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Computer-aided diagnosis using deep learning in the evaluation of early oesophageal adenocarcinoma
(2019)
Computer-aided diagnosis using deep learning (CAD-DL) may be an instrument to improve endoscopic assessment of Barrett’s oesophagus
(BE) and early oesophageal adenocarcinoma (EAC). Based on still images from two databases, the diagnosis of EAC by CAD-DL reached sensitivities/specificities of 97%/88% (Augsburg data) and 92%/100% (Medical Image Computing and Computer-Assisted Intervention [MICCAI]
data) for white light (WL) images and 94%/80% for narrow band images (NBI) (Augsburg data), respectively. Tumour margins delineated by
experts into images were detected satisfactorily with a Dice coefficient (D) of 0.72. This could be a first step towards CAD-DL for BE assessment. If developed further, it could become a useful
adjunctive tool for patient management.
The number of patients with Barret’s esophagus (BE) has increased in the last decades. Considering the dangerousness of the disease and its evolution to adenocarcinoma, an early diagnosis of BE may provide a high probability of cancer remission. However, limitations regarding traditional methods of detection and management of BE demand alternative solutions. As such, computer-aided tools have been recently used to assist in this problem, but the challenge still persists. To manage the problem, we introduce the infinity Restricted Boltzmann Machines (iRBMs) to the task of automatic identification of Barrett’s esophagus from endoscopic images of the lower esophagus. Moreover, since iRBM requires a proper selection of its meta-parameters, we also present a discriminative iRBM fine-tuning using six meta-heuristic optimization techniques. We showed that iRBMs are suitable for the context since it provides competitive results, as well as the meta-heuristic techniques showed to be appropriate for such task.
The growing number of publications on the application of artificial intelligence (AI) in medicine underlines the enormous importance and potential of this emerging field of research.
In gastrointestinal endoscopy, AI has been applied to all segments of the gastrointestinal tract most importantly in the detection and characterization of colorectal polyps. However, AI research has been published also in the stomach and esophagus for both neoplastic and non-neoplastic disorders.
The various technical as well as medical aspects of AI, however, remain confusing especially for non-expert physicians.
This physician-engineer co-authored review explains the basic technical aspects of AI and provides a comprehensive overview of recent publications on AI in gastrointestinal endoscopy. Finally, a basic insight is offered into understanding publications on AI in gastrointestinal endoscopy.
Based on previous work by our group with manual annotation of visible Barrett oesophagus (BE) cancer images, a real-time deep learning artificial intelligence (AI) system was developed. While an expert endoscopist conducts the endoscopic assessment of BE, our AI system captures random images from the real-time camera livestream and provides a global prediction (classification), as well as a dense prediction (segmentation) differentiating accurately between normal BE and early oesophageal adenocarcinoma (EAC). The AI system showed an accuracy of 89.9% on 14 cases with neoplastic BE.
Barrett's esophagus figured a swift rise in the number of cases in the past years. Although traditional diagnosis methods offered a vital role in early-stage treatment, they are generally time- and resource-consuming. In this context, computer-aided approaches for automatic diagnosis emerged in the literature since early detection is intrinsically related to remission probabilities. However, they still suffer from drawbacks because of the lack of available data for machine learning purposes, thus implying reduced recognition rates. This work introduces Generative Adversarial Networks to generate high-quality endoscopic images, thereby identifying Barrett's esophagus and adenocarcinoma more precisely. Further, Convolution Neural Networks are used for feature extraction and classification purposes. The proposed approach is validated over two datasets of endoscopic images, with the experiments conducted over the full and patch-split images. The application of Deep Convolutional Generative Adversarial Networks for the data augmentation step and LeNet-5 and AlexNet for the classification step allowed us to validate the proposed methodology over an extensive set of datasets (based on original and augmented sets), reaching results of 90% of accuracy for the patch-based approach and 85% for the image-based approach. Both results are based on augmented datasets and are statistically different from the ones obtained in the original datasets of the same kind. Moreover, the impact of data augmentation was evaluated in the context of image description and classification, and the results obtained using synthetic images outperformed the ones over the original datasets, as well as other recent approaches from the literature. Such results suggest promising insights related to the importance of proper data for the accurate classification concerning computer-assisted Barrett's esophagus and adenocarcinoma detection.
