Real-time computer-aided diagnosis of focal pancreatic masses from endoscopic ultrasound imaging based on a hybrid convolutional and long short-term memory neural network model

Anca Loredana Udriștoiu, Irina Mihaela Cazacu, Lucian Gheorghe Gruionu, Gabriel Gruionu, Andreea Valentina Iacob, Daniela Elena Burtea, Bogdan Silviu Ungureanu, Mădălin Ionuț Costache, Alina Constantin, Carmen Florina Popescu, Ștefan Udriștoiu, Adrian Săftoiu, Anca Loredana Udriștoiu, Irina Mihaela Cazacu, Lucian Gheorghe Gruionu, Gabriel Gruionu, Andreea Valentina Iacob, Daniela Elena Burtea, Bogdan Silviu Ungureanu, Mădălin Ionuț Costache, Alina Constantin, Carmen Florina Popescu, Ștefan Udriștoiu, Adrian Săftoiu

Abstract

Differential diagnosis of focal pancreatic masses is based on endoscopic ultrasound (EUS) guided fine needle aspiration biopsy (EUS-FNA/FNB). Several imaging techniques (i.e. gray-scale, color Doppler, contrast-enhancement and elastography) are used for differential diagnosis. However, diagnosis remains highly operator dependent. To address this problem, machine learning algorithms (MLA) can generate an automatic computer-aided diagnosis (CAD) by analyzing a large number of clinical images in real-time. We aimed to develop a MLA to characterize focal pancreatic masses during the EUS procedure. The study included 65 patients with focal pancreatic masses, with 20 EUS images selected from each patient (grayscale, color Doppler, arterial and venous phase contrast-enhancement and elastography). Images were classified based on cytopathology exam as: chronic pseudotumoral pancreatitis (CPP), neuroendocrine tumor (PNET) and ductal adenocarcinoma (PDAC). The MLA is based on a deep learning method which combines convolutional (CNN) and long short-term memory (LSTM) neural networks. 2688 images were used for training and 672 images for testing the deep learning models. The CNN was developed to identify the discriminative features of images, while a LSTM neural network was used to extract the dependencies between images. The model predicted the clinical diagnosis with an area under curve index of 0.98 and an overall accuracy of 98.26%. The negative (NPV) and positive (PPV) predictive values and the corresponding 95% confidential intervals (CI) are 96.7%, [94.5, 98.9] and 98.1%, [96.81, 99.4] for PDAC, 96.5%, [94.1, 98.8], and 99.7%, [99.3, 100] for CPP, and 98.9%, [97.5, 100] and 98.3%, [97.1, 99.4] for PNET. Following further validation on a independent test cohort, this method could become an efficient CAD tool to differentiate focal pancreatic masses in real-time.

Conflict of interest statement

The authors have read the journal’s policy and the authors of this manuscript have the following competing interests: SU is an unpaid consultant for INNES Worldwide. There are no patents, products in development or marketing products to declare. This does not alter our adherence to PLOS ONE policies on sharing data and materials.

Figures

Fig 1
Fig 1
EUS imaging of a pseudotumoral chronic pancreatitis in (A) gray scale. (B) elastography. (C) color Doppler. (D) contrast enhancement–arterial phase. (E) contrast enhancement–venous phase.
Fig 2
Fig 2
EUS imaging of a neuroendocrine tumor in (A) gray scale. (B) elastography. (C) color Doppler. (D) contrast enhancement–arterial phase. (E) contrast enhancement–venous phase.
Fig 3
Fig 3
EUS imaging of a pancreatic ductal adenocarcinoma in (A) gray scale. (B) elastography. (C) color Doppler. (D) contrast enhancement–arterial phase. (E) contrast enhancement–venous phase.
Fig 4. The architecture of the CNN-LSTM…
Fig 4. The architecture of the CNN-LSTM model.
Fig 5. The comparison between the accuracy…
Fig 5. The comparison between the accuracy of the training and the testing datasets.
Fig 6. The comparison between the loss…
Fig 6. The comparison between the loss of the training and validation datasets.
Fig 7. The ROC curves computed for…
Fig 7. The ROC curves computed for CNN-LSTM method.
Fig 8. The precision/recall curves computed for…
Fig 8. The precision/recall curves computed for CNN-LSTM method.

