Spatial Immunephenotypes of Distant Metastases but not Matched Primary Urothelial Carcinomas Predict Response to Immune Checkpoint Inhibition.


Journal

European urology
ISSN: 1873-7560
Titre abrégé: Eur Urol
Pays: Switzerland
ID NLM: 7512719

Informations de publication

Date de publication:
02 2023
Historique:
received: 11 07 2022
revised: 03 10 2022
accepted: 18 10 2022
pubmed: 14 11 2022
medline: 1 2 2023
entrez: 13 11 2022
Statut: ppublish

Résumé

The value of programmed cell death ligand-1 (PD-L1) to predict durable responses to immune checkpoint inhibitors (ICIs) in metastatic urothelial carcinoma (mUC) is inconsistent. We hypothesize that the use of archived primary tumor material (PRIM) for PD-L1 testing in clinical trials not properly reflecting the metastatic disease status (MET) contributes to this clinical issue. To analyze the predictive and prognostic value of PD-L1, spatial immunephenotypes, and major histocompatibility complex class I (MHC-I) determined in patient-matched PRIM/MET. PD-L1, spatial immunephenotypes, and MHC-I were examined in 154 mUC patients with at least one available pretreatment MET (138 patient-matched PRIM/MET pairs). PD-L1, spatial immunephenotype, and MHC-I status of (patient-matched PRIM and) pretreatment MET were correlated with chemotherapy and ICI response and outcomes. Discordance rates in patient-matched PRIM/MET were 25/30%, 36%, and 49% for PD-L1 (CPS10/IC5%), immunephenotypes, and MHC-I (loss vs preserved), respectively. Correlations with chemotherapy and ICI responses were observed for immunephenotypes and MHC-I status determined in MET (not for PD-L1 alone), but not in PRIM. In case of ICIs, patients with cytotoxic tumor immune microenvironment (TIME) showed durable responses with disease control rates of 90% and a hazard ratio for disease progression/death of 0.05 (95% confidence interval: 0.01-0.65) versus patients with immunedepleted MET (disease control rate 29%). MET MHC-I status added an incremental value to predict durable ICI responses. Limitations include the partly retrospective design and the lack of MET multisampling on individual patient level. The TIME is subject to substantial dynamics during metastatic evolution. MET immunephenotypes and MHC-I statuses show promising potential to predict chemotherapy and durable ICI responses, while the PRIM TIME does not. Thus, future clinical trials should rather rely on pretreatment MET biopsies reflecting the current immunological disease state than on PRIM. Prediction of chemotherapy and responses to immune checkpoint inhibitors might be possible using representative pretreatment metastatic biopsies.

Sections du résumé

BACKGROUND
The value of programmed cell death ligand-1 (PD-L1) to predict durable responses to immune checkpoint inhibitors (ICIs) in metastatic urothelial carcinoma (mUC) is inconsistent. We hypothesize that the use of archived primary tumor material (PRIM) for PD-L1 testing in clinical trials not properly reflecting the metastatic disease status (MET) contributes to this clinical issue.
OBJECTIVE
To analyze the predictive and prognostic value of PD-L1, spatial immunephenotypes, and major histocompatibility complex class I (MHC-I) determined in patient-matched PRIM/MET.
DESIGN, SETTING, AND PARTICIPANTS
PD-L1, spatial immunephenotypes, and MHC-I were examined in 154 mUC patients with at least one available pretreatment MET (138 patient-matched PRIM/MET pairs).
OUTCOME MEASUREMENTS AND STATISTICAL ANALYSIS
PD-L1, spatial immunephenotype, and MHC-I status of (patient-matched PRIM and) pretreatment MET were correlated with chemotherapy and ICI response and outcomes.
RESULTS AND LIMITATIONS
Discordance rates in patient-matched PRIM/MET were 25/30%, 36%, and 49% for PD-L1 (CPS10/IC5%), immunephenotypes, and MHC-I (loss vs preserved), respectively. Correlations with chemotherapy and ICI responses were observed for immunephenotypes and MHC-I status determined in MET (not for PD-L1 alone), but not in PRIM. In case of ICIs, patients with cytotoxic tumor immune microenvironment (TIME) showed durable responses with disease control rates of 90% and a hazard ratio for disease progression/death of 0.05 (95% confidence interval: 0.01-0.65) versus patients with immunedepleted MET (disease control rate 29%). MET MHC-I status added an incremental value to predict durable ICI responses. Limitations include the partly retrospective design and the lack of MET multisampling on individual patient level.
CONCLUSIONS
The TIME is subject to substantial dynamics during metastatic evolution. MET immunephenotypes and MHC-I statuses show promising potential to predict chemotherapy and durable ICI responses, while the PRIM TIME does not. Thus, future clinical trials should rather rely on pretreatment MET biopsies reflecting the current immunological disease state than on PRIM.
PATIENT SUMMARY
Prediction of chemotherapy and responses to immune checkpoint inhibitors might be possible using representative pretreatment metastatic biopsies.

