Advertisement

Utility of genomic platforms in treatment decisions in axilla-positive breast cancer

Published:August 04, 2022DOI:https://doi.org/10.1016/j.clbc.2022.07.014

      ABSTRACT

      Genomic platforms have proven to be more accurate as a prognostic tool than immunohistochemistry studies in patients with early, hormone receptor positive, HER 2 negative breast cancer and, in some cases, have also demonstrated predictive ability for chemotherapy benefit. They are now widely applied in node-negative disease, but their use in node-positive disease is more recent and more controversial, especially in premenopausal patients. In this article, we review the use of these tests in node-positive disease.

      Key words

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Clinical Breast Cancer
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      REFERENCES

        • Early Breast Cancer Trialists’ Collaborative Group (EBCTCG)
        Increasing the dose intensity of chemotherapy by more frequent administration or sequential scheduling: a patient-level meta-analysis of 37 298 women with early breast cancer in 26 randomised trials.
        Lancet Lond Engl. 2019; 393 (Apr 6): 1440-1452
        • Cortazar P
        • Zhang L
        • Untch M
        • Mehta K
        • Costantino JP
        • Wolmark N
        • et al.
        Pathological complete response and long-term clinical benefit in breast cancer: the CTNeoBC pooled analysis.
        Lancet Lond Engl. 2014; 384 (Jul 12): 164-172
        • Paik S
        • Shak S
        • Tang G
        • Kim C
        • Baker J
        • Cronin M
        • et al.
        A Multigene Assay to Predict Recurrence of Tamoxifen-Treated, Node-Negative Breast Cancer.
        N Engl J Med. 2004; 351 (Dec 30): 2817-2826
        • Kalinsky K
        • Barlow WE
        • Gralow JR
        • Meric-Bernstam F
        • Albain KS
        • Hayes DF
        • et al.
        21-Gene Assay to Inform Chemotherapy Benefit in Node-Positive Breast Cancer.
        N Engl J Med. 2021; 385 (Dec 16): 2336-2347
        • Dowsett M
        • Cuzick J
        • Wale C
        • Forbes J
        • Mallon EA
        • Salter J
        • et al.
        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.
        J Clin Oncol Off J Am Soc Clin Oncol. 2010; 28 (Apr 10): 1829-1834
        • Albain KS
        • Barlow WE
        • Shak S
        • Hortobagyi GN
        • Livingston RB
        • Yeh IT
        • et al.
        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.
        Lancet Oncol. 2010; 11 (Jan): 55-65
        • Natsuhara KH
        • Losk K
        • King TA
        • Lin NU
        • Camuso K
        • Golshan M
        • et al.
        Impact of Genomic Assay Testing and Clinical Factors on Chemotherapy Use After Implementation of Standardized Testing Criteria.
        The Oncologist. 2019; 24 (May): 595-602
        • Mamounas EP
        • Tang G
        • Paik S
        • Baehner FL
        • Liu Q
        • Jeong JH
        • et al.
        21-Gene Recurrence Score for prognosis and prediction of taxane benefit after adjuvant chemotherapy plus endocrine therapy: results from NSABP B-28/NRG Oncology.
        Breast Cancer Res Treat. 2018; 168 (Feb): 69-77
        • Penault-Llorca F
        • Filleron T
        • Asselain B
        • Baehner FL
        • Fumoleau P
        • Lacroix-Triki M
        • et al.
        The 21-gene Recurrence Score® assay predicts distant recurrence in lymph node-positive, hormone receptor-positive, breast cancer patients treated with adjuvant sequential epirubicin- and docetaxel-based or epirubicin-based chemotherapy (PACS-01 trial).
        BMC Cancer. 2018; 18 (May 4): 526
        • Goldstein LJ
        • Gray R
        • Badve S
        • Childs BH
        • Yoshizawa C
        • Rowley S
        • et al.
        Prognostic utility of the 21-gene assay in hormone receptor-positive operable breast cancer compared with classical clinicopathologic features.
        J Clin Oncol Off J Am Soc Clin Oncol. 2008; 26 (Sep 1): 4063-4071
        • Roberts MC
        • Miller DP
        • Shak S
        • Petkov VI.
        Breast cancer-specific survival in patients with lymph node-positive hormone receptor-positive invasive breast cancer and Oncotype DX Recurrence Score results in the SEER database.
        Breast Cancer Res Treat. 2017; 163 (Jun): 303-310
        • Stemmer SM
        • Steiner M
        • Rizel S
        • Geffen DB
        • Nisenbaum B
        • Peretz T
        • et al.
