Update Breast Cancer 2023 Part 1 – Early Stage Breast Cancer

Andreas D. Hartkopf; Tanja N. Fehm; Manfred Welslau; Volkmar Müller; Florian Schütz; Peter A. Fasching; Wolfgang Janni; Isabell Witzel; Christoph Thomssen; Milena Beierlein; Erik Belleville; Michael Untch; Marc Thill; Hans Tesch; Nina Ditsch; Michael P. Lux; Bahriye Aktas; Maggie Banys-Paluchowski; Cornelia Kolberg-Liedtke; Achim Wöckel; Hans-Christian Kolberg; Nadia Harbeck; Elmar Stickeler; Rupert Bartsch; Andreas Schneeweiss; Johannes Ettl; Rachel Würstlein; David Krug; Florin-Andrei Taran; Diana Lüftner

doi:10.1055/a-2074-0551

Geburtshilfe und Frauenheilkunde, Table of Contents

CC BY-NC-ND 4.0 · Geburtshilfe Frauenheilkd 2023; 83(06): 653-663
DOI: 10.1055/a-2074-0551

GebFra Science

Review

Update Breast Cancer 2023 Part 1 – Early Stage Breast Cancer

Article in several languages: English | deutsch

Andreas D. Hartkopf

¹Department of Gynecology and Obstetrics, Ulm University Hospital, Ulm, Germany (Ringgold ID: RIN27197)

,

Tanja N. Fehm

²Department of Gynecology and Obstetrics, University Hospital Düsseldorf, Düsseldorf, Germany

,

Manfred Welslau

³Onkologie Aschaffenburg, Aschaffenburg, Germany

,

Volkmar Müller

⁴Department of Gynecology, Hamburg-Eppendorf University Medical Center, Hamburg, Germany

,

Florian Schütz

⁵Gynäkologie und Geburtshilfe, Diakonissen-Stiftungs-Krankenhaus Speyer, Speyer, Germany (Ringgold ID: RIN123168)

,

Peter A. Fasching

⁶Erlangen University Hospital, Department of Gynecology and Obstetrics; Comprehensive Cancer Center Erlangen EMN, Friedrich-Alexander University Erlangen-Nuremberg, Erlangen, Germany (Ringgold ID: RIN207200)

,

Wolfgang Janni

¹Department of Gynecology and Obstetrics, Ulm University Hospital, Ulm, Germany (Ringgold ID: RIN27197)

,

Isabell Witzel

⁷Klinik für Gynäkologie, Universitätsspital Zürich, Zürich, Switzerland (Ringgold ID: RIN31005)

,

Christoph Thomssen

⁸Department of Gynaecology, Martin-Luther-University Halle-Wittenberg, Halle (Saale), Germany

,

Milena Beierlein

⁶Erlangen University Hospital, Department of Gynecology and Obstetrics; Comprehensive Cancer Center Erlangen EMN, Friedrich-Alexander University Erlangen-Nuremberg, Erlangen, Germany (Ringgold ID: RIN207200)

,

Erik Belleville

⁹ClinSol GmbH & Co KG, Würzburg, Germany

,

Michael Untch

¹⁰Clinic for Gynecology and Obstetrics, Breast Cancer Center, Gynecologic Oncology Center, Helios Klinikum Berlin Buch, Berlin, Germany (Ringgold ID: RIN62473)

,

Marc Thill

¹¹Department of Gynecology and Gynecological Oncology, Agaplesion Markus Krankenhaus, Frankfurt am Main, Germany (Ringgold ID: RIN84491)

,

Hans Tesch

¹²Oncology Practice at Bethanien Hospital, Frankfurt am Main, Germany

,

Nina Ditsch

¹³Department of Gynecology and Obstetrics, University Hospital Augsburg, Augsburg, Germany (Ringgold ID: RIN39694)

,

Michael P. Lux

¹⁴Klinik für Gynäkologie und Geburtshilfe, Frauenklinik St. Louise, Paderborn, St. Josefs-Krankenhaus, Salzkotten, St. Vincenz Krankenhaus GmbH, Paderborn, Germany

