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Evaluation of automatic discrimination between benign and malignant prostate tissue in the era of high precision digital pathology

BACKGROUND: Prostate cancer is a major health concern in aging men. Paralleling an aging society, prostate cancer prevalence increases emphasizing the need for efficient diagnostic algorithms. METHODS: Retrospectively, 106 prostate tissue samples from 48 patients (mean age, [Formula: see text] years...

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Autores principales: Zhdanovich, Yauheniya, Ackermann, Jörg, Wild, Peter J., Köllermann, Jens, Bankov, Katrin, Döring, Claudia, Flinner, Nadine, Reis, Henning, Wenzel, Mike, Höh, Benedikt, Mandel, Philipp, Vogl, Thomas J., Harter, Patrick, Filipski, Katharina, Koch, Ina, Bernatz, Simon
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9809030/
https://www.ncbi.nlm.nih.gov/pubmed/36597019
http://dx.doi.org/10.1186/s12859-022-05124-9
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author Zhdanovich, Yauheniya
Ackermann, Jörg
Wild, Peter J.
Köllermann, Jens
Bankov, Katrin
Döring, Claudia
Flinner, Nadine
Reis, Henning
Wenzel, Mike
Höh, Benedikt
Mandel, Philipp
Vogl, Thomas J.
Harter, Patrick
Filipski, Katharina
Koch, Ina
Bernatz, Simon
author_facet Zhdanovich, Yauheniya
Ackermann, Jörg
Wild, Peter J.
Köllermann, Jens
Bankov, Katrin
Döring, Claudia
Flinner, Nadine
Reis, Henning
Wenzel, Mike
Höh, Benedikt
Mandel, Philipp
Vogl, Thomas J.
Harter, Patrick
Filipski, Katharina
Koch, Ina
Bernatz, Simon
author_sort Zhdanovich, Yauheniya
collection PubMed
description BACKGROUND: Prostate cancer is a major health concern in aging men. Paralleling an aging society, prostate cancer prevalence increases emphasizing the need for efficient diagnostic algorithms. METHODS: Retrospectively, 106 prostate tissue samples from 48 patients (mean age, [Formula: see text] years) were included in the study. Patients suffered from prostate cancer (n = 38) or benign prostatic hyperplasia (n = 10) and were treated with radical prostatectomy or Holmium laser enucleation of the prostate, respectively. We constructed tissue microarrays (TMAs) comprising representative malignant (n = 38) and benign (n = 68) tissue cores. TMAs were processed to histological slides, stained, digitized and assessed for the applicability of machine learning strategies and open–source tools in diagnosis of prostate cancer. We applied the software QuPath to extract features for shape, stain intensity, and texture of TMA cores for three stainings, H&E, ERG, and PIN-4. Three machine learning algorithms, neural network (NN), support vector machines (SVM), and random forest (RF), were trained and cross-validated with 100 Monte Carlo random splits into 70% training set and 30% test set. We determined AUC values for single color channels, with and without optimization of hyperparameters by exhaustive grid search. We applied recursive feature elimination to feature sets of multiple color transforms. RESULTS: Mean AUC was above 0.80. PIN-4 stainings yielded higher AUC than H&E and ERG. For PIN-4 with the color transform saturation, NN, RF, and SVM revealed AUC of [Formula: see text] , [Formula: see text] , and [Formula: see text] , respectively. Optimization of hyperparameters improved the AUC only slightly by 0.01. For H&E, feature selection resulted in no increase of AUC but to an increase of 0.02–0.06 for ERG and PIN-4. CONCLUSIONS: Automated pipelines may be able to discriminate with high accuracy between malignant and benign tissue. We found PIN-4 staining best suited for classification. Further bioinformatic analysis of larger data sets would be crucial to evaluate the reliability of automated classification methods for clinical practice and to evaluate potential discrimination of aggressiveness of cancer to pave the way to automatic precision medicine. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12859-022-05124-9.
