SPARC-positive macrophages are the superior prognostic factor in the microenvironment of diffuse large B-cell lymphoma and independent of MYC rearrangement and double-/triple-hit status.


Journal

Annals of oncology : official journal of the European Society for Medical Oncology
ISSN: 1569-8041
Titre abrégé: Ann Oncol
Pays: England
ID NLM: 9007735

Informations de publication

Date de publication:
11 2021
Historique:
received: 28 06 2021
revised: 04 08 2021
accepted: 16 08 2021
pubmed: 27 8 2021
medline: 29 10 2021
entrez: 26 8 2021
Statut: ppublish

Résumé

Diffuse large B-cell lymphoma (DLBCL) is a heterogeneous disease with respect to outcome. Features of the tumor microenvironment (TME) are associated with prognosis when assessed by gene expression profiling. However, it is uncertain whether assessment of the microenvironment can add prognostic information to the most relevant and clinically well-established molecular subgroups when analyzed by immunohistochemistry (IHC). We carried out a histopathologic analysis of biomarkers related to TME in a very large cohort (n = 455) of DLBCL treated in prospective trials and correlated with clinicopathologic and molecular data, including chromosomal rearrangements and gene expression profiles for cell-of-origin and TME. The content of PD1+, FoxP3+ and CD8+, as well as vessel density, was not associated with outcome. However, we found a low content of CD68+ macrophages to be associated with inferior progression-free survival (PFS) and overall survival (OS; P = 0.023 and 0.040, respectively) at both univariable and multivariable analyses, adjusted for the factors of the International Prognostic Index (IPI), MYC break and BCL2/MYC and BCL6/MYC double-hit status. The subgroup of PDL1+ macrophages was not associated with survival. Instead, secreted protein acidic and cysteine rich (SPARC)-positive macrophages were identified as the subtype of macrophages most associated with survival. SPARC-positive macrophages and stromal cells directly correlated with favorable PFS and OS (both, P[log rank] <0.001, P[trend] < 0.001). The association of SPARC with prognosis was independent of the factors of the IPI, MYC double-/triple-hit status, Bcl2/c-myc double expression, cell-of-origin subtype and a recently published gene expression signature [lymphoma-associated macrophage interaction signature (LAMIS)]. SPARC expression in the TME detected by a single IHC staining with fair-to-good interobserver reproducibility is a powerful prognostic parameter. Thus SPARC expression is a strong candidate for risk assessment in DLBCL in daily practice.

Sections du résumé

BACKGROUND
Diffuse large B-cell lymphoma (DLBCL) is a heterogeneous disease with respect to outcome. Features of the tumor microenvironment (TME) are associated with prognosis when assessed by gene expression profiling. However, it is uncertain whether assessment of the microenvironment can add prognostic information to the most relevant and clinically well-established molecular subgroups when analyzed by immunohistochemistry (IHC).
PATIENTS AND METHODS
We carried out a histopathologic analysis of biomarkers related to TME in a very large cohort (n = 455) of DLBCL treated in prospective trials and correlated with clinicopathologic and molecular data, including chromosomal rearrangements and gene expression profiles for cell-of-origin and TME.
RESULTS
The content of PD1+, FoxP3+ and CD8+, as well as vessel density, was not associated with outcome. However, we found a low content of CD68+ macrophages to be associated with inferior progression-free survival (PFS) and overall survival (OS; P = 0.023 and 0.040, respectively) at both univariable and multivariable analyses, adjusted for the factors of the International Prognostic Index (IPI), MYC break and BCL2/MYC and BCL6/MYC double-hit status. The subgroup of PDL1+ macrophages was not associated with survival. Instead, secreted protein acidic and cysteine rich (SPARC)-positive macrophages were identified as the subtype of macrophages most associated with survival. SPARC-positive macrophages and stromal cells directly correlated with favorable PFS and OS (both, P[log rank] <0.001, P[trend] < 0.001). The association of SPARC with prognosis was independent of the factors of the IPI, MYC double-/triple-hit status, Bcl2/c-myc double expression, cell-of-origin subtype and a recently published gene expression signature [lymphoma-associated macrophage interaction signature (LAMIS)].
CONCLUSIONS
SPARC expression in the TME detected by a single IHC staining with fair-to-good interobserver reproducibility is a powerful prognostic parameter. Thus SPARC expression is a strong candidate for risk assessment in DLBCL in daily practice.