,

Bahriye Aktas

¹⁵Department of Gynecology, University of Leipzig Medical Center, Leipzig, Germany

,

Maggie Banys-Paluchowski

¹⁶Department of Gynecology and Obstetrics, University Hospital Schleswig-Holstein, Campus Lübeck, Lübeck, Germany

,

Cornelia Kolberg-Liedtke

¹⁷Department of Gynecology and Obstetrics, University Hospital Essen, Essen, Germany (Ringgold ID: RIN39081)

,

Achim Wöckel

¹⁸Department of Gynecology and Obstetrics, University Hospital Würzburg, Würzburg, Germany

,

Hans-Christian Kolberg

¹⁹Department of Gynecology and Obstetrics, Marienhospital Bottrop, Bottrop, Germany

,

Nadia Harbeck

²⁰Breast Center, Department of Gynecology and Obstetrics and CCC Munich LMU, LMU University Hospital, München, Germany

,

Elmar Stickeler

²¹Department of Obstetrics and Gynecology, Center for Integrated Oncology (CIO Aachen, Bonn, Cologne, Düsseldorf), University Hospital of RWTH Aachen, Aachen, Germany

,

Rupert Bartsch

²²Department of Medicine I, Division of Oncology, Medical University of Vienna, Vienna, Austria

,

Andreas Schneeweiss

²³National Center for Tumor Diseases, University Hospital and German Cancer Research Center, Heidelberg, Germany

,

Johannes Ettl

²⁴Klinik für Frauenheilkunde und Gynäkologie, Klinikum Kempten, Klinikverbund Allgäu, Kempten, Germany (Ringgold ID: RIN27663)

,

Rachel Würstlein

²⁰Breast Center, Department of Gynecology and Obstetrics and CCC Munich LMU, LMU University Hospital, München, Germany

,

David Krug

²⁵Klinik für Strahlentherapie, Universitätsklinkum Schleswig-Holstein, Campus Kiel, Kiel, Germany (Ringgold ID: RIN15056)

,

Florin-Andrei Taran

²⁶Department of Gynecology and Obstetrics, University Hospital Freiburg, Freiburg, Germany

,

Diana Lüftner

²⁷Medical University of Brandenburg Theodor-Fontane, Immanuel Hospital Märkische Schweiz, Buckow, Germany

› Author Affiliations

Abstract

With abemaciclib (monarchE study) and olaparib (OlympiA study) gaining approval in the adjuvant treatment setting, a significant change in the standard of care for patients with early stage breast cancer has been established for some time now. Accordingly, some diverse developments are slowly being transferred from the metastatic to the adjuvant treatment setting. Recently, there have also been positive reports of the NATALEE study.

Other clinical studies are currently investigating substances that are already established in the metastatic setting. These include, for example, the DESTINY Breast05 study with trastuzumab deruxtecan and the SASCIA study with sacituzumab govitecan.

In this review paper, we summarize and place in context the latest developments over the past months.

Keywords

breast cancer - early stage - adjuvant therapy - neoadjuvant therapy - endocrine therapy - biomarkers