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spelling pubmed-98090302023-01-04 Evaluation of automatic discrimination between benign and malignant prostate tissue in the era of high precision digital pathology Zhdanovich, Yauheniya Ackermann, Jörg Wild, Peter J. Köllermann, Jens Bankov, Katrin Döring, Claudia Flinner, Nadine Reis, Henning Wenzel, Mike Höh, Benedikt Mandel, Philipp Vogl, Thomas J. Harter, Patrick Filipski, Katharina Koch, Ina Bernatz, Simon BMC Bioinformatics Research BACKGROUND: Prostate cancer is a major health concern in aging men. Paralleling an aging society, prostate cancer prevalence increases emphasizing the need for efficient diagnostic algorithms. METHODS: Retrospectively, 106 prostate tissue samples from 48 patients (mean age, [Formula: see text] years) were included in the study. Patients suffered from prostate cancer (n = 38) or benign prostatic hyperplasia (n = 10) and were treated with radical prostatectomy or Holmium laser enucleation of the prostate, respectively. We constructed tissue microarrays (TMAs) comprising representative malignant (n = 38) and benign (n = 68) tissue cores. TMAs were processed to histological slides, stained, digitized and assessed for the applicability of machine learning strategies and open–source tools in diagnosis of prostate cancer. We applied the software QuPath to extract features for shape, stain intensity, and texture of TMA cores for three stainings, H&E, ERG, and PIN-4. Three machine learning algorithms, neural network (NN), support vector machines (SVM), and random forest (RF), were trained and cross-validated with 100 Monte Carlo random splits into 70% training set and 30% test set. We determined AUC values for single color channels, with and without optimization of hyperparameters by exhaustive grid search. We applied recursive feature elimination to feature sets of multiple color transforms. RESULTS: Mean AUC was above 0.80. PIN-4 stainings yielded higher AUC than H&E and ERG. For PIN-4 with the color transform saturation, NN, RF, and SVM revealed AUC of [Formula: see text] , [Formula: see text] , and [Formula: see text] , respectively. Optimization of hyperparameters improved the AUC only slightly by 0.01. For H&E, feature selection resulted in no increase of AUC but to an increase of 0.02–0.06 for ERG and PIN-4. CONCLUSIONS: Automated pipelines may be able to discriminate with high accuracy between malignant and benign tissue. We found PIN-4 staining best suited for classification. Further bioinformatic analysis of larger data sets would be crucial to evaluate the reliability of automated classification methods for clinical practice and to evaluate potential discrimination of aggressiveness of cancer to pave the way to automatic precision medicine. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12859-022-05124-9. BioMed Central 2023-01-03 /pmc/articles/PMC9809030/ /pubmed/36597019 http://dx.doi.org/10.1186/s12859-022-05124-9 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Zhdanovich, Yauheniya
Ackermann, Jörg
Wild, Peter J.
Köllermann, Jens
Bankov, Katrin
Döring, Claudia
Flinner, Nadine
Reis, Henning
Wenzel, Mike
Höh, Benedikt
Mandel, Philipp
Vogl, Thomas J.
Harter, Patrick
Filipski, Katharina
Koch, Ina
Bernatz, Simon
Evaluation of automatic discrimination between benign and malignant prostate tissue in the era of high precision digital pathology
title Evaluation of automatic discrimination between benign and malignant prostate tissue in the era of high precision digital pathology
title_full Evaluation of automatic discrimination between benign and malignant prostate tissue in the era of high precision digital pathology
title_fullStr Evaluation of automatic discrimination between benign and malignant prostate tissue in the era of high precision digital pathology
title_full_unstemmed Evaluation of automatic discrimination between benign and malignant prostate tissue in the era of high precision digital pathology
title_short Evaluation of automatic discrimination between benign and malignant prostate tissue in the era of high precision digital pathology
title_sort evaluation of automatic discrimination between benign and malignant prostate tissue in the era of high precision digital pathology
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9809030/
https://www.ncbi.nlm.nih.gov/pubmed/36597019
http://dx.doi.org/10.1186/s12859-022-05124-9
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