High throughput assessment of biomarkers in tissue microarrays using artificial intelligence: PTEN loss as a proof-of-principle in multi-center prostate cancer cohorts.


Journal

Modern pathology : an official journal of the United States and Canadian Academy of Pathology, Inc
ISSN: 1530-0285
Titre abrégé: Mod Pathol
Pays: United States
ID NLM: 8806605

Informations de publication

Date de publication:
02 2021
Historique:
received: 30 12 2019
accepted: 21 08 2020
revised: 21 08 2020
pubmed: 5 9 2020
medline: 17 7 2022
entrez: 5 9 2020
Statut: ppublish

Résumé

Phosphatase and tensin homolog (PTEN) loss is associated with adverse outcomes in prostate cancer and has clinical potential as a prognostic biomarker. The objective of this work was to develop an artificial intelligence (AI) system for automated detection and localization of PTEN loss on immunohistochemically (IHC) stained sections. PTEN loss was assessed using IHC in two prostate tissue microarrays (TMA) (internal cohort, n = 272 and external cohort, n = 129 patients). TMA cores were visually scored for PTEN loss by pathologists and, if present, spatially annotated. Cores from each patient within the internal TMA cohort were split into 90% cross-validation (N = 2048) and 10% hold-out testing (N = 224) sets. ResNet-101 architecture was used to train core-based classification using a multi-resolution ensemble approach (×5, ×10, and ×20). For spatial annotations, single resolution pixel-based classification was trained from patches extracted at ×20 resolution, interpolated to ×40 resolution, and applied in a sliding-window fashion. A final AI-based prediction model was created from combining multi-resolution and pixel-based models. Performance was evaluated in 428 cores of external cohort. From both cohorts, a total of 2700 cores were studied, with a frequency of PTEN loss of 14.5% in internal (180/1239) and external 13.5% (43/319) cancer cores. The final AI-based prediction of PTEN status demonstrated 98.1% accuracy (95.0% sensitivity, 98.4% specificity; median dice score = 0.811) in internal cohort cross-validation set and 99.1% accuracy (100% sensitivity, 99.0% specificity; median dice score = 0.804) in internal cohort test set. Overall core-based classification in the external cohort was significantly improved in the external cohort (area under the curve = 0.964, 90.6% sensitivity, 95.7% specificity) when further trained (fine-tuned) using 15% of cohort data (19/124 patients). These results demonstrate a robust and fully automated method for detection and localization of PTEN loss in prostate cancer tissue samples. AI-based algorithms have potential to streamline sample assessment in research and clinical laboratories.

Identifiants

pubmed: 32884130
doi: 10.1038/s41379-020-00674-w
pii: S0893-3952(22)00688-3
pmc: PMC9152638
mid: NIHMS1801793
doi:

Substances chimiques

Biomarkers, Tumor 0
PTEN Phosphohydrolase EC 3.1.3.67
PTEN protein, human EC 3.1.3.67

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

478-489

Subventions

Organisme : CCR NIH HHS
ID : HHSN261200800001C
Pays : United States
Organisme : NCI NIH HHS
ID : HHSN261200800001E
Pays : United States
Organisme : Intramural NIH HHS
ID : ZIH BC012032
Pays : United States
Organisme : Movember Foundation (Movember)
ID : T2014-01
Pays : International

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Auteurs

Stephanie A Harmon (SA)

Molecular Imaging Branch, National Cancer Institute, National Institutes of Health, Bethesda, MD, USA.
Clinical Research Directorate, Frederick National Laboratory for Cancer Research, Frederick, MD, USA.

Palak G Patel (PG)

Division of Cancer Biology & Genetics, Cancer Research Institute, Queen's University, Kingston, ON, Canada.
Department of Pathology and Molecular Medicine, Queen's University, Kingston, ON, Canada.
Department of Cell Biology at The Arthur and Sonia Labatt Brain Tumour Research Centre at the Hospital for Sick Children, Toronto, ON, Canada.

Thomas H Sanford (TH)

Molecular Imaging Branch, National Cancer Institute, National Institutes of Health, Bethesda, MD, USA.
Department of Urology, Upstate Medical University, Syracuse, NY, USA.

Isabelle Caven (I)

Division of Cancer Biology & Genetics, Cancer Research Institute, Queen's University, Kingston, ON, Canada.
Department of Pathology and Molecular Medicine, Queen's University, Kingston, ON, Canada.

Rachael Iseman (R)

Division of Cancer Biology & Genetics, Cancer Research Institute, Queen's University, Kingston, ON, Canada.
Department of Pathology and Molecular Medicine, Queen's University, Kingston, ON, Canada.

Thiago Vidotto (T)

Department of Genetics, Ribeirão Preto Medical School, University of São Paulo, Ribeirão Preto, Brazil.

Clarissa Picanço (C)

Department of Genetics, Ribeirão Preto Medical School, University of São Paulo, Ribeirão Preto, Brazil.

Jeremy A Squire (JA)

Department of Pathology and Molecular Medicine, Queen's University, Kingston, ON, Canada.
Department of Genetics, Ribeirão Preto Medical School, University of São Paulo, Ribeirão Preto, Brazil.

Samira Masoudi (S)

Molecular Imaging Branch, National Cancer Institute, National Institutes of Health, Bethesda, MD, USA.

Sherif Mehralivand (S)

Molecular Imaging Branch, National Cancer Institute, National Institutes of Health, Bethesda, MD, USA.

Peter L Choyke (PL)

Molecular Imaging Branch, National Cancer Institute, National Institutes of Health, Bethesda, MD, USA.

David M Berman (DM)

Division of Cancer Biology & Genetics, Cancer Research Institute, Queen's University, Kingston, ON, Canada.
Department of Pathology and Molecular Medicine, Queen's University, Kingston, ON, Canada.

Baris Turkbey (B)

Molecular Imaging Branch, National Cancer Institute, National Institutes of Health, Bethesda, MD, USA.

Tamara Jamaspishvili (T)

Division of Cancer Biology & Genetics, Cancer Research Institute, Queen's University, Kingston, ON, Canada. tamara.jamaspishvili@queensu.ca.
Department of Pathology and Molecular Medicine, Queen's University, Kingston, ON, Canada. tamara.jamaspishvili@queensu.ca.

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Classifications MeSH