Pixel-level classification is an essential part of computer vision. For learning from labeled data, many powerful deep learning models have been developed recently. In this work, we augment such supervised segmentation models by allowing them to learn from unlabeled data. Our semi-supervised approach, termed Error-Correcting Supervision, leverages a collaborative strategy. Apart from the supervised training on the labeled data, the segmentation network is judged by an additional network. The secondary correction network learns on the labeled data to optimally spot correct predictions, as well as to amend incorrect ones. As auxiliary regularization term, the corrector directly influences the supervised training of the segmentation network. On unlabeled data, the output of the correction network is essential to create a proxy for the unknown truth. The corrector’s output is combined with the segmentation network’s prediction to form the new target. We propose a loss function that incorporates both the pseudo-labels as well as the predictive certainty of the correction network. Our approach can easily be added to supervised segmentation models. We show consistent improvements over a supervised baseline on experiments on both the Pascal VOC 2012 and the Cityscapes datasets with varying amounts of labeled data.
Even though artificial intelligence and machine learning have demonstrated remarkable performances in medical image computing, their level of accountability and transparency must be provided in such evaluations. The reliability related to machine learning predictions must be explained and interpreted, especially if diagnosis support is addressed. For this task, the black-box nature of deep learning techniques must be lightened up to transfer its promising results into clinical practice. Hence, we aim to investigate the use of explainable artificial intelligence techniques to quantitatively highlight discriminative regions during the classification of earlycancerous tissues in Barrett’s esophagus-diagnosed patients. Four Convolutional Neural Network models (AlexNet, SqueezeNet, ResNet50, and VGG16) were analyzed using five different interpretation techniques (saliency, guided backpropagation, integrated gradients, input × gradients, and DeepLIFT) to compare their agreement with experts’ previous annotations of cancerous tissue. We could show that saliency attributes match best with the manual experts’ delineations. Moreover, there is moderate to high correlation between the sensitivity of a model and the human-and-computer agreement. The results also lightened that the higher the model’s sensitivity, the stronger the correlation of human and computational segmentation agreement. We observed a relevant relation between computational learning and experts’ insights, demonstrating how human knowledge may influence the correct computational learning.
Aims
Eosinophilic esophagitis (EoE) is easily missed during endoscopy, either because physicians are not familiar with its endoscopic features or the morphologic changes are too subtle. In this preliminary paper, we present the first attempt to detect EoE in endoscopic white light (WL) images using a deep learning network (EoE-AI).
Methods
401 WL images of eosinophilic esophagitis and 871 WL images of normal esophageal mucosa were evaluated. All images were assessed for the Endoscopic Reference score (EREFS) (edema, rings, exudates, furrows, strictures). Images with strictures were excluded. EoE was defined as the presence of at least 15 eosinophils per high power field on biopsy. A convolutional neural network based on the ResNet architecture with several five-fold cross-validation runs was used. Adding auxiliary EREFS-classification branches to the neural network allowed the inclusion of the scores as optimization criteria during training. EoE-AI was evaluated for sensitivity, specificity, and F1-score. In addition, two human endoscopists evaluated the images.
Results
EoE-AI showed a mean sensitivity, specificity, and F1 of 0.759, 0.976, and 0.834 respectively, averaged over the five distinct cross-validation runs. With the EREFS-augmented architecture, a mean sensitivity, specificity, and F1-score of 0.848, 0.945, and 0.861 could be demonstrated respectively. In comparison, the two human endoscopists had an average sensitivity, specificity, and F1-score of 0.718, 0.958, and 0.793.
Conclusions
To the best of our knowledge, this is the first application of deep learning to endoscopic images of EoE which were also assessed after augmentation with the EREFS-score. The next step is the evaluation of EoE-AI using an external dataset. We then plan to assess the EoE-AI tool on endoscopic videos, and also in real-time. This preliminary work is encouraging regarding the ability for AI to enhance physician detection of EoE, and potentially to do a true “optical biopsy” but more work is needed.
Aims
Celiac disease (CD) is a complex condition caused by an autoimmune reaction to ingested gluten. Due to its polymorphic manifestation and subtle endoscopic presentation, the diagnosis is difficult and thus the disorder is underreported. We aimed to use deep learning to identify celiac disease on endoscopic images of the small bowel.
