochemical prognostic model (IHC4) for both early and late recurrence in patients with oestrogen-receptor-positive, node-negative (N0) disease who took part in the Arimidex, Tamoxifen, Alone or in Combination (ATAC) clinical trial.

Methods: In this prospective comparison study, we obtained archival tumour blocks from the TransATAC tissue bank from all postmenopausal patients with oestrogen-receptor-positive breast cancer from whom the 21-gene recurrence score and IHC4 values had already been derived. We did BCI analysis in matched samples with sufficient residual RNA using two BCI models-cubic (BCI-C) and linear (BCI-L)-using previously validated cutoffs. We assessed prognostic ability of BCI for distant recurrence over 10 years (the primary endpoint) and compared it with that of the 21-gene recurrence score and IHC4. We also tested the ability of the assays to predict early (0-5 years) and late (5-10 years) distant recurrence. To assess the ability of the biomarkers to predict recurrence beyond standard clinicopathological variables, we calculated the change in the likelihood-ratio χ(2) (LR-Δχ(2)) from Cox proportional hazards models.

Findings: Suitable tissue was available from 665 patients with oestrogen-receptor-positive, N0 breast cancer for BCI analysis. The primary analysis showed significant differences in risk of distant recurrence over 10 years in the categorical BCI-C risk groups (p<0·0001) with 6·8% (95% CI 4·4-10·0) of patients in the low-risk group, 17·3% (12·0-24·7) in the intermediate group, and 22·2% (15·3-31·5) in the high-risk group having distant recurrence. The secondary analysis showed that BCI-L was a much stronger predictor for overall (0-10 year) distant recurrence compared with BCI-C (interquartile HR 2·30 [95% CI 1·62-3·27]; LR-Δχ(2)=22·69; p<0·0001). When compared with BCI-L, the 21-gene recurrence score was less predictive (HR 1·48 [95% CI 1·22-1·78]; LR-Δχ(2)=13·68; p=0·0002) and IHC4 was similar (HR 1·69 [95% CI 1·51-2·56]; LR-Δχ(2)=22·83; p<0·0001). All further analyses were done with the BCI-L model. In a multivariable analysis, all assays had significant prognostic ability for early distant recurrence (BCI-L HR 2·77 [95% CI 1·63-4·70], LR-Δχ(2)=15·42, p<0·0001; 21-gene recurrence score HR 1·80 [1·42-2·29], LR-Δχ(2)=18·48, p<0·0001; IHC4 HR 2·90 [2·01-4·18], LR-Δχ(2)=29·14, p<0·0001); however, only BCI-L was significant for late distant recurrence (BCI-L HR 1·95 [95% CI 1·22-3·14], LR-Δχ(2)=7·97, p=0·0048; 21-gene recurrence score HR 1·13 [0·82-1·56], LR-Δχ(2)=0·48, p=0·47; IHC4 HR 1·30 [0·88-1·94], LR-Δχ(2)=1·59, p=0·20).

Interpretation: BCI-L was the only significant prognostic test for risk of both early and late distant recurrence and identified two risk populations for each timeframe. It could help to identify patients at high risk for late distant recurrence who might benefit from extended endocrine or other therapy.

Funding: Avon Foundation, National Institutes of Health, Breast Cancer Foundation, US Department of Defense Breast Cancer Research Program, Susan G Komen for the Cure, Breakthrough Breast Cancer through the Mary-Jean Mitchell Green Foundation, AstraZeneca, Cancer Research UK, and the National Institute for Health Research Biomedical Research Centre at the Royal Marsden (London, UK).

A multigene assay to predict recurrence of tamoxifen-treated, node-negative breast cancer.
Soonmyung Paik, Steven Shak, +12 authors, Norman Wolmark.
N Engl J Med, 2004 Dec 14; 351(27). PMID: 15591335
Highly Cited.
Annual hazard rates of recurrence for breast cancer after primary therapy.
T Saphner, D C Tormey, R Gray.
J Clin Oncol, 1996 Oct 01; 14(10). PMID: 8874335
Highly Cited.
Effects of chemotherapy and hormonal therapy for early breast cancer on recurrence and 15-year survival: an overview of the randomised trials.
Early Breast Cancer Trialists' Collaborative Group (EBCTCG).
Lancet, 2005 May 17; 365(9472). PMID: 15894097
Highly Cited.
Estrogen-regulated genes predict survival in hormone receptor-positive breast cancers.
Daniel S Oh, Melissa A Troester, +6 authors, Charles M Perou.
J Clin Oncol, 2006 Mar 01; 24(11). PMID: 16505416
Highly Cited.
The HOXB13:IL17BR expression index is a prognostic factor in early-stage breast cancer.
Xiao-Jun Ma, Susan G Hilsenbeck, +6 authors, Mark G Erlander.
J Clin Oncol, 2006 Sep 30; 24(28). PMID: 17008703
Definition of clinically distinct molecular subtypes in estrogen receptor-positive breast carcinomas through genomic grade.
Sherene Loi, Benjamin Haibe-Kains, +14 authors, Christos Sotiriou.
J Clin Oncol, 2007 Apr 03; 25(10). PMID: 17401012
Highly Cited.
Long-term follow-up of the randomized Stockholm trial on adjuvant tamoxifen among postmenopausal patients with early stage breast cancer.
Lars E Rutqvist, Hemming Johansson, Stockholm Breast Cancer Study Group.
Acta Oncol, 2007 Apr 25; 46(2). PMID: 17453361
Strong time dependence of the 76-gene prognostic signature for node-negative breast cancer patients in the TRANSBIG multicenter independent validation series.
Christine Desmedt, Fanny Piette, +18 authors, TRANSBIG Consortium.
Clin Cancer Res, 2007 Jun 05; 13(11). PMID: 17545524
Highly Cited.
Effect of anastrozole and tamoxifen as adjuvant treatment for early-stage breast cancer: 100-month analysis of the ATAC trial.