Full Text

References

References/Literatur
1 Lopes Cardozo JMN, Andrulis IL, Bojesen SE. et al. Associations of a Breast Cancer Polygenic Risk Score With Tumor Characteristics and Survival. J Clin Oncol 2023; 41: 1849-1863
2 DeVries AA, Dennis J, Tyrer JP. et al. Copy Number Variants Are Ovarian Cancer Risk Alleles at Known and Novel Risk Loci. J Natl Cancer Inst 2022; 114: 1533-1544
3 Ruth KS, Day FR, Hussain J. et al. Genetic insights into biological mechanisms governing human ovarian ageing. Nature 2021; 596: 393-397
4 Kapoor PM, Mavaddat N, Choudhury PP. et al. Combined Associations of a Polygenic Risk Score and Classical Risk Factors With Breast Cancer Risk. J Natl Cancer Inst 2021; 113: 329-337
5 Dorling L, Carvalho S, Allen J. Breast Cancer Association Consortium. et al. Breast Cancer Risk Genes – Association Analysis in More than 113,000 Women. N Engl J Med 2021; 384: 428-439
6 Fachal L, Aschard H, Beesley J. et al. Fine-mapping of 150 breast cancer risk regions identifies 191 likely target genes. Nat Genet 2020;
7 Dorling L, Carvalho S, Allen J. et al. Breast cancer risks associated with missense variants in breast cancer susceptibility genes. Genome Med 2022; 14: 51
8 Vachon CM, Scott CG, Tamimi RM. et al. Joint association of mammographic density adjusted for age and body mass index and polygenic risk score with breast cancer risk. Breast Cancer Res 2019; 21: 68
9 Wu L, Shi W, Long J. et al. A transcriptome-wide association study of 229,000 women identifies new candidate susceptibility genes for breast cancer. Nat Genet 2018; 50: 968-978
10 Mavaddat N, Michailidou K, Dennis J. et al. Polygenic Risk Scores for Prediction of Breast Cancer and Breast Cancer Subtypes. Am J Hum Genet 2019; 104: 21-34
11 Milne RL, Kuchenbaecker KB, Michailidou K. et al. Identification of ten variants associated with risk of estrogen-receptor-negative breast cancer. Nat Genet 2017; 49: 1767-1778
12 Michailidou K, Lindstrom S, Dennis J. et al. Association analysis identifies 65 new breast cancer risk loci. Nature 2017; 551: 92-94
13 Day FR, Thompson DJ, Helgason H. et al. Genomic analyses identify hundreds of variants associated with age at menarche and support a role for puberty timing in cancer risk. Nat Genet 2017; 49: 834-841
14 Vachon CM, Pankratz VS, Scott CG. et al. The contributions of breast density and common genetic variation to breast cancer risk. J Natl Cancer Inst 2015; 107: dju397
15 Rudolph A, Fasching PA, Behrens S. et al. A comprehensive evaluation of interaction between genetic variants and use of menopausal hormone therapy on mammographic density. Breast Cancer Res 2015; 17: 110
16 Michailidou K, Beesley J, Lindstrom S. et al. Genome-wide association analysis of more than 120,000 individuals identifies 15 new susceptibility loci for breast cancer. Nat Genet 2015; 47: 373-380
17 Mavaddat N, Pharoah PD, Michailidou K. et al. Prediction of breast cancer risk based on profiling with common genetic variants. J Natl Cancer Inst 2015; 107: djv036
18 Day FR, Ruth KS, Thompson DJ. et al. Large-scale genomic analyses link reproductive aging to hypothalamic signaling, breast cancer susceptibility and BRCA1-mediated DNA repair. Nat Genet 2015; 47: 1294-1303
19 Pharoah PD, Tsai YY, Ramus SJ. et al. GWAS meta-analysis and replication identifies three new susceptibility loci for ovarian cancer. Nat Genet 2013; 45: 362-370
20 Michailidou K, Hall P, Gonzalez-Neira A. et al. Large-scale genotyping identifies 41 new loci associated with breast cancer risk. Nat Genet 2013; 45: 353-361
21 Garcia-Closas M, Couch FJ, Lindstrom S. et al. Genome-wide association studies identify four ER negative-specific breast cancer risk loci. Nat Genet 2013; 45: 392-398
