Assessment of the current and emerging criteria for the histopathological classification of lung neuroendocrine tumours in the lungNENomics project.

Ki-67 PHH3 deep learning histological classification lung neuroendocrine tumours

Journal

ESMO open
ISSN: 2059-7029
Titre abrégé: ESMO Open
Pays: England
ID NLM: 101690685

Informations de publication

Date de publication:
14 Jun 2024
Historique:
received: 06 12 2023
revised: 07 05 2024
accepted: 08 05 2024
medline: 16 6 2024
pubmed: 16 6 2024
entrez: 15 6 2024
Statut: aheadofprint

Résumé

Six thoracic pathologists reviewed 259 lung neuroendocrine tumours (LNETs) from the lungNENomics project, with 171 of them having associated survival data. This cohort presents a unique opportunity to assess the strengths and limitations of current World Health Organization (WHO) classification criteria and to evaluate the utility of emerging markers. Patients were diagnosed based on the 2021 WHO criteria, with atypical carcinoids (ACs) defined by the presence of focal necrosis and/or 2-10 mitoses per 2 mm The accuracy in distinguishing typical from ACs is hampered by interobserver variability in mitotic counting and the limitations of morphological criteria in identifying aggressive cases. Our study reveals that different Ki-67 cut-offs can categorise LNETs similarly to current WHO criteria. Counting mitoses in PHH3+ areas does not improve diagnosis, while providing a similar prognostic value to the current criteria. With the advantage of being time efficient, automated assessment of these markers leads to similar conclusions. Lastly, state-of-the-art deep learning modelling does not uncover undisclosed morphological features with diagnostic value. This study suggests that the mitotic criteria can be complemented by manual or automated assessment of Ki-67 or PHH3 protein expression, but these markers do not significantly improve the prognostic value of the current classification, as the AC group remains highly unspecific for aggressive cases. Therefore, we may have exhausted the potential of morphological features in classifying and prognosticating LNETs. Our study suggests that it might be time to shift the research focus towards investigating molecular markers that could contribute to a more clinically relevant morpho-molecular classification.

Sections du résumé

BACKGROUND BACKGROUND
Six thoracic pathologists reviewed 259 lung neuroendocrine tumours (LNETs) from the lungNENomics project, with 171 of them having associated survival data. This cohort presents a unique opportunity to assess the strengths and limitations of current World Health Organization (WHO) classification criteria and to evaluate the utility of emerging markers.
PATIENTS AND METHODS METHODS
Patients were diagnosed based on the 2021 WHO criteria, with atypical carcinoids (ACs) defined by the presence of focal necrosis and/or 2-10 mitoses per 2 mm
RESULTS RESULTS
The accuracy in distinguishing typical from ACs is hampered by interobserver variability in mitotic counting and the limitations of morphological criteria in identifying aggressive cases. Our study reveals that different Ki-67 cut-offs can categorise LNETs similarly to current WHO criteria. Counting mitoses in PHH3+ areas does not improve diagnosis, while providing a similar prognostic value to the current criteria. With the advantage of being time efficient, automated assessment of these markers leads to similar conclusions. Lastly, state-of-the-art deep learning modelling does not uncover undisclosed morphological features with diagnostic value.
CONCLUSIONS CONCLUSIONS
This study suggests that the mitotic criteria can be complemented by manual or automated assessment of Ki-67 or PHH3 protein expression, but these markers do not significantly improve the prognostic value of the current classification, as the AC group remains highly unspecific for aggressive cases. Therefore, we may have exhausted the potential of morphological features in classifying and prognosticating LNETs. Our study suggests that it might be time to shift the research focus towards investigating molecular markers that could contribute to a more clinically relevant morpho-molecular classification.

Identifiants

pubmed: 38878324
pii: S2059-7029(24)01360-7
doi: 10.1016/j.esmoop.2024.103591
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

103591

Informations de copyright

Copyright © 2024 World Health Organization. Published by Elsevier Ltd.. All rights reserved.