Methods
Patients with small intestinal histology compatible with CD (MARSH classification I-III) were extracted retrospectively from the database of Augsburg University hospital. They were compared to patients with no clinical signs of CD and histologically normal small intestinal mucosa. In a first step MARSH III and normal small intestinal mucosa were differentiated with the help of a deep learning algorithm. For this, the endoscopic white light images were divided into five equal-sized subsets. We avoided splitting the images of one patient into several subsets. A ResNet-50 model was trained with the images from four subsets and then validated with the remaining subset. This process was repeated for each subset, such that each subset was validated once. Sensitivity, specificity, and harmonic mean (F1) of the algorithm were determined.
Results
The algorithm showed values of 0.83, 0.88, and 0.84 for sensitivity, specificity, and F1, respectively. Further data showing a comparison between the detection rate of the AI model and that of experienced endoscopists will be available at the time of the upcoming conference.
Conclusions
We present the first clinical report on the use of a deep learning algorithm for the detection of celiac disease using endoscopic images. Further evaluation on an external data set, as well as in the detection of CD in real-time, will follow. However, this work at least suggests that AI can assist endoscopists in the endoscopic diagnosis of CD, and ultimately may be able to do a true optical biopsy in live-time.
Barrett's esophagus denotes a disorder in the digestive system that affects the esophagus' mucosal cells, causing reflux, and showing potential convergence to esophageal adenocarcinoma if not treated in initial stages. Thus, fast and reliable computer-aided diagnosis becomes considerably welcome. Nevertheless, such approaches usually suffer from imbalanced datasets, which can be addressed through Generative Adversarial Networks (GANs). Such techniques generate realistic images based on observed samples, even though at the cost of a proper selection of its hyperparameters. Many works employed a class of nature-inspired algorithms called metaheuristics to tackle the problem considering distinct deep learning approaches. Therefore, this paper's main contribution is to introduce metaheuristic techniques to fine-tune GANs in the context of Barrett's esophagus identification, as well as to investigate the feasibility of generating high-quality synthetic images for early-cancer assisted identification.
Pixel-level classification is an essential part of computer vision. For learning from labeled data, many powerful deep learning models have been developed recently. In this work, we augment such supervised segmentation models by allowing them to learn from unlabeled data. Our semi-supervised approach, termed Error-Correcting Supervision, leverages a collaborative strategy. Apart from the supervised training on the labeled data, the segmentation network is judged by an additional network.
Background and aims: The accurate differentiation between T1a and T1b Barrett’s cancer has both therapeutic and prognostic implications but is challenging even for experienced physicians. We trained an Artificial Intelligence (AI) system on the basis of deep artificial neural networks (deep learning) to differentiate between T1a and T1b Barrett’s cancer white-light images.
Methods: Endoscopic images from three tertiary care centres in Germany were collected retrospectively. A deep learning system was trained and tested using the principles of cross-validation. A total of 230 white-light endoscopic images (108 T1a and 122 T1b) was evaluated with the AI-system. For comparison, the images were also classified by experts specialized in endoscopic diagnosis and treatment of Barrett’s cancer.
Results: The sensitivity, specificity, F1 and accuracy of the AI-system in the differentiation between T1a and T1b cancer lesions was 0.77, 0.64, 0.73 and 0.71, respectively. There was no statistically significant difference between the performance of the AI-system and that of human experts with sensitivity, specificity, F1 and accuracy of 0.63, 0.78, 0.67 and 0.70 respectively.
Conclusion: This pilot study demonstrates the first multicenter application of an AI-based system in the prediction of submucosal invasion in endoscopic images of Barrett’s cancer. AI scored equal to international experts in the field, but more work is necessary to improve the system and apply it to video sequences and in a real-life setting. Nevertheless, the correct prediction of submucosal invasion in Barret´s cancer remains challenging for both experts and AI.
Clinical setting
Third space procedures such as endoscopic submucosal dissection (ESD) and peroral endoscopic myotomy (POEM) are complex minimally invasive techniques with an elevated risk for operator-dependent adverse events such as bleeding and perforation. This risk arises from accidental dissection into the muscle layer or through submucosal blood vessels as the submucosal cutting plane within the expanding resection site is not always apparent. Deep learning algorithms have shown considerable potential for the detection and characterization of gastrointestinal lesions. So-called AI – clinical decision support solutions (AI-CDSS) are commercially available for polyp detection during colonoscopy. Until now, these computer programs have concentrated on diagnostics whereas an AI-CDSS for interventional endoscopy has not yet been introduced. We aimed to develop an AI-CDSS („Smart ESD“) for real-time intra-procedural detection and delineation of blood vessels, tissue structures and endoscopic instruments during third-space endoscopic procedures.