22 Bojesen SE, Pooley KA, Johnatty SE. et al. Multiple independent variants at the TERT locus are associated with telomere length and risks of breast and ovarian cancer. Nat Genet 2013; 45: 371-384
23 Vachon CM, Scott CG, Fasching PA. et al. Common breast cancer susceptibility variants in LSP1 and RAD51L1 are associated with mammographic density measures that predict breast cancer risk. Cancer Epidemiol Biomarkers Prev 2012; 21: 1156-1166
24 Ghoussaini M, Fletcher O, Michailidou K. et al. Genome-wide association analysis identifies three new breast cancer susceptibility loci. Nat Genet 2012; 44: 312-318
25 Haiman CA, Chen GK, Vachon CM. et al. A common variant at the TERT-CLPTM1L locus is associated with estrogen receptor-negative breast cancer. Nat Genet 2011; 43: 1210-1214
26 Antoniou AC, Wang X, Fredericksen ZS. et al. A locus on 19p13 modifies risk of breast cancer in BRCA1 mutation carriers and is associated with hormone receptor-negative breast cancer in the general population. Nat Genet 2010; 42: 885-892
27 Wunderle M, Olmes G, Nabieva N. et al. Risk, Prediction and Prevention of Hereditary Breast Cancer – Large-Scale Genomic Studies in Times of Big and Smart Data. Geburtshilfe Frauenheilkd 2018; 78: 481-492
28 Chen H, Fan S, Stone J. et al. Genome-wide and transcriptome-wide association studies of mammographic density phenotypes reveal novel loci. Breast Cancer Res 2022; 24: 27
29 Lindstrom S, Thompson DJ, Paterson AD. et al. Genome-wide association study identifies multiple loci associated with both mammographic density and breast cancer risk. Nat Commun 2014; 5: 5303
30 Lindstrom S, Thompson DJ, Paterson AD. et al. Corrigendum: genome-wide association study identifies multiple loci associated with both mammographic density and breast cancer risk. Nat Commun 2015; 6: 8358
31 Rudolph A, Song M, Brook MN. et al. Joint associations of a polygenic risk score and environmental risk factors for breast cancer in the Breast Cancer Association Consortium. Int J Epidemiol 2018; 47: 526-536
32 Brouckaert O, Rudolph A, Laenen A. et al. Reproductive profiles and risk of breast cancer subtypes: a multi-center case-only study. Breast Cancer Res 2017; 19: 119
33 Barrdahl M, Rudolph A, Hopper JL. et al. Gene-environment interactions involving functional variants: Results from the Breast Cancer Association Consortium. Int J Cancer 2017; 141: 1830-1840
34 Ye ZF, Li S, Dite GS. et al. Weight is More Informative than Body Mass Index for Predicting Postmenopausal Breast Cancer Risk: Prospective Family Study Cohort (ProF-SC). Cancer Prev Res 2022; 15: 8
35 Pegington M, Harkness EF, Howell A. et al. Magnitude and attributed reasons for adult weight gain amongst women at increased risk of breast cancer. BMC Womens Health 2022; 22: 11
36 Niehoff NM, Terry MB, Bookwalter DB. et al. Air Pollution and Breast Cancer: An Examination of Modification By Underlying Familial Breast Cancer Risk. Cancer Epidemiol Biomarkers Prev 2022; 31: 422-429
37 Naaman SC, Shen S, Zeytinoglu M. et al. Obesity and Breast Cancer Risk: The Oncogenic Implications of Metabolic Dysregulation. J Clin Endocrinol Metab 2022; 107: 2154-2166
38 Kresovich JK, Xu ZL, O’Brien KM. et al. Blood DNA methylation profiles improve breast cancer prediction. Mol Oncol 2022; 16: 42-53
39 Geldhof V, de Rooij L, Sokol L. et al. Single cell atlas identifies lipid-processing and immunomodulatory endothelial cells in healthy and malignant breast. Nat Commun 2022; 13: 19
40 Smith SG, Sestak I, Morris MA. et al. The impact of body mass index on breast cancer incidence among women at increased risk: an observational study from the International Breast Intervention Studies. Breast Cancer Res Tr 2021; 188: 215-223