Déclaration de conflit d'intérêts

Disclosure Where authors are identified as personnel of the International Agency for Research on Cancer/WHO, the authors alone are responsible for the views expressed in this article and they do not necessarily represent the decisions, policy, or views of the International Agency for Research on Cancer/WHO. The rest of the authors declare no conflict of interest.

Auteurs

É Mathian (É)

Rare Cancers Genomic Team, Genomic Epidemiology Branch, International Agency for Research on Cancer (IARC-WHO), Lyon, France; Department of Mathematics and Informatics, Ecole Centrale de Lyon, Lyon, France.

Y Drouet (Y)

UMR CNRS 5558 LBBE, Claude Bernard Lyon 1 University, Villeurbanne, France; Prevention & Public Health Department, Centre Léon Bérard, Lyon, France.

A Sexton-Oates (A)

Rare Cancers Genomic Team, Genomic Epidemiology Branch, International Agency for Research on Cancer (IARC-WHO), Lyon, France.

M G Papotti (MG)

Department of Oncology, University of Turin, Turin, Italy.

G Pelosi (G)

Department of Oncology and Hemato-Oncology, University of Milan, Milan, Italy.

J-M Vignaud (JM)

Department of Biopathology, Institut De Cancérologie de Lorraine (CHRU-ICL), Vandoeuvre-lès-Nancy, France; University Hospital of Nancy (CHRU), Nancy, France.

L Brcic (L)

Diagnostic and Research Institute of Pathology, Medical University of Graz, Graz, Austria.

A Mansuet-Lupo (A)

Department of Pathology, Hôpital Cochin, AP-HP, Université de Paris, Paris, France.

F Damiola (F)

Department of Biopathology, Centre Léon Bérard & Pathology Research Platform, Cancer Research Center of Lyon, Lyon, France.

C Altun (C)

Department of Biopathology, Centre Léon Bérard & Pathology Research Platform, Cancer Research Center of Lyon, Lyon, France.

J-P Berthet (JP)

Department of Thoracic Surgery, FHU OncoAge, Nice Pasteur Hospital, University Cote d'Azur, Nice, France.

C B Fournier (CB)

Caen Lower Normandy Tumour Bank, Centre François Baclesse, Caen, France.

O T Brustugun (OT)

Section of Oncology, Drammen Hospital, Vestre Viken Hospital Trust, Drammen, Norway; Institute of Clinical Medicine, University of Oslo, Oslo, Norway.

G Centonze (G)

First Pathology Division, Department of Pathology and Laboratory Medicine, Fondazione IRCCS Istituto Nazionale dei Tumori, Milan, Italy.

L Chalabreysse (L)

Hospices Civils de Lyon, GHE, Institut de Pathologie Est, Bron, France.

V T de Montpréville (VT)

Department of Pathology, Hôpital Marie-Lannelongue, Groupe Hospitalier Paris Saint Joseph, Le Plessis Robinson, France.

C M di Micco (CM)

Unit of Oncology, Fondazione IRCCS Cas Sollievo della Sofferenza, San Giovanni Rotondo, Italy.

E Fadel (E)

Department of Pathology, Hôpital Marie-Lannelongue, Groupe Hospitalier Paris Saint Joseph, Le Plessis Robinson, France; Department of Thoracic and Vascular Surgery and Heart-Lung Transplantation, Université Paris-Saclay, Le Plessis-Robinson, France.

N Gadot (N)

Department of Biopathology, Centre Léon Bérard & Pathology Research Platform, Cancer Research Center of Lyon, Lyon, France.

P Graziano (P)

Unit of Oncology, Fondazione IRCCS Cas Sollievo della Sofferenza, San Giovanni Rotondo, Italy.

P Hofman (P)

FHU OncoAge, Biobank BB-0033-0025, Laboratory of Clinical and Experimental Pathology, Nice Pasteur Hospital, University Cote d'Azur, Nice, France.