Characteristics of Smart ESD
An AI-CDSS was invented that delineates blood vessels, tissue structures and endoscopic instruments during third-space endoscopy in real-time. The output can be displayed by an overlay over the endoscopic image with different modes of visualization, such as a color-coded semitransparent area overlay, or border tracing (demonstration video). Hereby the optimal layer for dissection can be visualized, which is close above or directly at the muscle layer, depending on the applied technique (ESD or POEM). Furthermore, relevant blood vessels (thickness> 1mm) are delineated. Spatial proximity between the electrosurgical knife and a blood vessel triggers a warning signal. By this guidance system, inadvertent dissection through blood vessels could be averted.
Technical specifications
A DeepLabv3+ neural network architecture with KSAC and a 101-layer ResNeSt backbone was used for the development of Smart ESD. It was trained and validated with 2565 annotated still images from 27 full length third-space endoscopic videos. The annotation classes were blood vessel, submucosal layer, muscle layer, electrosurgical knife and endoscopic instrument shaft. A test on a separate data set yielded an intersection over union (IoU) of 68%, a Dice Score of 80% and a pixel accuracy of 87%, demonstrating a high overlap between expert and AI segmentation. Further experiments on standardized video clips showed a mean vessel detection rate (VDR) of 85% with values of 92%, 70% and 95% for POEM, rectal ESD and esophageal ESD respectively. False positive measurements occurred 0.75 times per minute. 7 out of 9 vessels which caused intraprocedural bleeding were caught by the algorithm, as well as both vessels which required hemostasis via hemostatic forceps.
Future perspectives
Smart ESD performed well for vessel and tissue detection and delineation on still images, as well as on video clips. During a live demonstration in the endoscopy suite, clinical applicability of the innovation was examined. The lag time for processing of the live endoscopic image was too short to be visually detectable for the interventionist. Even though the algorithm could not be applied during actual dissection by the interventionist, Smart ESD appeared readily deployable during visual assessment by ESD experts. Therefore, we plan to conduct a clinical trial in order to obtain CE-certification of the algorithm. This new technology may improve procedural safety and speed, as well as training of modern minimally invasive endoscopic resection techniques.
The endoscopic features associated with eosinophilic esophagitis (EoE) may be missed during routine endoscopy. We aimed to develop and evaluate an Artificial Intelligence (AI) algorithm for detecting and quantifying the endoscopic features of EoE in white light images, supplemented by the EoE Endoscopic Reference Score (EREFS). An AI algorithm (AI-EoE) was constructed and trained to differentiate between EoE and normal esophagus using endoscopic white light images extracted from the database of the University Hospital Augsburg. In addition to binary classification, a second algorithm was trained with specific auxiliary branches for each EREFS feature (AI-EoE-EREFS). The AI algorithms were evaluated on an external data set from the University of North Carolina, Chapel Hill (UNC), and compared with the performance of human endoscopists with varying levels of experience. The overall sensitivity, specificity, and accuracy of AI-EoE were 0.93 for all measures, while the AUC was 0.986. With additional auxiliary branches for the EREFS categories, the AI algorithm (AI-EoEEREFS) performance improved to 0.96, 0.94, 0.95, and 0.992 for sensitivity, specificity, accuracy, and AUC, respectively. AI-EoE and AI-EoE-EREFS performed significantly better than endoscopy beginners and senior fellows on the same set of images. An AI algorithm can be trained to detect and quantify endoscopic features of EoE with excellent performance scores. The addition of the EREFS criteria improved the performance of the AI algorithm, which performed significantly better than endoscopists with a lower or medium experience level.