        Clinical outcomes in ER+ HER2 -node-positive breast cancer patients who were treated according to the Recurrence Score results: evidence from a large prospectively designed registry.
        NPJ Breast Cancer. 2017; 3: 32
        • Hortobagyi
        • hortobagyi GN
        • Shak S
        • Sledge Jr, GW
        • et al.
        Breast cancer specific mortality (BCSM) in patients (pts) with node-negative (N0) and node-positive breast cancer (BC) guided by the 21-gene assay: A SEER-genomic population-based study.
        San Antonio Breast Cancer Symposium. 2018; ([P3-11-02])
        • Petkov VI
        • Miller DP
        • Howlader N
        • Gliner N
        • Howe W
        • Schussler N
        • et al.
        Breast-cancer-specific mortality in patients treated based on the 21-gene assay: a SEER population-based study.
        NPJ Breast Cancer. 2016; 2: 16017
        • Wang M
        • Wu K
        • Zhang P
        • Zhang M
        • Ding A
        • Chen H.
        The Prognostic Significance of the Oncotype DX Recurrence Score in T1-2N1M0 Estrogen Receptor-Positive HER2-Negative Breast Cancer Based on the Prognostic Stage in the Updated AJCC 8th Edition.
        Ann Surg Oncol. 2019; 26 (May): 1227-1235
        • Sparano JA
        • Gray RJ
        • Makower DF
        • Pritchard KI
        • Albain KS
        • Hayes DF
        • et al.
        Adjuvant Chemotherapy Guided by a 21-Gene Expression Assay in Breast Cancer.
        N Engl J Med. 2018; 379 (Jul 12): 111-121
        • Parker JS
        • Mullins M
        • Cheang MCU
        • Leung S
        • Voduc D
        • Vickery T
        • et al.
        Supervised risk predictor of breast cancer based on intrinsic subtypes.
        J Clin Oncol Off J Am Soc Clin Oncol. 2009; 27 (Mar 10): 1160-1167
        • Mittempergher L
        • de Ronde JJ
        • Nieuwland M
        • Kerkhoven RM
        • Simon I
        • Rutgers EJT
        • et al.
        Gene expression profiles from formalin fixed paraffin embedded breast cancer tissue are largely comparable to fresh frozen matched tissue.
        PloS One. 2011; 6 (Feb 11): e17163
        • Mook S
        • Schmidt MK
        • Viale G
        • Pruneri G
        • Eekhout I
        • Floore A
        • et al.
        The 70-gene prognosis-signature predicts disease outcome in breast cancer patients with 1-3 positive lymph nodes in an independent validation study.
        Breast Cancer Res Treat. 2009; 116 (Jul): 295-302
        • Cardoso F
        • van't Veer LJ
        • Bogaerts J
        • Slaets L
        • Viale G
        • Delaloge S
        • et al.
        70-Gene Signature as an Aid to Treatment Decisions in Early-Stage Breast Cancer.
        N Engl J Med. 2016; 375 (Aug 25): 717-729
        • CARDOSO
        • Cardoso F
        • Lvt Veer
        • Poncet C
        • Cardozo JL
        • Delaloge S
        • Pierga J-Y
        • Vuylsteke P
        • Brain E
        • Viale G
        • Kuemmel S
        • Rubio IT
        • Zoppoli G
        • Thompson AM
        • Matos E
        • Zaman K
        • Hilbers F
        • Dudek-Perić A
        • Meulemans B
        • Piccart- Gebhart MJ
        • Rutgers EJ
        MINDACT: Longterm results of the large prospective trial testing the 70-gene signature MammaPrint as guidance for adjuvant chemotherapy in breast cancer patients.
        J Clin Oncol. 2020; 38: 506
        • Piccart M
        • van ’t Veer LJ
        • Poncet C
        • Cardozo JMNL
        • Delaloge S
        • Pierga JY
        • et al.
        70-gene signature as an aid for treatment decisions in early breast cancer: updated results of the phase 3 randomised MINDACT trial with an exploratory analysis by age.
        Lancet Oncol. 2021; 22 (Apr 1): 476-488
        • Tsai M
        • Lo S
        • Audeh W
        • Qamar R
        • Budway R
        • Levine E
        • et al.
        Association of 70-Gene Signature Assay Findings With Physicians’ Treatment Guidance for Patients With Early Breast Cancer Classified as Intermediate Risk by the 21-Gene Assay.
        JAMA Oncol. 2018; 4 (Jan 11)e173470
        • Krijgsman O
        • Roepman P
        • Zwart W
        • Carroll JS
        • Tian S
        • Snoo FAD
        • et al.
        A diagnostic gene profile for molecular subtyping of breast cancer associated with treatment response.