V Hofman (V)

FHU OncoAge, Biobank BB-0033-0025, Laboratory of Clinical and Experimental Pathology, Nice Pasteur Hospital, University Cote d'Azur, Nice, France.

S Lacomme (S)

University Hospital of Nancy (CHRU), Nancy, France.

M Lund-Iversen (M)

Department of Pathology, Oslo University Hospital, Oslo, Norway.

L Mangiante (L)

Rare Cancers Genomic Team, Genomic Epidemiology Branch, International Agency for Research on Cancer (IARC-WHO), Lyon, France; School of Medicine, Stanford University, Stanford, USA.

M Milione (M)

First Pathology Division, Department of Pathology and Laboratory Medicine, Fondazione IRCCS Istituto Nazionale dei Tumori, Milan, Italy.

L A Muscarella (LA)

Unit of Oncology, Fondazione IRCCS Cas Sollievo della Sofferenza, San Giovanni Rotondo, Italy.

C Perrin (C)

Hospices Civils de Lyon, GHE, Institut de Pathologie Est, Bron, France.

G Planchard (G)

Pathology Department, Caen University Hospital, Normandy University, Caen, France.

H Popper (H)

Diagnostic and Research Institute of Pathology, Medical University of Graz, Graz, Austria.

N Rousseau (N)

Caen Lower Normandy Tumour Bank, Centre François Baclesse, Caen, France.

L Roz (L)

Tumor Genomics Unit, Department of Research, Fondazione IRCCS Istituto Nazionale Dei Tumori, Milan, Italy.

G Sabella (G)

First Pathology Division, Department of Pathology and Laboratory Medicine, Fondazione IRCCS Istituto Nazionale dei Tumori, Milan, Italy.

S Tabone-Eglinger (S)

Biological Resource Center, Centre Léon Bérard, Lyon, France.

C Voegele (C)

Rare Cancers Genomic Team, Genomic Epidemiology Branch, International Agency for Research on Cancer (IARC-WHO), Lyon, France.

M Volante (M)

Department of Oncology, University of Turin, Turin, Italy.

T Walter (T)

Service d'Oncologie Médicale, Groupement Hospitalier Centre, Institut de Cancérologie des Hospices Civils de Lyon, Lyon, France.

A-M Dingemans (AM)

Department of Pulmonary Medicine, Erasmus MC Cancer Institute, University Medical Center, Rotterdam, The Netherlands.

L Moonen (L)

Department of Pathology, GROW School for Oncology and Reproduction, Maastricht University Medical Centre, Maastricht, Netherlands.

E J Speel (EJ)

Department of Pathology, GROW School for Oncology and Reproduction, Maastricht University Medical Centre, Maastricht, Netherlands.

J Derks (J)

Department of Pulmonary Diseases, GROW School for Oncology and Reproduction, Maastricht University Medical Centre, Maastricht, The Netherlands.

N Girard (N)

Institut Curie, Versailles, France.

L Chen (L)

Department of Mathematics and Informatics, Ecole Centrale de Lyon, Lyon, France; Institut Universitaire de France (IUF), Paris, France.

N Alcala (N)

Rare Cancers Genomic Team, Genomic Epidemiology Branch, International Agency for Research on Cancer (IARC-WHO), Lyon, France.

L Fernandez-Cuesta (L)

Rare Cancers Genomic Team, Genomic Epidemiology Branch, International Agency for Research on Cancer (IARC-WHO), Lyon, France. Electronic address: fernandezcuestal@iarc.who.int.

S Lantuejoul (S)

Department of Biopathology, Centre Léon Bérard & Pathology Research Platform, Cancer Research Center of Lyon, Lyon, France.

M Foll (M)

Rare Cancers Genomic Team, Genomic Epidemiology Branch, International Agency for Research on Cancer (IARC-WHO), Lyon, France.

Classifications MeSH