Arimidex, Tamoxifen, Alone or in Combination (ATAC) Trialists' Group, John F Forbes, +4 authors, Michael Baum.
Lancet Oncol, 2007 Dec 18; 9(1). PMID: 18083636
Highly Cited.
A five-gene molecular grade index and HOXB13:IL17BR are complementary prognostic factors in early stage breast cancer.
Xiao-Jun Ma, Ranelle Salunga, +8 authors, Dennis Sgroi.
Clin Cancer Res, 2008 May 03; 14(9). PMID: 18451222
Biological processes associated with breast cancer clinical outcome depend on the molecular subtypes.
Christine Desmedt, Benjamin Haibe-Kains, +6 authors, Christos Sotiriou.
Clin Cancer Res, 2008 Aug 14; 14(16). PMID: 18698033
Highly Cited.
Residual risk of breast cancer recurrence 5 years after adjuvant therapy.
Abenaa M Brewster, Gabriel N Hortobagyi, +8 authors, Francisco J Esteva.
J Natl Cancer Inst, 2008 Aug 13; 100(16). PMID: 18695137    Free PMC article.
Highly Cited.
Meta-analysis of gene expression profiles in breast cancer: toward a unified understanding of breast cancer subtyping and prognosis signatures.
Pratyaksha Wirapati, Christos Sotiriou, +10 authors, Mauro Delorenzi.
Breast Cancer Res, 2008 Jul 30; 10(4). PMID: 18662380    Free PMC article.
Highly Cited.
Assessment of letrozole and tamoxifen alone and in sequence for postmenopausal women with steroid hormone receptor-positive breast cancer: the BIG 1-98 randomised clinical trial at 8·1 years median follow-up.
Meredith M Regan, Patrick Neven, +14 authors, International Breast Cancer Study Group (IBCSG).
Lancet Oncol, 2011 Oct 25; 12(12). PMID: 22018631    Free PMC article.
Highly Cited.
Prognostic value of a combined estrogen receptor, progesterone receptor, Ki-67, and human epidermal growth factor receptor 2 immunohistochemical score and comparison with the Genomic Health recurrence score in early breast cancer.
Jack Cuzick, Mitch Dowsett, +10 authors, John F Forbes.
J Clin Oncol, 2011 Oct 13; 29(32). PMID: 21990413
Highly Cited.
Assessment of Ki67 in breast cancer: recommendations from the International Ki67 in Breast Cancer working group.
Mitch Dowsett, Torsten O Nielsen, +19 authors, International Ki-67 in Breast Cancer Working Group.
J Natl Cancer Inst, 2011 Oct 01; 103(22). PMID: 21960707    Free PMC article.
Highly Cited.
Prediction of late disease recurrence and extended adjuvant letrozole benefit by the HOXB13/IL17BR biomarker.
Dennis C Sgroi, Erin Carney, +16 authors, Paul E Goss.
J Natl Cancer Inst, 2013 Jul 03; 105(14). PMID: 23812955    Free PMC article.
Breast cancer index identifies early-stage estrogen receptor-positive breast cancer patients at risk for early- and late-distant recurrence.
Yi Zhang, Catherine A Schnabel, +7 authors, Mark G Erlander.
Clin Cancer Res, 2013 Jun 13; 19(15). PMID: 23757354
Prognostic and predictive value of the 21-gene recurrence score assay in postmenopausal women with node-positive, oestrogen-receptor-positive breast cancer on chemotherapy: a retrospective analysis of a randomised trial.
Kathy S Albain, William E Barlow, +20 authors, Breast Cancer Intergroup of North America.
Lancet Oncol, 2009 Dec 17; 11(1). PMID: 20005174    Free PMC article.
Highly Cited.
Prediction of risk of distant recurrence using the 21-gene recurrence score in node-negative and node-positive postmenopausal patients with breast cancer treated with anastrozole or tamoxifen: a TransATAC study.
Mitch Dowsett, Jack Cuzick, +11 authors, Steven Shak.
J Clin Oncol, 2010 Mar 10; 28(11). PMID: 20212256
Highly Cited.
A comparison of PAM50 intrinsic subtyping with immunohistochemistry and clinical prognostic factors in tamoxifen-treated estrogen receptor-positive breast cancer.
Torsten O Nielsen, Joel S Parker, +12 authors, Matthew J Ellis.
Clin Cancer Res, 2010 Sep 15; 16(21). PMID: 20837693    Free PMC article.
Highly Cited.
Utility of oncotype DX risk estimates in clinically intermediate risk hormone receptor-positive, HER2-normal, grade II, lymph node-negative breast cancers.
Catherine M Kelly, Savitri Krishnamurthy, +4 authors, Lajos Pusztai.
Cancer, 2010 Jul 29; 116(22). PMID: 20665886
Effect of anastrozole and tamoxifen as adjuvant treatment for early-stage breast cancer: 10-year analysis of the ATAC trial.
Jack Cuzick, Ivana Sestak, +5 authors, ATAC/LATTE investigators.
Lancet Oncol, 2010 Nov 23; 11(12). PMID: 21087898
Highly Cited.
Prognostic utility of HOXB13:IL17BR and molecular grade index in early-stage breast cancer patients from the Stockholm trial.
P-L Jerevall, X-J Ma, +9 authors, O Stål.
Br J Cancer, 2011 May 12; 104(11). PMID: 21559019    Free PMC article.
Gene-expression profiles to predict distant metastasis of lymph-node-negative primary breast cancer.
Yixin Wang, Jan G M Klijn, +11 authors, John A Foekens.
Lancet, 2005 Feb 22; 365(9460). PMID: 15721472
Highly Cited.
Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications.
T Sørlie, C M Perou, +14 authors, A L Børresen-Dale.
Proc Natl Acad Sci U S A, 2001 Sep 13; 98(19). PMID: 11553815    Free PMC article.
Highly Cited.
Genetic heterogeneity of single disseminated tumour cells in minimal residual cancer.