Semantic segmentation is an essential task in medical imaging research. Many powerful deep-learning-based approaches can be employed for this problem, but they are dependent on the availability of an expansive labeled dataset. In this work, we augment such supervised segmentation models to be suitable for learning from unlabeled data. Our semi-supervised approach, termed Error-Correcting Mean-Teacher, uses an exponential moving average model like the original Mean Teacher but introduces our new paradigm of error correction. The original segmentation network is augmented to handle this secondary correction task. Both tasks build upon the core feature extraction layers of the model. For the correction task, features detected in the input image are fused with features detected in the predicted segmentation and further processed with task-specific decoder layers. The combination of image and segmentation features allows the model to correct present mistakes in the given input pair. The correction task is trained jointly on the labeled data. On unlabeled data, the exponential moving average of the original network corrects the student’s prediction. The combined outputs of the students’ prediction with the teachers’ correction form the basis for the semi-supervised update. We evaluate our method with the 2017 and 2018 Robotic Scene Segmentation data, the ISIC 2017 and the BraTS 2020 Challenges, a proprietary Endoscopic Submucosal Dissection dataset, Cityscapes, and Pascal VOC 2012. Additionally, we analyze the impact of the individual components and examine the behavior when the amount of labeled data varies, with experiments performed on two distinct segmentation architectures. Our method shows improvements in terms of the mean Intersection over Union over the supervised baseline and competing methods. Code is available at https://github.com/CloneRob/ECMT.
Aims
Evaluation of the add-on effect an artificial intelligence (AI) based clinical decision support system has on the performance of endoscopists with different degrees of expertise in the field of Barrett's esophagus (BE) and Barrett's esophagus-related neoplasia (BERN).
Methods
The support system is based on a multi-task deep learning model trained to solve a segmentation and several classification tasks. The training approach represents an extension of the ECMT semi-supervised learning algorithm. The complete system evaluates a decision tree between estimated motion, classification, segmentation, and temporal constraints, to decide when and how the prediction is highlighted to the observer. In our current study, ninety-six video cases of patients with BE and BERN were prospectively collected and assessed by Barrett's specialists and non-specialists. All video cases were evaluated twice – with and without AI assistance. The order of appearance, either with or without AI support, was assigned randomly. Participants were asked to detect and characterize regions of dysplasia or early neoplasia within the video sequences.
Results
Standalone sensitivity, specificity, and accuracy of the AI system were 92.16%, 68.89%, and 81.25%, respectively. Mean sensitivity, specificity, and accuracy of expert endoscopists without AI support were 83,33%, 58,20%, and 71,48 %, respectively. Gastroenterologists without Barrett's expertise but with AI support had a comparable performance with a mean sensitivity, specificity, and accuracy of 76,63%, 65,35%, and 71,36%, respectively.
Conclusions
Non-Barrett's experts with AI support had a similar performance as experts in a video-based study.
Aims
AI has proven great potential in assisting endoscopists in diagnostics, however its role in therapeutic endoscopy remains unclear. Endoscopic submucosal dissection (ESD) is a technically demanding intervention with a slow learning curve and relevant risks like bleeding and perforation. Therefore, we aimed to develop an algorithm for the real-time detection and delineation of relevant structures during third-space endoscopy.
Methods
5470 still images from 59 full length videos (47 ESD, 12 POEM) were annotated. 179681 additional unlabeled images were added to the training dataset. Consequently, a DeepLabv3+ neural network architecture was trained with the ECMT semi-supervised algorithm (under review elsewhere). Evaluation of vessel detection was performed on a dataset of 101 standardized video clips from 15 separate third-space endoscopy videos with 200 predefined blood vessels.
Results
Internal validation yielded an overall mean Dice score of 85% (68% for blood vessels, 86% for submucosal layer, 88% for muscle layer). On the video test data, the overall vessel detection rate (VDR) was 94% (96% for ESD, 74% for POEM). The median overall vessel detection time (VDT) was 0.32 sec (0.3 sec for ESD, 0.62 sec for POEM).
Conclusions
Evaluation of the developed algorithm on a video test dataset showed high VDR and quick VDT, especially for ESD. Further research will focus on a possible clinical benefit of the AI application for VDR and VDT during third-space endoscopy.
Real-time computational speed and a high degree of precision are requirements for computer-assisted interventions. Applying a segmentation network to a medical video processing task can introduce significant inter-frame prediction noise. Existing approaches can reduce inconsistencies by including temporal information but often impose requirements on the architecture or dataset. This paper proposes a method to include temporal information in any segmentation model and, thus, a technique to improve video segmentation performance without alterations during training or additional labeling. With Motion-Corrected Moving Average, we refine the exponential moving average between the current and previous predictions. Using optical flow to estimate the movement between consecutive frames, we can shift the prior term in the moving-average calculation to align with the geometry of the current frame. The optical flow calculation does not require the output of the model and can therefore be performed in parallel, leading to no significant runtime penalty for our approach. We evaluate our approach on two publicly available segmentation datasets and two proprietary endoscopic datasets and show improvements over a baseline approach.