Surrogate End Points for Overall Survival in Neoadjuvant Randomized Clinical Trials for Early Breast Cancer

F Fabio Conforti (Division of Medical Oncology, Humanitas Gavazzeni, Bergamo, Italy) V Valentina Nekljudova (German Breast Group, Neu-Isenburg, Germany) I Isabella Sala (Fabio Conforti, MD, Division of Medical Oncology, Humanitas Gavazzeni, Bergamo, Italy, Humanitas University, Milan, Italy; Vincenzo Bagnardi, Department of Statistics and Quantitative Methods, University of Milano-Bicocca, Milan, Italy; and Isabella Sala, MSc, Humanitas University, Milan, Italy, Department of Medicine and Surgery, University of Milano-Bicocca, Milan, Italy) R Roberto Ascari (Department of Economics, Management and Statistics, University of Milano-Bicocca, Milan, Italy) C Christine Solbach (University Hospital Frankfurt, Frankfurt, Germany) M Michael Untch (From the National Surgical Adjuvant Breast and Bowel Project (NSABP) Foundation (C.E.G., E.P.M., N.W., P.R., I.L.W., A.M.B.) and University of Pittsburgh School of Medicine–UPMC Hillman Cancer Center (C.E.G., N.W., P.R., A.M.B.) — both in Pittsburgh; AGO-B and Helios Klinikum Berlin–Buch, Berlin (M.U.), the National Center for Tumor Diseases, Heidelberg University Hospital, and German Cancer Research Center, Heidelberg (A.S.), Evangelische Kliniken Gelsenkirchen, Gelsenkirchen (H.H.F.), Arbeitsgemeinschaft Gynäkologische Onkologie–Breast and Sana Klinikum Offenbach, Offenbach (C.J.), the Department of Gynecology and Obstetrics, University Hospital Erlangen, Comprehensive Cancer Center Erlangen–EMN, Friedrich–Alexander University Erlangen–Nuremberg, Erlangen (P.A.F.), German Breast Group, Neu-Isenburg (P.W., S.L.), and the Center for Hematology and Oncology Bethanien, Goethe University, Frankfurt (S.L.) — all in Germany; National Taiwan University Hospital and National Taiwan University College of Medicine,...) C Carsten Denkert (Institute of Pathology, Philipps University Marburg and University Hospital Marburg (UKGM), Marburg, Germany) V Vincenzo Bagnardi (Department of Statistics and Quantitative Methods, University of Milano-Bicocca, Milan, Italy) L Laura Pala (Humanitas University, Milan, Italy) P Peter A. Fasching A Andreas Schneeweiss (National Center for Tumor Diseases, University Hospital and German Cancer Research Center, Heidelberg, Germany) H Hans-Joachim Lück (Gynäkologisch-onkologische Praxis Neumarkt, Neumarkt in der Oberpfalz, Germany) E Eleonora Pagan (Department of Statistics and Quantitative Methods, University of Milano-Bicocca, Milan, Italy) T Tommaso De Pas (Humanitas University, Milan, Italy) M Marion van Mackelenbergh (Universitätsklinikum Schleswig-Holstein, Klinik für Gynäkologie und Geburtshilfe, Schleswig-Holstein, Germany) J Jens Huober (Breast Center, Kantonsspital St Gallen, St Gallen, Switzerland) V Volkmar Müller T Theresa Link (Department of Gynecology and Obstetrics, Medical Faculty and University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany) T Thomas Karn (Klinik für Frauenheilkunde und Geburtshilfe, Universitätsklinikum Frankfurt, Frankfurt, Germany) M Mattea Reinisch (Breast Unit, University Medical Center Mannheim, University of Heidelberg, Mannheim, Germany) F Frederik Marmé (Faculty of Medicine Mannheim, Department of Obstetrics and Gynecology, University of Heidelberg, Mannheim, Germany) V Vesna Bjelic-Radisic (Department of Senology, Breast Center, Helios University Clinic Wuppertal, Wuppertal, Germany) C Christian Schem (Mammazentrum Hamburg, Hamburg, Germany) A Andreas Hartkopf E Elmar Stickeler (University Hospital Aachen, Aachen, Germany) C Claus Hanusch (Rotkreuzklinikum München, München, Germany) J Jens-Uwe Blohmer (Gynäkologie mit Brustzentrum, Charité-Univesitätsmedizin Berlin, Berlin, Germany) T Tanja Fehm K Kerstin Rhiem J Johannes Holtschmidt (German Breast Group, Neu-Isenburg, Germany) R Richard D. Gelber (International Breast Cancer Study Group Statistical Center, Boston, MA) S Sibylle Loibl (Johann Wolfgang Goethe Universität, Frankfurt am Main, Germany)

Abstract

PURPOSE To assess trial-level surrogacy value for overall survival (OS) of the pathologic complete response (pCR) and invasive disease-free survival (iDFS) in randomized clinical trials (RCTs) for early breast cancer (BC). METHODS Individual patient data of neoadjuvant RCTs with available data on pCR, iDFS, and OS were included in the analysis. We used the coefficient of determination R 2 from weighted linear regression models to quantify the association between treatment effects on OS and on the surrogate end points. RESULTS Eleven RCTs, for a total of 15 treatment comparisons and 12,247 patients, were included in the analysis. There was a weak association between hazard ratios (HRs) for OS and odds ratio of pCR overall ( R 2 , 0.07; 95% CI, 0.00 to 0.48), as well as in all the subgroups explored. Overall, the R 2 for the association between HR OS and HR iDFS was 0.46 (95% CI, 0.08 to 0.71), which is just below the cutoff of 0.5 for moderate surrogacy. In the majority of subgroups explored, the R 2 ranged from 0.5 to <0.7, while in hormone receptor–/human epidermal growth factor receptor 2– subtype, histologic grade 1-2 tumors, and lobular tumors, surrogacy was strong (ie, R 2 ≥0.7). The surrogacy value of iDFS for OS was affected by follow-up (FUP) length: R 2 substantially increased up to 36 months of FUP, with little further improvement after 48 months of FUP. CONCLUSION iDFS with sufficient FUP is an acceptable surrogate end point to confidently anticipate final OS results of neoadjuvant RCTs for early BC. This recommendation holds true across many subgroups, with the notable exception of HR+ disease. There is definite need to reassess whether OS is the optimal end point for treatment efficacy measurement in HR+ early BC.