Christoph A Klein, Thomas J F Blankenstein, +4 authors, Gert Riethmüller.
Lancet, 2002 Sep 21; 360(9334). PMID: 12241875
Highly Cited.
A gene-expression signature as a predictor of survival in breast cancer.
Marc J van de Vijver, Yudong D He, +18 authors, René Bernards.
N Engl J Med, 2002 Dec 20; 347(25). PMID: 12490681
Highly Cited.
From latent disseminated cells to overt metastasis: genetic analysis of systemic breast cancer progression.
Oleg Schmidt-Kittler, Thomas Ragg, +13 authors, Christoph A Klein.
Proc Natl Acad Sci U S A, 2003 Jun 17; 100(13). PMID: 12808139    Free PMC article.
Highly Cited.
A two-gene expression ratio predicts clinical outcome in breast cancer patients treated with tamoxifen.
Xiao-Jun Ma, Zuncai Wang, +27 authors, Dennis C Sgroi.
Cancer Cell, 2004 Jun 15; 5(6). PMID: 15193263
Highly Cited.
The EndoPredict score provides prognostic information on late distant metastases in ER+/HER2- breast cancer patients.
P Dubsky, J C Brase, +18 authors, Austrian Breast and Colorectal Cancer Study Group (ABCSG).
Br J Cancer, 2013 Oct 26; 109(12). PMID: 24157828    Free PMC article.
Highly Cited.
An unmet need: tailoring extended adjuvant endocrine therapy.
G Bianchini, L Gianni.
Br J Cancer, 2013 Nov 21; 109(12). PMID: 24253504    Free PMC article.
How do I recommend extended adjuvant hormonal therapy?
Amitkumar Mehta, John T Carpenter.
Curr Treat Options Oncol, 2013 Dec 18; 15(1). PMID: 24338340
Review.
Clinical validation of the EndoPredict test in node-positive, chemotherapy-treated ER+/HER2- breast cancer patients: results from the GEICAM 9906 trial.
Miguel Martin, Jan C Brase, +15 authors, Alvaro Rodriguez-Lescure.
Breast Cancer Res, 2014 Apr 15; 16(2). PMID: 24725534    Free PMC article.
Late recurrences in early breast cancer: for whom and how long is endocrine therapy beneficial?
Michael Knauer, Martin Filipits, Peter Dubsky.
Breast Care (Basel), 2014 Jun 20; 9(2). PMID: 24944551    Free PMC article.
Review.
Evaluation of the ability of adjuvant tamoxifen-benefit gene signatures to predict outcome of hormone-naive estrogen receptor-positive breast cancer patients treated with tamoxifen in the advanced setting.
Anieta M Sieuwerts, Maria B Lyng, +6 authors, Henrik J Ditzel.
Mol Oncol, 2014 Aug 02; 8(8). PMID: 25081647    Free PMC article.
Genome-based risk prediction for early stage breast cancer.
Christina Adaniel, Komal Jhaveri, Adriana Heguy, Francisco J Esteva.
Oncologist, 2014 Sep 05; 19(10). PMID: 25187476    Free PMC article.
Review.
Linking estrogen-induced apoptosis with decreases in mortality following long-term adjuvant tamoxifen therapy.
V Craig Jordan.
J Natl Cancer Inst, 2014 Oct 02; 106(11). PMID: 25269699    Free PMC article.
Time dependence of biomarkers: non-proportional effects of immunohistochemical panels predicting relapse risk in early breast cancer.
J Stephen, G Murray, +13 authors, J M S Bartlett.
Br J Cancer, 2014 Oct 15; 111(12). PMID: 25314051    Free PMC article.
Biology of breast cancer in young women.
Hatem A Azim, Ann H Partridge.
Breast Cancer Res, 2014 Dec 02; 16(4). PMID: 25436920    Free PMC article.
Highly Cited. Review.
Network-based approach to identify prognostic biomarkers for estrogen receptor-positive breast cancer treatment with tamoxifen.
Rong Liu, Cheng-Xian Guo, Hong-Hao Zhou.
Cancer Biol Ther, 2015 Mar 11; 16(2). PMID: 25756514    Free PMC article.
[Molecular pathology for breast cancer: Importance of the gene expression profile].
C Denkert, B M Pfitzner, B I Heppner, M Dietel.
Pathologe, 2015 Apr 04; 36(2). PMID: 25836324
Review.
Multigene prognostic tests in breast cancer: past, present, future.
Balázs Győrffy, Christos Hatzis, +3 authors, Lajos Pusztai.
Breast Cancer Res, 2015 Apr 08; 17. PMID: 25848861    Free PMC article.
Highly Cited. Review.
Markers for the identification of late breast cancer recurrence.
Ivana Sestak, Jack Cuzick.
Breast Cancer Res, 2015 Apr 08; 17. PMID: 25848913    Free PMC article.
Review.
Developing a new generation of breast cancer clinical gene expression tests.
Zuzana Kos, Torsten O Nielsen.
Breast Cancer Res, 2014 Jan 01; 16(4). PMID: 25928431    Free PMC article.
New breast cancer prognostic factors identified by computer-aided image analysis of HE stained histopathology images.
Jia-Mei Chen, Ai-Ping Qu, +7 authors, Yan Li.
Sci Rep, 2015 May 30; 5. PMID: 26022540    Free PMC article.
The UZ Leuven Policy for Extended Adjuvant Anti-estrogen Therapy in Women With Early Estrogen Receptor-Positive Breast Cancer.
Kathleen Van Asten, An Poppe, +4 authors, Patrick Neven.
Curr Treat Options Oncol, 2015 Jun 03; 16(7). PMID: 26031545
Review.
Effect of tumor size on breast cancer-specific survival stratified by joint hormone receptor status in a SEER population-based study.
Yi-Zi Zheng, Lei Wang, Xin Hu, Zhi-Ming Shao.
Oncotarget, 2015 Jun 04; 6(26). PMID: 26036636    Free PMC article.
