Skin cancer classification via convolutional neural networks: systematic review of studies involving human experts.


Journal

European journal of cancer (Oxford, England : 1990)
ISSN: 1879-0852
Titre abrégé: Eur J Cancer
Pays: England
ID NLM: 9005373

Informations de publication

Date de publication:
10 2021
Historique:
received: 16 05 2021
revised: 18 06 2021
accepted: 28 06 2021
pubmed: 12 9 2021
medline: 23 11 2021
entrez: 11 9 2021
Statut: ppublish

Résumé

Multiple studies have compared the performance of artificial intelligence (AI)-based models for automated skin cancer classification to human experts, thus setting the cornerstone for a successful translation of AI-based tools into clinicopathological practice. The objective of the study was to systematically analyse the current state of research on reader studies involving melanoma and to assess their potential clinical relevance by evaluating three main aspects: test set characteristics (holdout/out-of-distribution data set, composition), test setting (experimental/clinical, inclusion of metadata) and representativeness of participating clinicians. PubMed, Medline and ScienceDirect were screened for peer-reviewed studies published between 2017 and 2021 and dealing with AI-based skin cancer classification involving melanoma. The search terms skin cancer classification, deep learning, convolutional neural network (CNN), melanoma (detection), digital biomarkers, histopathology and whole slide imaging were combined. Based on the search results, only studies that considered direct comparison of AI results with clinicians and had a diagnostic classification as their main objective were included. A total of 19 reader studies fulfilled the inclusion criteria. Of these, 11 CNN-based approaches addressed the classification of dermoscopic images; 6 concentrated on the classification of clinical images, whereas 2 dermatopathological studies utilised digitised histopathological whole slide images. All 19 included studies demonstrated superior or at least equivalent performance of CNN-based classifiers compared with clinicians. However, almost all studies were conducted in highly artificial settings based exclusively on single images of the suspicious lesions. Moreover, test sets mainly consisted of holdout images and did not represent the full range of patient populations and melanoma subtypes encountered in clinical practice.

Sections du résumé

BACKGROUND
Multiple studies have compared the performance of artificial intelligence (AI)-based models for automated skin cancer classification to human experts, thus setting the cornerstone for a successful translation of AI-based tools into clinicopathological practice.
OBJECTIVE
The objective of the study was to systematically analyse the current state of research on reader studies involving melanoma and to assess their potential clinical relevance by evaluating three main aspects: test set characteristics (holdout/out-of-distribution data set, composition), test setting (experimental/clinical, inclusion of metadata) and representativeness of participating clinicians.
METHODS
PubMed, Medline and ScienceDirect were screened for peer-reviewed studies published between 2017 and 2021 and dealing with AI-based skin cancer classification involving melanoma. The search terms skin cancer classification, deep learning, convolutional neural network (CNN), melanoma (detection), digital biomarkers, histopathology and whole slide imaging were combined. Based on the search results, only studies that considered direct comparison of AI results with clinicians and had a diagnostic classification as their main objective were included.
RESULTS
A total of 19 reader studies fulfilled the inclusion criteria. Of these, 11 CNN-based approaches addressed the classification of dermoscopic images; 6 concentrated on the classification of clinical images, whereas 2 dermatopathological studies utilised digitised histopathological whole slide images.
CONCLUSIONS
All 19 included studies demonstrated superior or at least equivalent performance of CNN-based classifiers compared with clinicians. However, almost all studies were conducted in highly artificial settings based exclusively on single images of the suspicious lesions. Moreover, test sets mainly consisted of holdout images and did not represent the full range of patient populations and melanoma subtypes encountered in clinical practice.

Identifiants

pubmed: 34509059
pii: S0959-8049(21)00444-5
doi: 10.1016/j.ejca.2021.06.049
pii:
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Systematic Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

202-216

Subventions

Organisme : NCI NIH HHS
ID : P30 CA008748
Pays : United States

Informations de copyright

Copyright © 2021 The Author(s). Published by Elsevier Ltd.. All rights reserved.