41 Oh H, Wild RA, Manson JE. et al. Obesity, Height, and Serum Androgen Metabolism among Postmenopausal Women in the Women’s Health Initiative Observational Study. Cancer Epidemiol Biomarkers Prev 2021; 30: 2018-2029
42 Mubarik S, Liu XX, Malik SS. et al. Evaluation of lifestyle risk factor differences in global patterns of breast cancer mortality and DALYs during 1990–2017 using hierarchical age-period-cohort analysis. Environ Sci Pollut Res 2021; 28: 49864-49876
43 Masala G, Palli D, Ermini I. et al. The DAMA25 Study: Feasibility of a Lifestyle Intervention Programme for Cancer Risk Reduction in Young Italian Women with Breast Cancer Family History. Int J Environ Res Public Health 2021; 18: 13
44 Lukasiewicz S, Czeczelewski M, Forma A. et al. Breast Cancer-Epidemiology, Risk Factors, Classification, Prognostic Markers, and Current Treatment Strategies-An Updated Review. Cancers 2021; 13: 30
45 Kapoor PM, Mavaddat N, Choudhury PP. et al. Combined Associations of a Polygenic Risk Score and Classical Risk Factors With Breast Cancer Risk. J Natl Cancer Inst 2021; 113: 329-337
46 Houghton LC, Howland RE, Wei Y. et al. The Steroid Metabolome and Breast Cancer Risk in Women with a Family History of Breast Cancer: The Novel Role of Adrenal Androgens and Glucocorticoids. Cancer Epidemiol Biomarkers Prev 2021; 30: 89-96
47 Daly AA, Rolph R, Cutress RI. et al. A Review of Modifiable Risk Factors in Young Women for the Prevention of Breast Cancer. Breast Cancer (Dove Med Press) 2021; 13: 241-257
48 Hopper JL, Dite GS, MacInnis RJ. et al. Age-specific breast cancer risk by body mass index and familial risk: prospective family study cohort (ProF-SC). Breast Cancer Res 2018; 20: 132
49 Bhardwaj P, Iyengar NM, Zahid H. et al. Obesity promotes breast epithelium DNA damage in women carrying a germline mutation in BRCA1 or BRCA2. Sci Transl Med 2023; 15: eade1857
50 Marra A, Gazzo A, Gupta A. et al. Mutational signature analysis reveals patterns of genomic instability linked to resistance to endocrine therapy (ET) +/- CDK 4/6 inhibition (CDK4/6i) in estrogen receptor-positive/HER2-negative (ER+/HER2-) metastatic breast cancer (MBC). Ann Oncol 2022; 33 (Suppl. 7) S88-S121
51 Barone I, Caruso A, Gelsomino L. et al. Obesity and endocrine therapy resistance in breast cancer: Mechanistic insights and perspectives. Obes Rev 2022; 23: e13358
52 Yadav S, Boddicker NJ, Na J. et al. Abstract GS4–04: Population-based estimates of contralateral breast cancer risk among carriers of germline pathogenic variants in ATM, BRCA1, BRCA2, CHEK2, and PALB2. San Antonio Breast Cancer Symposium 2022. Cancer Res 2023; 83 (Suppl. 5) GS4–04
53 Shimelis H, LaDuca H, Hu C. et al. Triple-Negative Breast Cancer Risk Genes Identified by Multigene Hereditary Cancer Panel Testing. J Natl Cancer Inst 2018; 110: 855-862
54 Hoyer J, Vasileiou G, Uebe S. et al. Addition of triple negativity of breast cancer as an indicator for germline mutations in predisposing genes increases sensitivity of clinical selection criteria. BMC Cancer 2018; 18: 926
55 Harbeck N, Rastogi P, Martin M. et al. Adjuvant abemaciclib combined with endocrine therapy for high-risk early breast cancer: updated efficacy and Ki-67 analysis from the monarchE study. Ann Oncol 2021; 32: 1571-1581
56 Johnston SRD, Harbeck N, Hegg R. et al. Abemaciclib Combined With Endocrine Therapy for the Adjuvant Treatment of HR+, HER2-, Node-Positive, High-Risk, Early Breast Cancer (monarchE). J Clin Oncol 2020; 38: 3987-3998
57 Johnston SRD, Toi M, O’Shaughnessy J. et al. Abemaciclib plus endocrine therapy for hormone receptor-positive, HER2-negative, node-positive, high-risk early breast cancer (monarchE): results from a preplanned interim analysis of a randomised, open-label, phase 3 trial. Lancet Oncol 2023; 24: 77-90