High PD-L1 expression was associated with poor prognosis in 870 Chinese patients with breast cancer.
Tao Qin, Yin-duo Zeng, +11 authors, Shu-sen Wang.
Oncotarget, 2015 Sep 18; 6(32). PMID: 26378017    Free PMC article.
Highly Cited.
Prospective Validation of a 21-Gene Expression Assay in Breast Cancer.
Joseph A Sparano, Robert J Gray, +28 authors, George W Sledge.
N Engl J Med, 2015 Sep 29; 373(21). PMID: 26412349    Free PMC article.
Highly Cited.
Ki67/SATB1 ratio is an independent prognostic factor of overall survival in patients with early hormone receptor-positive invasive ductal breast carcinoma.
Arvydas Laurinavicius, Andrew R Green, +4 authors, Ian O Ellis.
Oncotarget, 2015 Oct 30; 6(38). PMID: 26512778    Free PMC article.
Prospective assessment of the decision-making impact of the Breast Cancer Index in recommending extended adjuvant endocrine therapy for patients with early-stage ER-positive breast cancer.
Tara Sanft, Bilge Aktas, +11 authors, Lajos Pusztai.
Breast Cancer Res Treat, 2015 Nov 19; 154(3). PMID: 26578401    Free PMC article.
A pooled analysis of post-diagnosis lifestyle factors in association with late estrogen-receptor-positive breast cancer prognosis.
Sarah Nechuta, Wendy Y Chen, +7 authors, Xiao Ou Shu.
Int J Cancer, 2015 Nov 26; 138(9). PMID: 26606746    Free PMC article.
Recommendations from the EGAPP Working Group: does the use of Oncotype DX tumor gene expression profiling to guide treatment decisions improve outcomes in patients with breast cancer?
Evaluation of Genomic Applications in Practice and Prevention (EGAPP) Working Group*.
Genet Med, 2015 Dec 19; 18(8). PMID: 26681310
FOXA1 expression affects the proliferation activity of luminal breast cancer stem cell populations.
Kana Tachi, Akira Shiraishi, +5 authors, Osamu Ohneda.
Cancer Sci, 2015 Dec 29; 107(3). PMID: 26708273    Free PMC article.
Assessment of the prognostic and predictive utility of the Breast Cancer Index (BCI): an NCIC CTG MA.14 study.
Dennis C Sgroi, Judy-Anne W Chapman, +10 authors, Michael Pollak.
Breast Cancer Res, 2016 Jan 06; 18(1). PMID: 26728744    Free PMC article.
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.
Lyndsay N Harris, Nofisat Ismaila, +11 authors, American Society of Clinical Oncology.
J Clin Oncol, 2016 Feb 10; 34(10). PMID: 26858339    Free PMC article.
Highly Cited. Review.
Digital image analysis outperforms manual biomarker assessment in breast cancer.
Gustav Stålhammar, Nelson Fuentes Martinez, +9 authors, Johan Hartman.
Mod Pathol, 2016 Feb 27; 29(4). PMID: 26916072
Identification and prioritization of candidate genes for symptom variability in breast cancer survivors based on disease characteristics at the cellular level.
Theresa A Koleck, Yvette P Conley.
Breast Cancer (Dove Med Press), 2016 Mar 30; 8. PMID: 27022301    Free PMC article.
Adjuvant endocrine therapy in premenopausal women with breast cancer.
Kunal C Kadakia, N Lynn Henry.
Clin Adv Hematol Oncol, 2016 Apr 09; 13(10). PMID: 27058571    Free PMC article.
Comparing Breast Cancer Multiparameter Tests in the OPTIMA Prelim Trial: No Test Is More Equal Than the Others.
John M S Bartlett, Jane Bayani, +18 authors, OPTIMA TMG.
J Natl Cancer Inst, 2016 May 01; 108(9). PMID: 27130929    Free PMC article.
Prognostic Impact of the Combination of Recurrence Score and Quantitative Estrogen Receptor Expression (ESR1) on Predicting Late Distant Recurrence Risk in Estrogen Receptor-Positive Breast Cancer After 5 Years of Tamoxifen: Results From NRG Oncology/National Surgical Adjuvant Breast and Bowel Project B-28 and B-14.
Norman Wolmark, Eleftherios P Mamounas, +6 authors, Soonmyung Paik.
J Clin Oncol, 2016 May 25; 34(20). PMID: 27217450    Free PMC article.
Factors associated with late recurrence after completion of 5-year adjuvant tamoxifen in estrogen receptor positive breast cancer.
Eun-Shin Lee, Wonshik Han, +9 authors, Eun Sook Lee.
BMC Cancer, 2016 Jul 09; 16. PMID: 27388210    Free PMC article.
Comparison of EndoPredict and EPclin With Oncotype DX Recurrence Score for Prediction of Risk of Distant Recurrence After Endocrine Therapy.
Richard Buus, Ivana Sestak, +7 authors, Mitch Dowsett.
J Natl Cancer Inst, 2016 Jul 13; 108(11). PMID: 27400969    Free PMC article.
Highly Cited.
Multiparametric Genomic Assays for Breast Cancer: Time for the Next Generation?
Adam M Brufsky, Nancy E Davidson.
Clin Cancer Res, 2016 Aug 16; 22(20). PMID: 27521446    Free PMC article.
How cancer cells dictate their microenvironment: present roles of extracellular vesicles.
Yutaka Naito, Yusuke Yoshioka, Yusuke Yamamoto, Takahiro Ochiya.
Cell Mol Life Sci, 2016 Sep 02; 74(4). PMID: 27582126    Free PMC article.
Review.
A combination of Nottingham prognostic index and IHC4 score predicts pathological complete response of neoadjuvant chemotherapy in estrogen receptor positive breast cancer.
Weige Tan, Wei Luo, +6 authors, Chang Gong.
Oncotarget, 2016 Nov 29; 7(52). PMID: 27894097    Free PMC article.