Déclaration de conflit d'intérêts

Conflict of interest statement The authors declare the following financial interests/personal relationships which may be considered as potential competing interests: J.S.U. is on the advisory board or has received honoraria and travel support from Amgen, Bristol Myers Squibb, GSK, LEO Pharma, Merck Sharp and Dohme, Novartis, Pierre Fabre and Roche, outside the submitted work. M.G. has received speaker's honoraria and/or has served as a consultant and/or member of advisory boards for Almirall, Argenx, Biotest, Eli Lilly, Janssen Cilag, LEO Pharma, Novartis and UCB, outside the submitted work. H.A.H. worked as a consultant or received honoraria and travel support from Heine Optotechnik GmbH, JenLab GmbH, FotoFinder Systems GmbH, Magnosco GmbH, SciBase AB, Beiersdorf AG, Almirall Hermal GmbH and Galderma Laboratorium GmbH. V.M.R. is on the advisory board or has received honoraria or ownership in Inhabit Brands, Inc. unrelated to this work. Sondermann W. reports grants from medi GmbH Bayreuth, personal fees from Janssen, grants and personal fees from Novartis, personal fees from Lilly, personal fees from UCB, personal fees from Almirall, personal fees from LEO Pharma and personal fees from Sanofi Genzyme, outside the submitted work. H.P.S. is a shareholder of MoleMap NZ Limited and e-derm consult GmbH and undertakes regular tele-dermatological reporting for both companies. H.P.S. is a medical consultant for Canfield Scientific, Inc., MoleMap Australia Pty Ltd and Revenio Research Oy and a medical advisor for First Derm. M.L-V. has received speaker's honoraria and/or received grants and/or participated in clinical trials of AbbVie, Almirall, Amgen, Celgene, Eli Lilly, Janssen Cilag, LEO Pharma, Novartis and UCB, outside the submitted work. A.Z. has been an advisor and/or received speaker's honoraria and/or received grants and/or participated in clinical trials of AbbVie, Almirall, Amgen, Beiersdorf Dermo Medical, Bencard Allergy, Celgene, Eli Lilly, Janssen Cilag, LEO Pharma, Novartis, Sanofi-Aventis and UCB Pharma, outside the submitted work. Kittler H. received speaker's honoraria from FotoFinder Systems GmbH and received non-financial support from Heine Optotechnik GmbH, Derma Medical and 3Gen. T.J.B. reports owning a company that develops mobile apps, including the teledermatology services AppDoc (https://online-hautarzt.de) and Intimarzt (https://Intimarzt.de); Smart Health Heidelberg GmbH, Handschuhsheimer Landstr. 9/1, 69120 Heidelberg, https://smarthealth.de. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Auteurs

Sarah Haggenmüller (S)

Digital Biomarkers for Oncology Group, National Center for Tumor Diseases (NCT), German Cancer Research Center (DKFZ), Heidelberg, Germany; German Cancer Consortium (DKTK), Heidelberg, Germany.

Roman C Maron (RC)

Digital Biomarkers for Oncology Group, National Center for Tumor Diseases (NCT), German Cancer Research Center (DKFZ), Heidelberg, Germany; German Cancer Consortium (DKTK), Heidelberg, Germany.

Achim Hekler (A)

Digital Biomarkers for Oncology Group, National Center for Tumor Diseases (NCT), German Cancer Research Center (DKFZ), Heidelberg, Germany; German Cancer Consortium (DKTK), Heidelberg, Germany.

Jochen S Utikal (JS)

Department of Dermatology, Heidelberg University, Mannheim, Germany; Skin Cancer Unit, German Cancer Research Center (DKFZ), Heidelberg, Germany.

Catarina Barata (C)

Institute for Systems and Robotics (ISR/IST), Instituto Superior Técnico, University of Lisbon, Portugal.

Raymond L Barnhill (RL)

Departments of Pathology and Translational Research, Institut Curie, Paris, France.

Helmut Beltraminelli (H)

Department of Dermatology, Inselspital Bern University Hospital, University of Bern, Bern, Switzerland.

Carola Berking (C)

Department of Dermatology, University Hospital Erlangen, Erlangen, Germany.

Brigid Betz-Stablein (B)

The University of Queensland Diamantina Institute, The University of Queensland, Dermatology Research Centre, Brisbane, Australia.

Andreas Blum (A)

Public, Private and Teaching Practice of Dermatology, Konstanz, Germany.

Stephan A Braun (SA)

Department of Dermatology, Medical Faculty, Heinrich-Heine-University, Düsseldorf, Germany; Department of Dermatology, University Hospital Münster, Germany.