Identifiants

pubmed: 36372626
pii: S0302-2838(22)02774-9
doi: 10.1016/j.eururo.2022.10.020
pii:
doi:

Substances chimiques

Immune Checkpoint Inhibitors 0
B7-H1 Antigen 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

133-142

Commentaires et corrections

Type : CommentIn
Type : CommentIn

Informations de copyright

Copyright © 2022 The Author(s). Published by Elsevier B.V. All rights reserved.

Auteurs

Franziska Erlmeier (F)

Institute of Pathology, University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg (FAU), Erlangen, Germany; Comprehensive Cancer Center EMN, University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany; BRIDGE-Consortium Germany e.V, Mannheim, Germany; Institute of Pathology, Technical University Munich, Munich, Germany; Bayerisches Zentrum für Krebsforschung (BZKF), Bavaria, Germany.

Niklas Klümper (N)

Department of Urology and Pediatric Urology, University Medical Center Bonn (UKB), Bonn, Germany; Institute of Experimental Oncology, University Medical Center Bonn (UKB), Bonn, Germany; Center for Integrated Oncology, Aachen/Bonn/Cologne/Düsseldorf (CIO-ABCD), Germany.

Laura Landgraf (L)

Institute of Pathology, University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg (FAU), Erlangen, Germany; Comprehensive Cancer Center EMN, University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany; Bayerisches Zentrum für Krebsforschung (BZKF), Bavaria, Germany.

Pamela L Strissel (PL)

Institute of Pathology, University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg (FAU), Erlangen, Germany; Comprehensive Cancer Center EMN, University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany; BRIDGE-Consortium Germany e.V, Mannheim, Germany; Bayerisches Zentrum für Krebsforschung (BZKF), Bavaria, Germany; Department of Gynecology and Obstetrics, University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany.

Reiner Strick (R)

Comprehensive Cancer Center EMN, University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany; BRIDGE-Consortium Germany e.V, Mannheim, Germany; Bayerisches Zentrum für Krebsforschung (BZKF), Bavaria, Germany; Department of Gynecology and Obstetrics, University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany.

Danijel Sikic (D)

Comprehensive Cancer Center EMN, University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany; BRIDGE-Consortium Germany e.V, Mannheim, Germany; Bayerisches Zentrum für Krebsforschung (BZKF), Bavaria, Germany; Department of Urology and Pediatric Urology, University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany.

Helge Taubert (H)

Comprehensive Cancer Center EMN, University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany; BRIDGE-Consortium Germany e.V, Mannheim, Germany; Bayerisches Zentrum für Krebsforschung (BZKF), Bavaria, Germany; Department of Urology and Pediatric Urology, University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany.

Sven Wach (S)

Comprehensive Cancer Center EMN, University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany; BRIDGE-Consortium Germany e.V, Mannheim, Germany; Bayerisches Zentrum für Krebsforschung (BZKF), Bavaria, Germany; Department of Urology and Pediatric Urology, University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany.