Hormonal Modulation of Breast Cancer Gene Expression: Implications for Intrinsic Subtyping in Premenopausal Women.
Sarah M Bernhardt, Pallave Dasari, +3 authors, Wendy V Ingman.
Front Oncol, 2016 Nov 30; 6. PMID: 27896218    Free PMC article.
Review.
Epsin Family Member 3 and Ribosome-Related Genes Are Associated with Late Metastasis in Estrogen Receptor-Positive Breast Cancer and Long-Term Survival in Non-Small Cell Lung Cancer Using a Genome-Wide Identification and Validation Strategy.
Birte Hellwig, Katrin Madjar, +11 authors, Jörg Rahnenführer.
PLoS One, 2016 Dec 08; 11(12). PMID: 27926932    Free PMC article.
Optimizing the Use of Gene Expression Profiling in Early-Stage Breast Cancer.
Hyun-Seok Kim, Christopher B Umbricht, +22 authors, Leslie Cope.
J Clin Oncol, 2016 Dec 22; 34(36). PMID: 27998227    Free PMC article.
Selecting postoperative adjuvant systemic therapy for early stage breast cancer: A critical assessment of commercially available gene expression assays.
David M Hyams, Eric Schuur, +7 authors, Aníbal Nuñez De Pierro.
J Surg Oncol, 2017 Feb 18; 115(6). PMID: 28211064    Free PMC article.
Review.
Is Completion Axillary Dissection Necessary for This Patient?
Sadullah Girgin, Atilla Soran, +2 authors, Gökhan Demir.
J Breast Health, 2014 Jan 01; 10(3). PMID: 28331668    Free PMC article.
A new molecular prognostic score for predicting the risk of distant metastasis in patients with HR+/HER2- early breast cancer.
Gyungyub Gong, Mi Jeong Kwon, +15 authors, Young Kee Shin.
Sci Rep, 2017 Mar 30; 7. PMID: 28350001    Free PMC article.
Towards decision-making using individualized risk estimates for personalized medicine: A systematic review of genomic classifiers of solid tumors.
Daniel M Trifiletti, Vanessa N Sturz, Timothy N Showalter, Jennifer M Lobo.
PLoS One, 2017 May 10; 12(5). PMID: 28486497    Free PMC article.
Systematic Review.
St. Gallen/Vienna 2017: A Brief Summary of the Consensus Discussion about Escalation and De-Escalation of Primary Breast Cancer Treatment.
Michael Gnant, Nadia Harbeck, Christoph Thomssen.
Breast Care (Basel), 2017 Jun 01; 12(2). PMID: 28559767    Free PMC article.
Highly Cited. Review.
Clinical utility of gene-expression signatures in early stage breast cancer.
Maryann Kwa, Andreas Makris, Francisco J Esteva.
Nat Rev Clin Oncol, 2017 Jun 01; 14(10). PMID: 28561071
Highly Cited. Review.
Clinical use of the Oncotype DX genomic test to guide treatment decisions for patients with invasive breast cancer.
Terri P McVeigh, Michael J Kerin.
Breast Cancer (Dove Med Press), 2017 Jun 16; 9. PMID: 28615971    Free PMC article.
Review.
Metastatic triple-negative breast cancer patient with TP53 tumor mutation experienced 11 months progression-free survival on bortezomib monotherapy without adverse events after ending standard treatments with grade 3 adverse events.
Tobias Meißner, Adam Mark, +12 authors, Michael Forster.
Cold Spring Harb Mol Case Stud, 2017 Jul 07; 3(4). PMID: 28679691    Free PMC article.
Internet tools to enhance breast cancer care.
Shlomit Strulov Shachar, Hyman B Muss.
NPJ Breast Cancer, 2016 Apr 27; 2. PMID: 28721377    Free PMC article.
Learning from big data: are we undertreating older women with high-risk breast cancer?
Joseph A Sparano, Hyman Muss.
NPJ Breast Cancer, 2017 Jul 20; 2. PMID: 28721380    Free PMC article.
Body mass index, waist-to-hip ratio and late outcomes: a report from the Shanghai Breast Cancer Survival Study.
Minlu Zhang, Hui Cai, +4 authors, Ying Zheng.
Sci Rep, 2017 Aug 03; 7(1). PMID: 28765555    Free PMC article.
How to Achieve Optimal Care in Early Breast Cancer with 'Less' or 'More' Treatment.
Giuseppe Curigliano.
Breast Care (Basel), 2017 Aug 09; 12(3). PMID: 28785179    Free PMC article.
Extended Adjuvant Endocrine Therapy in Hormone Receptor-Positive Early Breast Cancer.
Dara B Bracken-Clarke, Mairi W Lucas, Michaela J Higgins.
Breast Care (Basel), 2017 Aug 09; 12(3). PMID: 28785180    Free PMC article.
Review.
Identifying Biomarkers to Select Patients with Early Breast Cancer Suitable for Extended Adjuvant Endocrine Therapy.
Ivana Sestak.
Breast Care (Basel), 2017 Aug 09; 12(3). PMID: 28785181    Free PMC article.
Review.
Risk stratification with Breast Cancer Index for late distant recurrence in patients with clinically low-risk (T1N0) estrogen receptor-positive breast cancer.
Brock Schroeder, Yi Zhang, +4 authors, Catherine A Schnabel.
NPJ Breast Cancer, 2017 Aug 11; 3. PMID: 28795152    Free PMC article.
De-escalating and escalating treatments for early-stage breast cancer: the St. Gallen International Expert Consensus Conference on the Primary Therapy of Early Breast Cancer 2017.
G Curigliano, H J Burstein, +52 authors, B Xu.
Ann Oncol, 2017 Aug 26; 28(8). PMID: 28838210    Free PMC article.
Highly Cited.
Extended Adjuvant Endocrine Therapy for Postmenopausal Women: Treating Many to Benefit a Few.
Paula R Pohlmann, Claudine Isaacs.