        Breast Cancer Res Treat. 2012; 133: 37-47
        • Mittempergher L
        • Delahaye L
        • Witteveen A
        • Spangler JB
        • Hassenmahomed F
        • Mee S
        • et al.
        MammaPrint and BluePrint Molecular Diagnostics using targeted RNA Next-Generation Sequencing technology.
        J Mol Diagn JMD. 2019;
        • Hanahan D
        • Weinberg RA.
        Hallmarks of Cancer: The Next Generation.
        Cell. 2011; 144 (Mar 4): 646-674
        • Haan JC
        • Bhaskaran R
        • Ellappalayam A
        • Bijl Y
        • Griffioen CJ
        • Lujinovic E
        • et al.
        MammaPrint and BluePrint comprehensively capture the cancer hallmarks in early-stage breast cancer patients.
        Genes Chromosomes Cancer. 2022; ([Internet]637736544000000000 [citedJul 11]; Available from)
        • Whitworth P
        • Stork-Sloots L
        • de Snoo FA
        • Richards P
        • Rotkis M
        • Beatty J
        • et al.
        Chemosensitivity predicted by BluePrint 80-gene functional subtype and MammaPrint in the Prospective Neoadjuvant Breast Registry Symphony Trial (NBRST).
        Ann Surg Oncol. 2014; 21 (Oct): 3261-3267
        • Ehsani S
        • Wisinski KB.
        Genomic Testing in the Management of Early-Stage Breast Cancer.
        J Clin Outcomes Manag JCOM. 2017; 24 (May): 229-238
        • Kwa M
        • Makris A
        • Esteva FJ.
        Clinical utility of gene-expression signatures in early stage breast cancer.
        Nat Rev Clin Oncol. 2017; 14 (Oct): 595-610
        • Markopoulos C
        • van de Velde C
        • Zarca D
        • Ozmen V
        • Masetti R.
        Clinical evidence supporting genomic tests in early breast cancer: Do all genomic tests provide the same information?.
        Eur J Surg Oncol J Eur Soc Surg Oncol Br Assoc Surg Oncol. 2017; 43 (May): 909-920
        • Ovcaricek T
        • Takac I
        • Matos E.
        Multigene expression signatures in early hormone receptor positive HER 2 negative breast cancer.
        Radiol Oncol. 2019; 53 (Sep 24): 285-292
        • Gnant M
        • Sestak I
        • Filipits M
        • Dowsett M
        • Balic M
        • Lopez-Knowles E
        • et al.
        Identifying clinically relevant prognostic subgroups of postmenopausal women with node-positive hormone receptor-positive early-stage breast cancer treated with endocrine therapy: a combined analysis of ABCSG-8 and ATAC using the PAM50 risk of recurrence score and intrinsic subtype.
        Ann Oncol Off J Eur Soc Med Oncol. 2015; 26 (Aug): 1685-1691
        • Makris A
        • Hughes-Davies L
        • MacPherson IR
        • Marshall A
        • Campbell AF
        • Bartlett J
        • et al.
        OPTIMA (Optimal Personalised Treatment of early breast cancer usIng Multi-parameter Analysis): A prospective trial to validate the predictive utility and cost-effectiveness of gene expression test-directed chemotherapy decisions.
        J Clin Oncol. 2016; 34 (May 20–TPS623): TPS623
        • FILIPITS MARTIN
        • Filipits Martin
        • Nielsen Torsten O.
        • Rudas Margaretha
        • Greil Richard
        • Stöger Herbert
        • Jakes Raimund
        • et al.
        The PAM50 Risk-of-Recurrence Score Predicts Risk for Late Distant Recurrence after Endocrine Therapy in Postmenopausal Women with Endocrine-Responsive Early Breast Cancer Clin Cancer.
        Res. 2022; 20: 1298-1305
        • Gnant M
        • Filipits M
        • Greil R
        • Stoeger H
        • Rudas M
        • Bago-Horvath Z
        • et al.
        Predicting distant recurrence in receptor-positive breast cancer patients with limited clinicopathological risk: using the PAM50 Risk of Recurrence score in 1478 postmenopausal patients of the ABCSG-8 trial treated with adjuvant endocrine therapy alone.
        Ann Oncol Off J Eur Soc Med Oncol. 2014; 25 (Feb): 339-345
        • Lænkholm AV
        • Jensen MB
        • Eriksen JO
        • Rasmussen BB
        • Knoop AS
        • Buckingham W
        • et al.
        PAM50 Risk of Recurrence Score Predicts 10-Year Distant Recurrence in a Comprehensive Danish Cohort of Postmenopausal Women Allocated to 5 Years of Endocrine Therapy for Hormone Receptor-Positive Early Breast Cancer.
