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Attention-Based Deep Neural Networks for Detection of Cancerous and Precancerous Esophagus Tissue on Histopathological Slides

IMPORTANCE: Deep learning–based methods, such as the sliding window approach for cropped-image classification and heuristic aggregation for whole-slide inference, for analyzing histological patterns in high-resolution microscopy images have shown promising results. These approaches, however, require...

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Autores principales: Tomita, Naofumi, Abdollahi, Behnaz, Wei, Jason, Ren, Bing, Suriawinata, Arief, Hassanpour, Saeed
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Medical Association 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6865275/
https://www.ncbi.nlm.nih.gov/pubmed/31693124
http://dx.doi.org/10.1001/jamanetworkopen.2019.14645
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author Tomita, Naofumi
Abdollahi, Behnaz
Wei, Jason
Ren, Bing
Suriawinata, Arief
Hassanpour, Saeed
author_facet Tomita, Naofumi
Abdollahi, Behnaz
Wei, Jason
Ren, Bing
Suriawinata, Arief
Hassanpour, Saeed
author_sort Tomita, Naofumi
collection PubMed
description IMPORTANCE: Deep learning–based methods, such as the sliding window approach for cropped-image classification and heuristic aggregation for whole-slide inference, for analyzing histological patterns in high-resolution microscopy images have shown promising results. These approaches, however, require a laborious annotation process and are fragmented. OBJECTIVE: To evaluate a novel deep learning method that uses tissue-level annotations for high-resolution histological image analysis for Barrett esophagus (BE) and esophageal adenocarcinoma detection. DESIGN, SETTING, AND PARTICIPANTS: This diagnostic study collected deidentified high-resolution histological images (N = 379) for training a new model composed of a convolutional neural network and a grid-based attention network. Histological images of patients who underwent endoscopic esophagus and gastroesophageal junction mucosal biopsy between January 1, 2016, and December 31, 2018, at Dartmouth-Hitchcock Medical Center (Lebanon, New Hampshire) were collected. MAIN OUTCOMES AND MEASURES: The model was evaluated on an independent testing set of 123 histological images with 4 classes: normal, BE-no-dysplasia, BE-with-dysplasia, and adenocarcinoma. Performance of this model was measured and compared with that of the current state-of-the-art sliding window approach using the following standard machine learning metrics: accuracy, recall, precision, and F1 score. RESULTS: Of the independent testing set of 123 histological images, 30 (24.4%) were in the BE-no-dysplasia class, 14 (11.4%) in the BE-with-dysplasia class, 21 (17.1%) in the adenocarcinoma class, and 58 (47.2%) in the normal class. Classification accuracies of the proposed model were 0.85 (95% CI, 0.81-0.90) for the BE-no-dysplasia class, 0.89 (95% CI, 0.84-0.92) for the BE-with-dysplasia class, and 0.88 (95% CI, 0.84-0.92) for the adenocarcinoma class. The proposed model achieved a mean accuracy of 0.83 (95% CI, 0.80-0.86) and marginally outperformed the sliding window approach on the same testing set. The F1 scores of the attention-based model were at least 8% higher for each class compared with the sliding window approach: 0.68 (95% CI, 0.61-0.75) vs 0.61 (95% CI, 0.53-0.68) for the normal class, 0.72 (95% CI, 0.63-0.80) vs 0.58 (95% CI, 0.45-0.69) for the BE-no-dysplasia class, 0.30 (95% CI, 0.11-0.48) vs 0.22 (95% CI, 0.11-0.33) for the BE-with-dysplasia class, and 0.67 (95% CI, 0.54-0.77) vs 0.58 (95% CI, 0.44-0.70) for the adenocarcinoma class. However, this outperformance was not statistically significant. CONCLUSIONS AND RELEVANCE: Results of this study suggest that the proposed attention-based deep neural network framework for BE and esophageal adenocarcinoma detection is important because it is based solely on tissue-level annotations, unlike existing methods that are based on regions of interest. This new model is expected to open avenues for applying deep learning to digital pathology.