J Natl Cancer Inst, 2017 Sep 20; 110(1). PMID: 28922782    Free PMC article.
Prognostic immune-related gene models for breast cancer: a pooled analysis.
Jianli Zhao, Ying Wang, +6 authors, Kai Chen.
Onco Targets Ther, 2017 Oct 06; 10. PMID: 28979134    Free PMC article.
ER-positive breast cancer patients with more than three positive nodes or grade 3 tumors are at high risk of late recurrence after 5-year adjuvant endocrine therapy.
Fangbin Song, Jianbing Zhang, +6 authors, Junming Xu.
Onco Targets Ther, 2017 Oct 19; 10. PMID: 29042797    Free PMC article.
Assessing the Clinical Benefit of Systemic Adjuvant Therapies for Early Breast Cancer.
Volker Möbus, Susanne Hell, Marcus Schmidt.
Geburtshilfe Frauenheilkd, 2017 Nov 03; 77(10). PMID: 29093601    Free PMC article.
20-Year Risks of Breast-Cancer Recurrence after Stopping Endocrine Therapy at 5 Years.
Hongchao Pan, Richard Gray, +9 authors, EBCTCG.
N Engl J Med, 2017 Nov 09; 377(19). PMID: 29117498    Free PMC article.
Highly Cited.
Prognostic value of PAM50 and risk of recurrence score in patients with early-stage breast cancer with long-term follow-up.
Hege O Ohnstad, Elin Borgen, +11 authors, Bjørn Naume.
Breast Cancer Res, 2017 Nov 16; 19(1). PMID: 29137653    Free PMC article.
Evaluation of applying IHC4 as a prognostic model in the translational study of Intergroup Exemestane Study (IES): PathIES.
M C U Cheang, J M Bliss, +13 authors, PathIES Sub-Committee.
Breast Cancer Res Treat, 2017 Nov 28; 168(1). PMID: 29177605    Free PMC article.
Endocrine Therapy for Early Breast Cancer: Updated Review.
Alexander Tremont, Jonathan Lu, John T Cole.
Ochsner J, 2017 Dec 13; 17(4). PMID: 29230126    Free PMC article.
Review.
Tumor Heterogeneity in Breast Cancer.
Gulisa Turashvili, Edi Brogi.
Front Med (Lausanne), 2017 Dec 26; 4. PMID: 29276709    Free PMC article.
Highly Cited. Review.
Cost Effectiveness of Gene Expression Profile Testing in Community Practice.
Young Chandler, Clyde B Schechter, +8 authors, Jeanne S Mandelblatt.
J Clin Oncol, 2018 Jan 09; 36(6). PMID: 29309250    Free PMC article.
Endocrine therapy and related issues in hormone receptor-positive early breast cancer: a roundtable discussion by the breast cancer therapy expert group (BCTEG).
Jame Abraham, Humberto Caldera, +11 authors, Chuck Vogel.
Breast Cancer Res Treat, 2018 Jan 21; 169(1). PMID: 29352368    Free PMC article.
Review.
Extended Adjuvant Aromatase Inhibitor Therapy in Post-Menopausal Women.
Stephen M Schleicher, Maura N Dickler.
Curr Breast Cancer Rep, 2018 Feb 06; 9(4). PMID: 29399271    Free PMC article.
Comparison of the Performance of 6 Prognostic Signatures for Estrogen Receptor-Positive Breast Cancer: A Secondary Analysis of a Randomized Clinical Trial.
Ivana Sestak, Richard Buus, +9 authors, Mitch Dowsett.
JAMA Oncol, 2018 Feb 17; 4(4). PMID: 29450494    Free PMC article.
Highly Cited.
Luminal A Breast Cancer and Molecular Assays: A Review.
Jennifer J Gao, Sandra M Swain.
Oncologist, 2018 Feb 24; 23(5). PMID: 29472313    Free PMC article.
Review.
Spotlight on the utility of the Oncotype DX® breast cancer assay.
Zhen Rong Siow, Richard H De Boer, Geoffrey J Lindeman, G Bruce Mann.
Int J Womens Health, 2018 Mar 06; 10. PMID: 29503586    Free PMC article.
Review.
Prognostic & predictive factors for planning adjuvant chemotherapy of early-stage breast cancer.
Onur Esbah, Berna Oksuzoglu.
Indian J Med Res, 2018 Mar 08; 146(5). PMID: 29512598    Free PMC article.
Review.
Integration of Clinical Variables for the Prediction of Late Distant Recurrence in Patients With Estrogen Receptor-Positive Breast Cancer Treated With 5 Years of Endocrine Therapy: CTS5.
Mitch Dowsett, Ivana Sestak, +5 authors, Jack Cuzick.
J Clin Oncol, 2018 Apr 21; 36(19). PMID: 29676944    Free PMC article.
Late distant recurrence of breast carcinoma and metastasis to the main bronchus and choroid: A case report.
Zhijie Luo, Qin Cai, +3 authors, Linzhu Zhai.
Medicine (Baltimore), 2018 May 17; 97(20). PMID: 29768356    Free PMC article.
Clinical application and utility of genomic assays in early-stage breast cancer: key lessons learned to date.
S K L Chia.
Curr Oncol, 2018 Jun 19; 25(Suppl 1). PMID: 29910655    Free PMC article.
Review.
Genomic Testing in the Management of Early-Stage Breast Cancer.
Sima Ehsani, Kari Braun Wisinski.
J Clin Outcomes Manag, 2017 May 01; 24(5). PMID: 30158821    Free PMC article.
Novel 18-gene signature for predicting relapse in ER-positive, HER2-negative breast cancer.
Richard Buus, Belinda Yeo, +7 authors, Mitch Dowsett.
Breast Cancer Res, 2018 Sep 06; 20(1). PMID: 30180877    Free PMC article.
An Update on Breast Cancer Multigene Prognostic Tests-Emergent Clinical Biomarkers.
André Filipe Vieira, Fernando Schmitt.