        J Clin Oncol Off J Am Soc Clin Oncol. 2018; 36 (Mar 10): 735-740
        • Jensen MB
        • Lænkholm AV
        • Balslev E
        • Buckingham W
        • Ferree S
        • Glavicic V
        • et al.
        The Prosigna 50-gene profile and responsiveness to adjuvant anthracycline-based chemotherapy in high-risk breast cancer patients.
        NPJ Breast Cancer. 2020; 6 (Feb 26): 7
        • Dowsett M
        • Sestak I
        • Lopez-Knowles E
        • Sidhu K
        • Dunbier AK
        • Cowens JW
        • et al.
        Comparison of PAM50 risk of recurrence score with oncotype DX and IHC4 for predicting risk of distant recurrence after endocrine therapy.
        J Clin Oncol Off J Am Soc Clin Oncol. 2013; 31 (Aug 1): 2783-2790
        • Bartlett JMS
        • Bayani J
        • Marshall A
        • Dunn JA
        • Campbell A
        • Cunningham C
        • et al.
        Comparing Breast Cancer Multiparameter Tests in the OPTIMA Prelim Trial: No Test Is More Equal Than the Others.
        J Natl Cancer Inst. 2016; 108 (Sep)
        • Filipits M
        • Rudas M
        • Jakesz R
        • Dubsky P
        • Fitzal F
        • Singer CF
        • et al.
        A new molecular predictor of distant recurrence in ER-positive, HER2-negative breast cancer adds independent information to conventional clinical risk factors.
        Clin Cancer Res Off J Am Assoc Cancer Res. 2011; 17 (Sep 15): 6012-6020
        • Filipits M
        • Dubsky P
        • Rudas M
        • Greil R
        • Balic M
        • Bago-Horvath Z
        • et al.
        Prediction of Distant Recurrence Using EndoPredict Among Women with ER+, HER2- Node-Positive and Node-Negative Breast Cancer Treated with Endocrine Therapy Only.
        Clin Cancer Res Off J Am Assoc Cancer Res. 2019; 25 (Jul 1): 3865-3872
        • Sestak I
        • Buus R
        • Cuzick J
        • Dubsky P
        • Kronenwett R
        • Denkert C
        • et al.
        Comparison of the Performance of 6 Prognostic Signatures for Estrogen Receptor–Positive Breast Cancer.
        JAMA Oncol. 2018; 4 (Apr): 545-553
        • Martin M
        • Brase JC
        • Calvo L
        • Krappmann K
        • Ruiz-Borrego M
        • Fisch K
        • et al.
        Clinical validation of the EndoPredict test in node-positive, chemotherapy-treated ER+/HER2- breast cancer patients: results from the GEICAM 9906 trial.
        Breast Cancer Res BCR. 2014; 16 (Apr 12): R38
        • Sestak I
        • Filipits M
        • Buus R
        • Rudas M
        • Balic M
        • Knauer M
        • et al.
        Prognostic Value of EndoPredict in Women with Hormone Receptor–Positive, HER2-Negative Invasive Lobular Breast Cancer.
        Clin Cancer Res. 2020; 26 (Sep 1): 4682-4687
        • Soliman H
        • Flake DD
        • Magliocco A
        • Robson M
        • Schwartzberg L
        • Sharma P
        • et al.
        Predicting Expected Absolute Chemotherapy Treatment Benefit in Women With Early-Stage Breast Cancer Using EndoPredict, an Integrated 12-Gene Clinicomolecular Assay.
        JCO Precis Oncol. 2019; (Dec): 1-10
        • Puppe J
        • Seifert T
        • Eichler C
        • Pilch H
        • Mallmann P
        • Malter W.
        Genomic Signatures in Luminal Breast Cancer.
        Breast Care Basel Switz. 2020; 15 (Aug): 355-365
        • Liefers GJ
        • Noordhoek I
        • Treuner K
        • Putter H
        • Zhang Y
        • Meershoek – Klein Kranenbarg E
        • et al.
        Breast cancer index (BCI) predicts benefit of two-and-a-half versus five years of extended endocrine therapy in HR+ breast cancer patients treated in the ideal trial.
        J Clin Oncol. 2020; 38 (May 20–512): 512
        • sgroi
        • Sgroi D
        • Zhang Y
        • Schnabel CA.
        Comparative performance of Breast Cancer Index (BCIN+) and CTS5 in hormone receptor-positive (HR+) lymph node- positive (N+) breast cancer patients with one to three positive nodes (N1).