Carol I Geppert (CI)

Institute of Pathology, University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg (FAU), Erlangen, Germany; Comprehensive Cancer Center EMN, University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany; Bayerisches Zentrum für Krebsforschung (BZKF), Bavaria, Germany.

Veronika Bahlinger (V)

Institute of Pathology, University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg (FAU), Erlangen, Germany; Comprehensive Cancer Center EMN, University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany; BRIDGE-Consortium Germany e.V, Mannheim, Germany; Bayerisches Zentrum für Krebsforschung (BZKF), Bavaria, Germany.

Johannes Breyer (J)

BRIDGE-Consortium Germany e.V, Mannheim, Germany; Bayerisches Zentrum für Krebsforschung (BZKF), Bavaria, Germany; Department of Urology, University of Regensburg, Caritas St. Josef, Regensburg, Germany.

Manuel Ritter (M)

BRIDGE-Consortium Germany e.V, Mannheim, Germany; Department of Urology and Pediatric Urology, University Medical Center Bonn (UKB), Bonn, Germany; Center for Integrated Oncology, Aachen/Bonn/Cologne/Düsseldorf (CIO-ABCD), Germany.

Christian Bolenz (C)

BRIDGE-Consortium Germany e.V, Mannheim, Germany; Department of Urology and Pediatric Urology, University Hospital Ulm, University of Ulm, Ulm, Germany.

Florian Roghmann (F)

BRIDGE-Consortium Germany e.V, Mannheim, Germany; Department of Urology, Marien Hospital, Ruhr-University Bochum, Herne, Germany.

Philipp Erben (P)

BRIDGE-Consortium Germany e.V, Mannheim, Germany; Department of Urology, University Hospital Mannheim, University of Heidelberg, Mannheim, Germany.

Kristina Schwamborn (K)

Institute of Pathology, Technical University Munich, Munich, Germany; Bayerisches Zentrum für Krebsforschung (BZKF), Bavaria, Germany.

Ralph M Wirtz (RM)

BRIDGE-Consortium Germany e.V, Mannheim, Germany; STRATIFYER Molecular Pathology, Cologne, Germany.

Thomas Horn (T)

Bayerisches Zentrum für Krebsforschung (BZKF), Bavaria, Germany; Department of Urology, Technical University Munich, Munich, Germany.

Bernd Wullich (B)

Comprehensive Cancer Center EMN, University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany; BRIDGE-Consortium Germany e.V, Mannheim, Germany; Bayerisches Zentrum für Krebsforschung (BZKF), Bavaria, Germany; Department of Urology and Pediatric Urology, University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany.

Michael Hölzel (M)

Institute of Experimental Oncology, University Medical Center Bonn (UKB), Bonn, Germany; Center for Integrated Oncology, Aachen/Bonn/Cologne/Düsseldorf (CIO-ABCD), Germany.

Arndt Hartmann (A)

Institute of Pathology, University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg (FAU), Erlangen, Germany; Comprehensive Cancer Center EMN, University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany; BRIDGE-Consortium Germany e.V, Mannheim, Germany; Bayerisches Zentrum für Krebsforschung (BZKF), Bavaria, Germany.

Jürgen E Gschwend (JE)

Bayerisches Zentrum für Krebsforschung (BZKF), Bavaria, Germany; Department of Urology, Technical University Munich, Munich, Germany.

Wilko Weichert (W)

Institute of Pathology, Technical University Munich, Munich, Germany; Bayerisches Zentrum für Krebsforschung (BZKF), Bavaria, Germany.

Markus Eckstein (M)

Institute of Pathology, University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg (FAU), Erlangen, Germany; Comprehensive Cancer Center EMN, University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany; BRIDGE-Consortium Germany e.V, Mannheim, Germany; Bayerisches Zentrum für Krebsforschung (BZKF), Bavaria, Germany. Electronic address: markus.eckstein@uk-erlangen.de.

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