Identifiants

pubmed: 34438040
pii: S0923-7534(21)04275-7
doi: 10.1016/j.annonc.2021.08.1991
pii:
doi:

Substances chimiques

MYC protein, human 0
Osteonectin 0
Proto-Oncogene Proteins c-bcl-2 0
Proto-Oncogene Proteins c-bcl-6 0
Proto-Oncogene Proteins c-myc 0
SPARC protein, human 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

1400-1409

Commentaires et corrections

Type : CommentIn

Informations de copyright

Copyright © 2021 European Society for Medical Oncology. Published by Elsevier Ltd. All rights reserved.

Déclaration de conflit d'intérêts

Disclosure GAC received travel support/congress support from Novartis (not related to work); VP received travel support/congress support from AbbVie, Amgen, BMS, Gilead and Roche (not related to work); WK received grants from Amgen, Regeneron, and Takeda (not related to work). All remaining authors have declared no conflicts of interest.

Auteurs

G A Croci (GA)

Institute of Pathology, Hematopathology Section and Lymph Node Registry, University Hospital Schleswig-Holstein, Campus Kiel, Kiel, Germany; Department of Pathophysiology and Transplantation, University of Milan, Milan, Italy; Division of Pathology, Fondazione IRCCS Ca' Granda Ospedale Maggiore Policlinico, Milan, Italy. Electronic address: giorgio.croci@unimi.it.

R K H Au-Yeung (RKH)

Institute of Pathology, Hematopathology Section and Lymph Node Registry, University Hospital Schleswig-Holstein, Campus Kiel, Kiel, Germany; Department of Pathology, Queen Mary Hospital, The University of Hong Kong, Hong Kong.

S Reinke (S)

Institute of Pathology, Hematopathology Section and Lymph Node Registry, University Hospital Schleswig-Holstein, Campus Kiel, Kiel, Germany.

A M Staiger (AM)

Department of Clinical Pathology, Robert-Bosch-Krankenhaus, Stuttgart, Germany; Dr. Margarete Fischer-Bosch Institute of Clinical Pharmacology, Stuttgart and University of Tuebingen, Tübingen, Germany.

K Koch (K)

Institute of Pathology, Hematopathology Section and Lymph Node Registry, University Hospital Schleswig-Holstein, Campus Kiel, Kiel, Germany.

I Oschlies (I)

Institute of Pathology, Hematopathology Section and Lymph Node Registry, University Hospital Schleswig-Holstein, Campus Kiel, Kiel, Germany.

J Richter (J)

Institute of Pathology, Hematopathology Section and Lymph Node Registry, University Hospital Schleswig-Holstein, Campus Kiel, Kiel, Germany.

V Poeschel (V)

Department of Internal Medicine 1 (Oncology, Hematology, Clinical Immunology, and Rheumatology), Saarland University Medical School, Homburg/Saar, Germany.

G Held (G)

DSHNHL Studiensekretariat, Universitätsklinikum des Saarlandes, Homburg, Germany.

M Loeffler (M)

Institute for Medical Informatics, Statistics and Epidemiology, University of Leipzig, Leipzig, Germany.

L Trümper (L)

Department of Hematology and Oncology, Georg-August Universität, Göttingen, Germany.

A Rosenwald (A)

Institute of Pathology, Universität Würzburg and Comprehensive Cancer Center Mainfranken (CCCMF), Würzburg, Germany.

G Ott (G)

Department of Clinical Pathology, Robert-Bosch-Krankenhaus, Stuttgart, Germany; Dr. Margarete Fischer-Bosch Institute of Clinical Pharmacology, Stuttgart and University of Tuebingen, Tübingen, Germany.

R Spang (R)

Statistical Bioinformatics, Institute of Functional Genomics, University of Regensburg, Regensburg, Germany.

B Altmann (B)

DSHNHL Studiensekretariat, Universitätsklinikum des Saarlandes, Homburg, Germany.

M Ziepert (M)

Institute for Medical Informatics, Statistics and Epidemiology, University of Leipzig, Leipzig, Germany.

W Klapper (W)

Institute of Pathology, Hematopathology Section and Lymph Node Registry, University Hospital Schleswig-Holstein, Campus Kiel, Kiel, Germany.

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Classifications MeSH