Richard Carr (R)

Department of Pathology, Warwick Hospital, Warwick, UK.

Marc Combalia (M)

Department of Dermatology, Hospital Clinic of Barcelona, IDIBAPS, University of Barcelona, Ciber de Enfermedades Raras ISCIII, Barcelona, Spain.

Maria-Teresa Fernandez-Figueras (MT)

Hospital Universitari General de Catalunya, Grupo Quironsalud, Universitat Internacional de Catalunya, Sant Cugat Del Vallés, Barcelona, Spain.

Gerardo Ferrara (G)

Anatomic Pathology Unit, Macerata General Hospital, Macerata, Italy.

Sylvie Fraitag (S)

Department of Pathology, University Paris Descartes, Necker-Enfants Malades Hospital, Assistance Publique Hospitals of Paris, Paris, France.

Lars E French (LE)

Department of Dermatology and Allergy, University Hospital, LMU Munich, Munich, Germany; Dr. Philip Frost, Department of Dermatology and Cutaneous Surgery, University of Miami Miller School of Medicine, Miami, FL, USA.

Frank F Gellrich (FF)

Skin Cancer Center at the University Cancer Centre and National Center for Tumor Diseases Dresden, Department of Dermatology, University Hospital Carl Gustav Carus, Technische Universität Dresden, Germany.

Kamran Ghoreschi (K)

Charité - Universitätsmedizin Berlin, Department of Dermatology, Venereology and Allergology, Berlin, Germany.

Matthias Goebeler (M)

Department of Dermatology, Venereology and Allergology, University Hospital Würzburg, Würzburg, Germany.

Pascale Guitera (P)

Sydney Melanoma Diagnostic Centre, Royal Prince Alfred Hospital, Sydney, New South Wales, Australia; Melanoma Institute Australia, And the University of Sydney, Australia.

Holger A Haenssle (HA)

Department of Dermatology, University Hospital Heidelberg, Heidelberg, Germany.

Sebastian Haferkamp (S)

Department of Dermatology, University Hospital Regensburg, Regensburg, Germany.

Lucie Heinzerling (L)

Department of Dermatology and Allergy, University Hospital, LMU Munich, Munich, Germany.

Markus V Heppt (MV)

Department of Dermatology, University Hospital Erlangen, Erlangen, Germany.

Franz J Hilke (FJ)

Charité - Universitätsmedizin Berlin, Department of Dermatology, Venereology and Allergology, Berlin, Germany.

Sarah Hobelsberger (S)

Skin Cancer Center at the University Cancer Centre and National Center for Tumor Diseases Dresden, Department of Dermatology, University Hospital Carl Gustav Carus, Technische Universität Dresden, Germany.

Dieter Krahl (D)

Dres. Krahl Dermatopathology, Heidelberg, Germany.

Heinz Kutzner (H)

Dermatopathology Friedrichshafen, Friedrichshafen, Germany.

Aimilios Lallas (A)

First Department of Dermatology, School of Medicine, Faculty of Health Sciences, Aristotle University, Thessaloniki, Greece.

Konstantinos Liopyris (K)

Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Mar Llamas-Velasco (M)

Department of Dermatology, University Hospital La Princesa, Madrid, Spain.

Josep Malvehy (J)

Department of Dermatology, Hospital Clinic of Barcelona, IDIBAPS, University of Barcelona, Ciber de Enfermedades Raras ISCIII, Barcelona, Spain.

Friedegund Meier (F)

Skin Cancer Center at the University Cancer Centre and National Center for Tumor Diseases Dresden, Department of Dermatology, University Hospital Carl Gustav Carus, Technische Universität Dresden, Germany.

Cornelia S L Müller (CSL)

Institute for Histology, Cytology and Molecular Diagnostic, Trier, Germany.

Alexander A Navarini (AA)

Department of Dermatology, University Hospital of Basel, Switzerland.

Cristián Navarrete-Dechent (C)

Department of Dermatology, Escuela de Medicina, Pontificia Universidad Católica de Chile, Santiago, Chile.

Antonio Perasole (A)

Anatomic and Cytopathology, Az. ULSS 8 Berica, Regione Veneto, Ospedale San Bortolo, Vicenza, Italy.