Article Details

Volume / Issue Vol. 43, Issue 12
Published April 20, 2025
Pages 1441-1452
ISSN 0732-183X
Publisher Lippincott Williams & Wilkins

Journal Info

Journal of Clinical Oncology

Lippincott Williams & Wilkins

ISSN: 0732-183X Health Sciences

Authors (32)

F

Fabio Conforti

Division of Medical Oncology, Humanitas Gavazzeni, Bergamo, Italy

V

Valentina Nekljudova

German Breast Group, Neu-Isenburg, Germany

I

Isabella Sala

Fabio Conforti, MD, Division of Medical Oncology, Humanitas Gavazzeni, Bergamo, Italy, Humanitas University, Milan, Italy; Vincenzo Bagnardi, Department of Statistics and Quantitative Methods, University of Milano-Bicocca, Milan, Italy; and Isabella Sala, MSc, Humanitas University, Milan, Italy, Department of Medicine and Surgery, University of Milano-Bicocca, Milan, Italy

R

Roberto Ascari

Department of Economics, Management and Statistics, University of Milano-Bicocca, Milan, Italy

C

Christine Solbach

University Hospital Frankfurt, Frankfurt, Germany

M

Michael Untch

From the National Surgical Adjuvant Breast and Bowel Project (NSABP) Foundation (C.E.G., E.P.M., N.W., P.R., I.L.W., A.M.B.) and University of Pittsburgh School of Medicine–UPMC Hillman Cancer Center (C.E.G., N.W., P.R., A.M.B.) — both in Pittsburgh; AGO-B and Helios Klinikum Berlin–Buch, Berlin (M.U.), the National Center for Tumor Diseases, Heidelberg University Hospital, and German Cancer Research Center, Heidelberg (A.S.), Evangelische Kliniken Gelsenkirchen, Gelsenkirchen (H.H.F.), Arbeitsgemeinschaft Gynäkologische Onkologie–Breast and Sana Klinikum Offenbach, Offenbach (C.J.), the Department of Gynecology and Obstetrics, University Hospital Erlangen, Comprehensive Cancer Center Erlangen–EMN, Friedrich–Alexander University Erlangen–Nuremberg, Erlangen (P.A.F.), German Breast Group, Neu-Isenburg (P.W., S.L.), and the Center for Hematology and Oncology Bethanien, Goethe University, Frankfurt (S.L.) — all in Germany; National Taiwan University Hospital and National Taiwan University College of Medicine,...

C

Carsten Denkert

Institute of Pathology, Philipps University Marburg and University Hospital Marburg (UKGM), Marburg, Germany

V

Vincenzo Bagnardi

Department of Statistics and Quantitative Methods, University of Milano-Bicocca, Milan, Italy

L

Laura Pala

Humanitas University, Milan, Italy

P

Peter A. Fasching

A

Andreas Schneeweiss

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

H

Hans-Joachim Lück

Gynäkologisch-onkologische Praxis Neumarkt, Neumarkt in der Oberpfalz, Germany

E

Eleonora Pagan

Department of Statistics and Quantitative Methods, University of Milano-Bicocca, Milan, Italy

T

Tommaso De Pas

Humanitas University, Milan, Italy

M

Marion van Mackelenbergh

Universitätsklinikum Schleswig-Holstein, Klinik für Gynäkologie und Geburtshilfe, Schleswig-Holstein, Germany

J

Jens Huober

Breast Center, Kantonsspital St Gallen, St Gallen, Switzerland

V

Volkmar Müller

T

Theresa Link

Department of Gynecology and Obstetrics, Medical Faculty and University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden, Germany

T

Thomas Karn

Klinik für Frauenheilkunde und Geburtshilfe, Universitätsklinikum Frankfurt, Frankfurt, Germany

M

Mattea Reinisch

Breast Unit, University Medical Center Mannheim, University of Heidelberg, Mannheim, Germany

F

Frederik Marmé

Faculty of Medicine Mannheim, Department of Obstetrics and Gynecology, University of Heidelberg, Mannheim, Germany

V

Vesna Bjelic-Radisic

Department of Senology, Breast Center, Helios University Clinic Wuppertal, Wuppertal, Germany

C

Christian Schem

Mammazentrum Hamburg, Hamburg, Germany

A

Andreas Hartkopf

E

Elmar Stickeler

University Hospital Aachen, Aachen, Germany

C

Claus Hanusch

Rotkreuzklinikum München, München, Germany

J

Jens-Uwe Blohmer

Gynäkologie mit Brustzentrum, Charité-Univesitätsmedizin Berlin, Berlin, Germany

T

Tanja Fehm

K

Kerstin Rhiem

J

Johannes Holtschmidt

German Breast Group, Neu-Isenburg, Germany

R

Richard D. Gelber

International Breast Cancer Study Group Statistical Center, Boston, MA

S

Sibylle Loibl

Johann Wolfgang Goethe Universität, Frankfurt am Main, Germany