Front Med (Lausanne), 2018 Sep 21; 5. PMID: 30234119    Free PMC article.
Review.
Panoptic View of Prognostic Models for Personalized Breast Cancer Management.
Geetanjali Saini, Karuna Mittal, +3 authors, Ritu Aneja.
Cancers (Basel), 2019 Sep 11; 11(9). PMID: 31500225    Free PMC article.
Review.
Decision of Adjuvant Systemic Treatment in HR+ HER2- Early Invasive Breast Cancer: Which Biomarkers Could Help?
Marie Alexandre, Aurélie Maran-Gonzalez, +6 authors, Séverine Guiu.
Cancer Manag Res, 2019 Dec 19; 11. PMID: 31849525    Free PMC article.
Review.
Microarray and RNA in situ hybridization assay for recurrence risk markers of breast carcinoma and ductal carcinoma in situ: Evidence supporting the use of diverse pathways panels.
Mark Francis Evans, Pamela Mary Vacek, +3 authors, Donald Lee Weaver.
J Cell Biochem, 2019 Oct 09; 121(2). PMID: 31595577    Free PMC article.
Breast Cancer Index and prediction of benefit from extended endocrine therapy in breast cancer patients treated in the Adjuvant Tamoxifen-To Offer More? (aTTom) trial.
J M S Bartlett, D C Sgroi, +8 authors, D W Rea.
Ann Oncol, 2019 Sep 11; 30(11). PMID: 31504126    Free PMC article.
Endocrine-responsive lobular carcinoma of the breast: features associated with risk of late distant recurrence.
Fabio Conforti, Laura Pala, +12 authors, Aron Goldhirsch.
Breast Cancer Res, 2020 Jan 01; 21(1). PMID: 31888717    Free PMC article.
Evaluation of the 12-Gene Molecular Score and the 21-Gene Recurrence Score as Predictors of Response to Neo-adjuvant Chemotherapy in Estrogen Receptor-Positive, HER2-Negative Breast Cancer.
Hatem Soliman, Susanne Wagner, +9 authors, William Gradishar.
Ann Surg Oncol, 2020 Jan 08; 27(3). PMID: 31907749    Free PMC article.
Indications for prognostic gene expression profiling in early breast cancer.
Erin F Cobain, Daniel F Hayes.
Curr Treat Options Oncol, 2015 May 02; 16(5). PMID: 25929335
Review.
Association of Circulating Tumor Cells With Late Recurrence of Estrogen Receptor-Positive Breast Cancer: A Secondary Analysis of a Randomized Clinical Trial.
Joseph Sparano, Anne O'Neill, +5 authors, Kathy D Miller.
JAMA Oncol, 2018 Jul 29; 4(12). PMID: 30054636    Free PMC article.
Highly Cited.
Introduction of a New Staging System of Breast Cancer for Radiologists: An Emphasis on the Prognostic Stage.
Jieun Koh, Min Jung Kim.
Korean J Radiol, 2019 Jan 11; 20(1). PMID: 30627023    Free PMC article.
Dynamics of breast-cancer relapse reveal late-recurring ER-positive genomic subgroups.
Oscar M Rueda, Stephen-John Sammut, +21 authors, Christina Curtis.
Nature, 2019 Mar 15; 567(7748). PMID: 30867590    Free PMC article.
Highly Cited.
DEAD-box RNA Helicase 39 Promotes Invasiveness and Chemoresistance of ER-positive Breast Cancer.
Xiudi Wang, Peipei Li, +4 authors, Jiajin Lin.
J Cancer, 2020 Mar 21; 11(7). PMID: 32194796    Free PMC article.
Validation of CTS5 model in large-scale breast cancer population and the impact of menopausal and HER2 status on its prognostic value.
Changjun Wang, Chang Chen, +10 authors, Qiang Sun.
Sci Rep, 2020 Mar 15; 10(1). PMID: 32170181    Free PMC article.
Use of letrozole after aromatase inhibitor-based therapy in postmenopausal breast cancer (NRG Oncology/NSABP B-42): a randomised, double-blind, placebo-controlled, phase 3 trial.
Eleftherios P Mamounas, Hanna Bandos, +17 authors, Norman Wolmark.
Lancet Oncol, 2018 Dec 05; 20(1). PMID: 30509771    Free PMC article.
Absolute Improvements in Freedom From Distant Recurrence to Tailor Adjuvant Endocrine Therapies for Premenopausal Women: Results From TEXT and SOFT.
Olivia Pagani, Prudence A Francis, +13 authors, SOFT and TEXT Investigators and International Breast Cancer Study Group.
J Clin Oncol, 2019 Oct 17; 38(12). PMID: 31618131    Free PMC article.
MiR-891a-5p as a prognostic marker and therapeutic target for hormone receptor-positive breast cancer.
Zhiqiang Zhang, Lu Xu, +7 authors, Xiujuan Qu.
J Cancer, 2020 Apr 25; 11(13). PMID: 32328182    Free PMC article.
Precision Medicine and the Role of Biomarkers of Radiotherapy Response in Breast Cancer.
James Meehan, Mark Gray, +8 authors, Arran K Turnbull.
Front Oncol, 2020 May 12; 10. PMID: 32391281    Free PMC article.
Review.
Risk stratification in luminal-type breast cancer: Comparison of Ki-67 with EndoPredict test results.
Aurelia Noske, Sophie-Isabelle Anders, +6 authors, Evelyn Klein.
Breast, 2019 Dec 02; 49. PMID: 31786414    Free PMC article.
Computational approaches to support comparative analysis of multiparametric tests: Modelling versus Training.
John M S Bartlett, Jane Bayani, +8 authors, OPTIMA Trial Management Group.
PLoS One, 2020 Sep 04; 15(9). PMID: 32881987    Free PMC article.
A Pathology-Based Combined Model to Identify PAM50 Non-luminal Intrinsic Disease in Hormone Receptor-Positive HER2-Negative Breast Cancer.