Gabriela Poch (G)

Charité - Universitätsmedizin Berlin, Department of Dermatology, Venereology and Allergology, Berlin, Germany.

Sebastian Podlipnik (S)

Department of Dermatology, Hospital Clinic of Barcelona, IDIBAPS, University of Barcelona, Ciber de Enfermedades Raras ISCIII, Barcelona, Spain.

Luis Requena (L)

Dermatology Department, Hospital Fundación Jiménez Díaz, Madrid, Spain.

Veronica M Rotemberg (VM)

Dermatology Service, Department of Medicine, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Andrea Saggini (A)

Dermatopathology Friedrichshafen, Friedrichshafen, Germany.

Omar P Sangueza (OP)

Dermatopathology, Wake Forest School of Medicine, Winston-Salem, North Carolina, USA.

Carlos Santonja (C)

Pathology Department, Fundación Jiménez Díaz, Madrid, Spain.

Dirk Schadendorf (D)

German Cancer Consortium (DKTK), Heidelberg, Germany; Department of Dermatology, Venereology and Allergology, University Hospital Essen, University Duisburg-Essen, Essen, Germany.

Bastian Schilling (B)

Department of Dermatology, Venereology and Allergology, University Hospital Würzburg, Würzburg, Germany.

Max Schlaak (M)

Charité - Universitätsmedizin Berlin, Department of Dermatology, Venereology and Allergology, Berlin, Germany.

Justin G Schlager (JG)

Department of Dermatology and Allergy, University Hospital, LMU Munich, Munich, Germany.

Mildred Sergon (M)

Skin Cancer Center at the University Cancer Centre and National Center for Tumor Diseases Dresden, Department of Dermatology, University Hospital Carl Gustav Carus, Technische Universität Dresden, Germany.

Wiebke Sondermann (W)

Department of Dermatology, Venereology and Allergology, University Hospital Essen, University Duisburg-Essen, Essen, Germany.

H Peter Soyer (HP)

The University of Queensland Diamantina Institute, The University of Queensland, Dermatology Research Centre, Brisbane, Australia.

Hans Starz (H)

Dermpath München, Munich, Germany.

Wilhelm Stolz (W)

Department of Dermatology, Allergology and Environmental Medicine II, Hospital Thalkirchner Street, Munich, Germany.

Esmeralda Vale (E)

Department of Dermatology and Dermatopathology, Hospital da Luz, Lisbon, Portugal.

Wolfgang Weyers (W)

Center for Dermatopathology, Freiburg, Germany.

Alexander Zink (A)

Department of Dermatology and Allergy, Faculty of Medicine, Technical University of Munich, 80802, Munich, Germany.

Eva Krieghoff-Henning (E)

Digital Biomarkers for Oncology Group, National Center for Tumor Diseases (NCT), German Cancer Research Center (DKFZ), Heidelberg, Germany; German Cancer Consortium (DKTK), Heidelberg, Germany.

Jakob N Kather (JN)

Department of Medicine III, University Hospital RWTH Aachen, Aachen, Germany.

Christof von Kalle (C)

Department of Clinical-Translational Sciences, Charité University Medicine and Berlin Institute of Health (BIH), Berlin, Germany.

Daniel B Lipka (DB)

German Cancer Consortium (DKTK), Heidelberg, Germany; Department of Translational Medical Oncology, National Center for Tumor Diseases (NCT) Heidelberg and German Cancer Research Center (DKFZ), Heidelberg, Germany.

Stefan Fröhling (S)

German Cancer Consortium (DKTK), Heidelberg, Germany; Department of Translational Medical Oncology, National Center for Tumor Diseases (NCT) Heidelberg and German Cancer Research Center (DKFZ), Heidelberg, Germany.

Axel Hauschild (A)

Department of Dermatology, University Hospital of Schleswig-Holstein (UKSH), Campus Kiel, Kiel, Germany.

Harald Kittler (H)

ViDIR Group, Department of Dermatology, Medical University of Vienna, Vienna, Austria.

Titus J Brinker (TJ)

Digital Biomarkers for Oncology Group, National Center for Tumor Diseases (NCT), German Cancer Research Center (DKFZ), Heidelberg, Germany; German Cancer Consortium (DKTK), Heidelberg, Germany. Electronic address: titus.brinker@dkfz.de.

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