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spelling pubmed-68652752019-12-06 Attention-Based Deep Neural Networks for Detection of Cancerous and Precancerous Esophagus Tissue on Histopathological Slides Tomita, Naofumi Abdollahi, Behnaz Wei, Jason Ren, Bing Suriawinata, Arief Hassanpour, Saeed JAMA Netw Open Original Investigation IMPORTANCE: Deep learning–based methods, such as the sliding window approach for cropped-image classification and heuristic aggregation for whole-slide inference, for analyzing histological patterns in high-resolution microscopy images have shown promising results. These approaches, however, require a laborious annotation process and are fragmented. OBJECTIVE: To evaluate a novel deep learning method that uses tissue-level annotations for high-resolution histological image analysis for Barrett esophagus (BE) and esophageal adenocarcinoma detection. DESIGN, SETTING, AND PARTICIPANTS: This diagnostic study collected deidentified high-resolution histological images (N = 379) for training a new model composed of a convolutional neural network and a grid-based attention network. Histological images of patients who underwent endoscopic esophagus and gastroesophageal junction mucosal biopsy between January 1, 2016, and December 31, 2018, at Dartmouth-Hitchcock Medical Center (Lebanon, New Hampshire) were collected. MAIN OUTCOMES AND MEASURES: The model was evaluated on an independent testing set of 123 histological images with 4 classes: normal, BE-no-dysplasia, BE-with-dysplasia, and adenocarcinoma. Performance of this model was measured and compared with that of the current state-of-the-art sliding window approach using the following standard machine learning metrics: accuracy, recall, precision, and F1 score. RESULTS: Of the independent testing set of 123 histological images, 30 (24.4%) were in the BE-no-dysplasia class, 14 (11.4%) in the BE-with-dysplasia class, 21 (17.1%) in the adenocarcinoma class, and 58 (47.2%) in the normal class. Classification accuracies of the proposed model were 0.85 (95% CI, 0.81-0.90) for the BE-no-dysplasia class, 0.89 (95% CI, 0.84-0.92) for the BE-with-dysplasia class, and 0.88 (95% CI, 0.84-0.92) for the adenocarcinoma class. The proposed model achieved a mean accuracy of 0.83 (95% CI, 0.80-0.86) and marginally outperformed the sliding window approach on the same testing set. The F1 scores of the attention-based model were at least 8% higher for each class compared with the sliding window approach: 0.68 (95% CI, 0.61-0.75) vs 0.61 (95% CI, 0.53-0.68) for the normal class, 0.72 (95% CI, 0.63-0.80) vs 0.58 (95% CI, 0.45-0.69) for the BE-no-dysplasia class, 0.30 (95% CI, 0.11-0.48) vs 0.22 (95% CI, 0.11-0.33) for the BE-with-dysplasia class, and 0.67 (95% CI, 0.54-0.77) vs 0.58 (95% CI, 0.44-0.70) for the adenocarcinoma class. However, this outperformance was not statistically significant. CONCLUSIONS AND RELEVANCE: Results of this study suggest that the proposed attention-based deep neural network framework for BE and esophageal adenocarcinoma detection is important because it is based solely on tissue-level annotations, unlike existing methods that are based on regions of interest. This new model is expected to open avenues for applying deep learning to digital pathology. American Medical Association 2019-11-06 /pmc/articles/PMC6865275/ /pubmed/31693124 http://dx.doi.org/10.1001/jamanetworkopen.2019.14645 Text en Copyright 2019 Tomita N et al. JAMA Network Open. http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the CC-BY License.
spellingShingle Original Investigation
Tomita, Naofumi
Abdollahi, Behnaz
Wei, Jason
Ren, Bing
Suriawinata, Arief
Hassanpour, Saeed
Attention-Based Deep Neural Networks for Detection of Cancerous and Precancerous Esophagus Tissue on Histopathological Slides
title Attention-Based Deep Neural Networks for Detection of Cancerous and Precancerous Esophagus Tissue on Histopathological Slides
title_full Attention-Based Deep Neural Networks for Detection of Cancerous and Precancerous Esophagus Tissue on Histopathological Slides
title_fullStr Attention-Based Deep Neural Networks for Detection of Cancerous and Precancerous Esophagus Tissue on Histopathological Slides
title_full_unstemmed Attention-Based Deep Neural Networks for Detection of Cancerous and Precancerous Esophagus Tissue on Histopathological Slides
title_short Attention-Based Deep Neural Networks for Detection of Cancerous and Precancerous Esophagus Tissue on Histopathological Slides
title_sort attention-based deep neural networks for detection of cancerous and precancerous esophagus tissue on histopathological slides
topic Original Investigation
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6865275/
https://www.ncbi.nlm.nih.gov/pubmed/31693124
http://dx.doi.org/10.1001/jamanetworkopen.2019.14645
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