        J Clin Oncol. 2019; 37: 555https://doi.org/10.1200/JCO.2019.37.15_suppl.555
        • Bartlett
        • Bartlett J
        • Sgroi D
        • Treuner K
        • Zhang Y
        • Ahmed I
        • Piper T
        • et al.
        from Extended Endocrine Therapy in Breast Cancer Patients Treated in the Adjuvant Tamoxifen–To Offer More?(aTTom).
        Trial. 2019; 30: 1176-1183https://doi.org/10.1093/annonc/mdz289
        • Noordhoek I
        • Treuner K
        • Putter H
        • Zhang Y
        • Wong J
        • Meershoek-Klein Kranenbarg E
        • et al.
        Breast Cancer Index Predicts Extended Endocrine Benefit to Individualize Selection of Patients with HR+ Early-stage Breast Cancer for 10 Years of Endocrine Therapy.
        Clin Cancer Res Off J Am Assoc Cancer Res. 2021; 27 (Jan 1): 311-319
        • Sotiriou C
        • Wirapati P
        • Loi S
        • Harris A
        • Fox S
        • Smeds J
        • et al.
        Gene expression profiling in breast cancer: understanding the molecular basis of histologic grade to improve prognosis.
        J Natl Cancer Inst. 2006; 98 (Feb 15): 262-272
        • Filho OM
        • Ignatiadis M
        • Sotiriou C.
        Genomic Grade Index: An important tool for assessing breast cancer tumor grade and prognosis.
        Crit Rev Oncol Hematol. 2011; 77 (Jan 1): 20-29
        • Bertucci F
        • Finetti P
        • Roche H
        • Le Doussal JM
        • Marisa L
        • Martin AL
        • et al.
        Comparison of the prognostic value of genomic grade index, Ki67 expression and mitotic activity index in early node-positive breast cancer patients.
        Ann Oncol Off J Eur Soc Med Oncol. 2013; 24 (Mar): 625-632
        • Bartlett JMS
        • Christiansen J
        • Gustavson M
        • Rimm DL
        • Piper T
        • de Velde CJH van
        • et al.
        Validation of the IHC4 Breast Cancer Prognostic Algorithm Using Multiple Approaches on the Multinational TEAM Clinical Trial.
        Arch Pathol Lab Med. 2016; 140 (Jan 1): 66-74
        • Cheang MCU
        • Chia SK
        • Voduc D
        • Gao D
        • Leung S
        • Snider J
        • et al.
        Ki67 index, HER2 status, and prognosis of patients with luminal B breast cancer.
        J Natl Cancer Inst. 2009; 101 (May 20): 736-750
        • Cuzick J
        • Dowsett M
        • Pineda S
        • Wale C
        • Salter J
        • Quinn E
        • et al.
        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.
        J Clin Oncol Off J Am Soc Clin Oncol. 2011; 29 (Nov 10): 4273-4278
        • Nielsen TO
        • Parker JS
        • Leung S
        • Voduc D
        • Ebbert M
        • Vickery T
        • et al.
        A comparison of PAM50 intrinsic subtyping with immunohistochemistry and clinical prognostic factors in tamoxifen-treated estrogen receptor-positive breast cancer.
        Clin Cancer Res Off J Am Assoc Cancer Res. 2010; 16 (Nov 1): 5222-5232
        • Andre F
        • Ismaila N
        • Allison KH
        • Barlow WE
        • Collyar DE
        • Damodaran S
        • et al.
        Biomarkers for Adjuvant Endocrine and Chemotherapy in Early-Stage Breast Cancer: ASCO Guideline Update.
        J Clin Oncol. 2022; ([Internet]Apr 19 [cited 2022 Jul 3]; Available from)
        • Nitz U
        • Gluz O
        • Clemens M
        • Malter W
        • Reimer T
        • Nuding B
        • et al.
        West German Study PlanB Trial: Adjuvant Four Cycles of Epirubicin and Cyclophosphamide Plus Docetaxel Versus Six Cycles of Docetaxel and Cyclophosphamide in HER2-Negative Early Breast Cancer.
        J Clin Oncol Off J Am Soc Clin Oncol. 2019; 37 (Apr 1): 799-808
        • Gluz O
        • Nitz UA
        • Christgen M
        • Kates RE
        • Shak S
        • Clemens M
        • et al.
        West German Study Group Phase III PlanB Trial: First Prospective Outcome Data for the 21-Gene Recurrence Score Assay and Concordance of Prognostic Markers by Central and Local Pathology Assessment.
        J Clin Oncol Off J Am Soc Clin Oncol. 2016; 34 (Jul 10): 2341-2349
      1. NCCN Guidelines Version 4.
        2022