58 United States Food and Drug Administration (FDA). FDA expands early breast cancer indication for abemaciclib with endocrine therapy. 2023 Accessed April 03, 2023 at: https://www.fda.gov/drugs/resources-information-approved-drugs/fda-expands-early-breast-cancer-indication-abemaciclib-endocrine-therapy
59 Johnston SRD, Andre V. Abemaciclib plus endocrine therapy for hormone receptor-positive, HER2-negative, node-positive, high-risk, early breast cancer – Authors’ reply. Lancet Oncol 2023; 24: e104
60 Translational Research in Oncology. NATALEE (TRIO033) Phase III trial demonstrates ribociclib significantly reduces the risk of recurrence for patients with early breast cancer, at interim analysis. 2023 Accessed April 05, 2023 at: https://www.trioncology.org/news/natalee-trio033-phase-iii-trial-demonstrates-ribociclib-significantly-reduces-the-risk-of-recurrence-for-patients-with-early-breast-cancer-at-interim-analysis/
61 clinicaltrials.gov. NCT03701334. A Trial to Evaluate Efficacy and Safety of Ribociclib With Endocrine Therapy as Adjuvant Treatment in Patients With HR+/HER2− Early Breast Cancer (NATALEE). NIH US National Library of Medicine; 2018. Accessed November 07, 2020 at: https://clinicaltrials.gov/ct2/show/NCT03701334
62 Slamon DJ, Fasching PA, Patel R. et al. NATALEE: Phase III study of ribociclib (RIBO) + endocrine therapy (ET) as adjuvant treatment in hormone receptor–positive (HR+), human epidermal growth factor receptor 2–negative (HER2–) early breast cancer (EBC). J Clin Oncol 2019; 37: TPS597
63 Novartis. Novartis Kisqali® Phase III NATALEE trial meets primary endpoint at interim analysis demonstrating clinically meaningful benefit in broad population of patients with early breast cancer. 2023 Accessed April 03, 2023 at: https://www.novartis.com/news/media-releases/novartis-kisqali-phase-iii-natalee-trial-meets-primary-endpoint-interim-analysis-demonstrating-clinically-meaningful-benefit-broad-population-patients-early-breast-cancer
64 Fasching PA. Breast cancer in young women: do BRCA1 or BRCA2 mutations matter?. Lancet Oncol 2018; 19: 150-151
65 Copson ER, Maishman TC, Tapper WJ. et al. Germline BRCA mutation and outcome in young-onset breast cancer (POSH): a prospective cohort study. Lancet Oncol 2018; 19: 169-180
66 Partridge AH, Niman SM, Ruggeri M. et al. Abstract GS4–09: Pregnancy Outcome and Safety of Interrupting Therapy for women with endocrine responsIVE breast cancer: Primary Results from the POSITIVE Trial (IBCSG 48–14/BIG 8–13). San Antonio Breast Cancer Symposium 2022. Cancer Res 2023; 83 (Suppl. 5) GS4–09
67 Pagani O, Walley BA, Fleming GF. et al. Adjuvant Exemestane With Ovarian Suppression in Premenopausal Breast Cancer: Long-Term Follow-Up of the Combined TEXT and SOFT Trials. J Clin Oncol 2023; 41: 1376-1382
68 Geyer Jr. CE, Garber JE, Gelber RD. et al. Overall survival in the OlympiA phase III trial of adjuvant olaparib in patients with germline pathogenic variants in BRCA1/2 and high-risk, early breast cancer. Ann Oncol 2022; 33: 1250-1268
69 Tung NM, Robson ME, Ventz S. et al. TBCRC 048: Phase II Study of Olaparib for Metastatic Breast Cancer and Mutations in Homologous Recombination-Related Genes. J Clin Oncol 2020; 38: 4274-4282
70 Ngoi NYL, Tan DSP. The role of homologous recombination deficiency testing in ovarian cancer and its clinical implications: do we need it?. ESMO Open 2021; 6: 100144
71 Fasching PA, Link T, Hauke J. et al. Neoadjuvant paclitaxel/olaparib in comparison to paclitaxel/carboplatinum in patients with HER2-negative breast cancer and homologous recombination deficiency (GeparOLA study). Ann Oncol 2021; 32: 49-57