Tomás Pascual, Miguel Martin, +21 authors, Aleix Prat.
Front Oncol, 2019 May 21; 9. PMID: 31106144    Free PMC article.
Gene Expression Assays for Early-Stage Hormone Receptor-Positive Breast Cancer: Understanding the Differences.
Ana Tablante Nunes, Deborah E Collyar, Lyndsay N Harris.
JNCI Cancer Spectr, 2017 Dec 11; 1(1). PMID: 31360834    Free PMC article.
Review.
Endocrine Therapy in Early Breast Cancer.
Katja Krauss, Elmar Stickeler.
Breast Care (Basel), 2020 Sep 29; 15(4). PMID: 32982643    Free PMC article.
Review.
Genomic Signatures in Luminal Breast Cancer.
Julian Puppe, Tabea Seifert, +3 authors, Wolfram Malter.
Breast Care (Basel), 2020 Sep 29; 15(4). PMID: 32982645    Free PMC article.
Review.
Considerations for feature selection using gene pairs and applications in large-scale dataset integration, novel oncogene discovery, and interpretable cancer screening.
Laura Moody, Hong Chen, Yuan-Xiang Pan.
BMC Med Genomics, 2020 Oct 23; 13(Suppl 10). PMID: 33087122    Free PMC article.
How to Predict Metastasis in Luminal Breast Cancer? Current Solutions and Future Prospects.
Sylwia Tabor, Małgorzata Szostakowska-Rodzos, Anna Fabisiewicz, Ewa A Grzybowska.
Int J Mol Sci, 2020 Nov 14; 21(21). PMID: 33182512    Free PMC article.
Review.
Identification and clinical validation of a multigene assay that interrogates the biology of cancer stem cells and predicts metastasis in breast cancer: A retrospective consecutive study.
Salvatore Pece, Davide Disalvatore, +8 authors, Pier Paolo Di Fiore.
EBioMedicine, 2019 Mar 09; 42. PMID: 30846393    Free PMC article.
Changes in Recurrence Score by neoadjuvant endocrine therapy of breast cancer and their prognostic implication.
Takayuki Ueno, Shigehira Saji, +11 authors, Masakazu Toi.
ESMO Open, 2019 Apr 10; 4(1). PMID: 30962956    Free PMC article.
Prediction of chemotherapy benefit by EndoPredict in patients with breast cancer who received adjuvant endocrine therapy plus chemotherapy or endocrine therapy alone.
Ivana Sestak, Miguel Martín, +12 authors, Michael Gnant.
Breast Cancer Res Treat, 2019 May 02; 176(2). PMID: 31041683    Free PMC article.
Impact of molecular subtypes on the prediction of distant recurrence in estrogen receptor (ER) positive, human epidermal growth factor receptor 2 (HER2) negative breast cancer upon five years of endocrine therapy.
Mark Laible, Kerstin Hartmann, +7 authors, Annette Ramaswamy.
BMC Cancer, 2019 Jul 17; 19(1). PMID: 31307414    Free PMC article.
Rapid Induction of the Unfolded Protein Response and Apoptosis by Estrogen Mimic TTC-352 for the Treatment of Endocrine-Resistant Breast Cancer.
Balkees Abderrahman, Philipp Y Maximov, +12 authors, V Craig Jordan.
Mol Cancer Ther, 2020 Nov 13; 20(1). PMID: 33177154    Free PMC article.
The clinical usefulness of the CTS5 in the prediction of late distant recurrence in postmenopausal women with estrogen receptor-positive early breast cancer.
Wakako Tajiri, Hideki Ijichi, +8 authors, Eriko Tokunaga.
Breast Cancer, 2020 Jul 01; 28(1). PMID: 32601800    Free PMC article.
Twenty-year risks of breast cancer-specific mortality for stage III breast cancer in the surveillance, epidemiology, and end results registry.
José P Leone, Bernardo A Leone, +7 authors, Nancy U Lin.
Breast Cancer Res Treat, 2021 Feb 17;. PMID: 33590387
Genomic Assays in Node Positive Breast Cancer Patients: A Review.
Maroun Bou Zerdan, Maryam Ibrahim, +2 authors, Hazem I Assi.
Front Oncol, 2021 Mar 06; 10. PMID: 33665165    Free PMC article.
Review.
Molecular Biomarkers for Contemporary Therapies in Hormone Receptor-Positive Breast Cancer.
Allegra Freelander, Lauren J Brown, +4 authors, Elgene Lim.
Genes (Basel), 2021 Mar 07; 12(2). PMID: 33671468    Free PMC article.
Review.
Advanced Approaches to Breast Cancer Classification and Diagnosis.
M Zubair, S Wang, N Ali.
Front Pharmacol, 2021 Mar 16; 11. PMID: 33716731    Free PMC article.
Review.
Clinical validity of clinical treatment score 5 (CTS5) for estimating risk of late recurrence in unselected, non-trial patients with early oestrogen receptor-positive breast cancer.
Juliet Richman, Alistair Ring, Mitch Dowsett, Ivana Sestak.
Breast Cancer Res Treat, 2020 Nov 23; 186(1). PMID: 33222093    Free PMC article.
Active behavior of triple-negative breast cancer with adipose tissue invasion: a single center and retrospective review.
Junzo Yamaguchi, Hiroki Moriuchi, +6 authors, Mikio Nakamura.
BMC Cancer, 2021 Apr 22; 21(1). PMID: 33879104    Free PMC article.
The bone microenvironment increases phenotypic plasticity of ER+ breast cancer cells.
Igor L Bado, Weijie Zhang, +23 authors, Xiang H-F Zhang.
Dev Cell, 2021 Apr 21; 56(8). PMID: 33878299    Free PMC article.
Factors associated with late risks of breast cancer-specific mortality in the SEER registry.
José P Leone, Carlos T Vallejo, +8 authors, Nancy U Lin.
Breast Cancer Res Treat, 2021 Apr 25;. PMID: 33893907