References

    1. Cancer Stat Facts: Pancreatic Cancer. 2018. [cited 2019 Aug 1]. Available from: .
    1. Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA: A Cancer Journal for Clinicians. 2018; 68:394–424.
    1. Kitano M, Yoshida T, Itonaga M, Tamura T, Hatamaru K, Yamashita Y. Impact of endoscopic ultrasonography on diagnosis of pancreatic cancer. J Gastroenterol. 2019;54:19–32. doi: 10.1007/s00535-018-1519-2
    1. Litjens G, Kooi T, Bejnordi BE, Setio AAA, Ciompi F, Ghafoorian M, et al.. A survey on deep learning in medical image analysis. Medical Image Analysis. 2017; 42:60–88. doi: 10.1016/j.media.2017.07.005
    1. Christ PF, Elshaer MEA, Ettlinger F, Tatavarty S, Bickel M, Bilic P, et al.. Automatic liver and lesion segmentation in CT using cascaded fully convolutional neural networks and 3D conditional random fields. Proceedings of International Conference on Medical Image Computing and Computer-Assisted Intervention. 2016: 415–23.
    1. Thong W, Kadoury S, Piché N, Pal CJ. Convolutional networks for kidney segmentation in contrast-enhanced CT scans. Computer Methods in Biomechanics and Biomedical Engineering: Imaging & Visualization. 2018; 6:277–82.
    1. Cai J, Lu L, Zhang Z, Xing F, Yang L, Yin Q. Pancreas segmentation in MRI using graph-based decision fusion on convolutional neural networks. Proceedings of International Conference on Medical Image Computing and Computer-Assisted Intervention. 2016: 442–50. doi: 10.1007/978-3-319-46723-8_51
    1. Lu N, Wu Y, Feng L, Song J. Deep learning for fall detection: Three-dimensional CNN combined with LSTM on video kinematic data. IEEE Journal of Biomedical and Health Informatics. 2018; 23:314–23. doi: 10.1109/JBHI.2018.2808281
    1. Donahue J, Anne Hendricks L, Guadarrama S, Rohrbach M, Venugopalan S, Darrell T, et al.. Long-term recurrent convolutional networks for visual recognition and description. Proceedings of the IEEE Conference on Computer Vision and Pattern Recognition. 2015: 2625–34.
    1. Nair VJ, Szanto J, Vandervoort E, Henderson E, Avruch L, Malone S. Feasibility, detectability and clinical experience with platinum fiducial seeds for MRI/CT fusion and real-time tumor tracking during CyberKnife® stereotactic ablative radiotherapy. Journal of Radiosurgery and SBRT. 2015;3:315.
    1. Srivastava N, Hinton G, Krizhevsky A, Sutskever I, Salakhutdinov R. Dropout: a simple way to prevent neural networks from overfitting. The Journal of Machine Learning Research. 2014;15:1929–58.
    1. Keras: Deep learning for Python. [cited 2019 May 20]. Available from: .
    1. Walt SV, Colbert SC, Varoquaux G. The NumPy array: a structure for efficient numerical computation. Computing in Science & Engineering. 2011;13:22–30.
    1. Pedregosa F, Varoquaux G, Gramfort A, Michel V, Thirion B. Scikit-learn: Machine learning in Python. Journal of Machine Learning Research. 2011; 12:2825–30.
    1. Mercaldo ND, Lau KF, Zhou XH. Confidence intervals for predictive values with an emphasis to case–control studies. Statistics in medicine. 2017; 26(10): 2170–2183.
    1. Saito T, Rehmsmeier M. The precision-recall plot is more informative than the ROC plot when evaluating binary classifiers on imbalanced datasets. PloS One. 2015;10(3): e0118432. doi: 10.1371/journal.pone.0118432
    1. Dodge S, Karam L. Understanding how image quality affects deep neural networks. Proceedings of Eighth International Conference on Quality of Multimedia Experience. 2016: 1–6.
    1. Zhu M, Xu C, Yu J, Wu Y, Li C, Zhang M, et al.. Differentiation of pancreatic cancer and chronic pancreatitis using computer-aided diagnosis of endoscopic ultrasound (EUS) images: a diagnostic test. PLoS One. 2013; 8(5):e63820. doi: 10.1371/journal.pone.0063820
    1. Das A, Nguyen CC, Li F, Li B. Digital image analysis of EUS images accurately differentiates pancreatic cancer from chronic pancreatitis and normal tissue. Gastrointestinal Endoscopy. 2008; 67: 861–7. doi: 10.1016/j.gie.2007.08.036
    1. Ozkan M, Cakiroglu M, Kocaman O, Kurt M, Yilmaz B, Can G, et al.. Age-based computer-aided diagnosis approach for pancreatic cancer on endoscopic ultrasound images. Endoscopic Ultrasound. 2016; 5(2):101–107. doi: 10.4103/2303-9027.180473
    1. Kuwahara T, Hara K, Mizuno N, Okuno N, Matsumoto S, Obata M, et al.. Usefulness of Deep Learning Analysis for the Diagnosis of Malignancy in Intraductal Papillary Mucinous Neoplasms of the Pancreas. Clinical and Translational Gastroenterology. 2019;10(5):1–8.
    1. Kurita Y, Kuwahara T, Hara K, Mizuno N, Okuno N, Matsumoto S, et al.. Diagnostic ability of artificial intelligence using deep learning analysis of cyst fluid in differentiating malignant from benign pancreatic cystic lesions. Scientific reports. 2019;9(1):6893. doi: 10.1038/s41598-019-43314-3

Source: PubMed

3
Iratkozz fel