72 Fasching PA, Schmatloch S, Hauke J. et al. Neoadjuvant paclitaxel/olaparib in comparison to paclitaxel/carboplatinum in patients with HER2-negative early breast cancer and homologous recombination deficiency – long-term survival of the GeparOLA study. San Antonio Breast Cancer Symposium 2022. Cancer Res 2023; 83 (Suppl. 5) GS5–02
73 Sparano JA, Gray RJ, Makower DF. et al. Adjuvant Chemotherapy Guided by a 21-Gene Expression Assay in Breast Cancer. N Engl J Med 2018; 379: 111-121
74 Sparano JA, Gray RJ, Makower DF. et al. Prospective Validation of a 21-Gene Expression Assay in Breast Cancer. N Engl J Med 2015; 373: 2005-2014
75 Jonat W, Kaufmann M, Sauerbrei W. et al. Goserelin versus cyclophosphamide, methotrexate, and fluorouracil as adjuvant therapy in premenopausal patients with node-positive breast cancer: The Zoladex Early Breast Cancer Research Association Study. J Clin Oncol 2002; 20: 4628-4635
76 Ruddy KJ, Schaid DJ, Partridge AH. et al. Genetic predictors of chemotherapy-related amenorrhea in women with breast cancer. Fertil Steril 2019; 112: 731-739.e1
77 Walshe JM, Denduluri N, Swain SM. Amenorrhea in premenopausal women after adjuvant chemotherapy for breast cancer. J Clin Oncol 2006; 24: 5769-5779
78 Pagani O, O’Neill A, Castiglione M. et al. Prognostic impact of amenorrhoea after adjuvant chemotherapy in premenopausal breast cancer patients with axillary node involvement: results of the International Breast Cancer Study Group (IBCSG) Trial VI. Eur J Cancer 1998; 34: 632-640
79 Francis PA. Role of Ovarian Suppression in Early Premenopausal Breast Cancer. Hematol Oncol Clin North Am 2023; 37: 79-88
80 Sparano J, Gray RJ, Makower D. et al. Abstract GS1–05: Trial Assigning Individualized Options for Treatment (TAILORx): An update including 12-year event rates. San Antonio Breast Cancer Symposium 2022. Cancer Res 2023; 83 (Suppl. 5) GS1–05
81 Karadal B, Kim G, Sharma V. et al. Abstract GS1–02: Racial Disparity in Tumor Microenvironment and Outcomes in Residual Breast Cancer Treated with Neoadjuvant Chemotherapy. San Antonio Breast Cancer Symposium 2022. Cancer Res 2023; 83 (Suppl. 5) GS1–02
82 Roh-Johnson M, Bravo-Cordero JJ, Patsialou A. et al. Macrophage contact induces RhoA GTPase signaling to trigger tumor cell intravasation. Oncogene 2014; 33: 4203-4212
83 Wyckoff JB, Wang Y, Lin EY. et al. Direct visualization of macrophage-assisted tumor cell intravasation in mammary tumors. Cancer Res 2007; 67: 2649-2656
84 Harney AS, Arwert EN, Entenberg D. et al. Real-Time Imaging Reveals Local, Transient Vascular Permeability, and Tumor Cell Intravasation Stimulated by TIE2hi Macrophage-Derived VEGFA. Cancer Discov 2015; 5: 932-943
85 Robinson BD, Sica GL, Liu YF. et al. Tumor microenvironment of metastasis in human breast carcinoma: a potential prognostic marker linked to hematogenous dissemination. Clin Cancer Res 2009; 15: 2433-2441
86 Karagiannis GS, Condeelis JS, Oktay MH. Chemotherapy-induced metastasis: mechanisms and translational opportunities. Clin Exp Metastasis 2018; 35: 269-284
87 Rohan TE, Xue X, Lin HM. et al. Tumor microenvironment of metastasis and risk of distant metastasis of breast cancer. J Natl Cancer Inst 2014; 106: dju136
88 Sparano JA, Gray R, Oktay MH. et al. A metastasis biomarker (MetaSite Breast Score) is associated with distant recurrence in hormone receptor-positive, HER2-negative early-stage breast cancer. NPJ Breast Cancer 2017; 3: 42
89 Karagiannis GS, Pastoriza JM, Wang Y. et al. Neoadjuvant chemotherapy induces breast cancer metastasis through a TMEM-mediated mechanism. Sci Transl Med 2017; 9: eaan0026
90 DeMichele A, Yee D, Esserman L. Mechanisms of Resistance to Neoadjuvant Chemotherapy in Breast Cancer. N Engl J Med 2017; 377: 2287-2289