A bi-atrial statistical shape model for large-scale in silico studies of human atria: Model development and application to ECG simulations

Large-scale electrophysiological simulations to obtain electrocardiograms (ECG) carry the potential to produce extensive datasets for training of machine learning classifiers to, e.g., discriminate between different cardiac pathologies. The adoption of simulations for these purposes is limited due to a lack of ready-to-use models covering atrial anatomical variability. We built a bi-atrial statistical shape model (SSM) of the endocardial wall based on 47 segmented human CT and MRI datasets using Gaussian process morphable models. Generalization, specificity, and compactness metrics were evaluated. The SSM was applied to simulate atrial ECGs in 100 random volumetric instances. The first eigenmode of our SSM reflects a change of the total volume of both atria, the second the asymmetry between left vs. right atrial volume, the third a change in the prominence of the atrial appendages. The SSM is capable of generalizing well to unseen geometries and 95% of the total shape variance is covered by its first 24 eigenvectors. The P waves in the 12-lead ECG of 100 random instances showed a duration of 109.7±12.2 ms in accordance with large cohort studies. The novel bi-atrial SSM itself as well as 100 exemplary instances with rule-based augmentation of atrial wall thickness, fiber orientation, inter-atrial bridges and tags for anatomical structures have been made publicly available. This novel, openly available bi-atrial SSM can in future be employed to generate large sets of realistic atrial geometries as a basis for in silico big data approaches.

[1]  Mathias Wilhelms,et al.  Influence of chronic atrial fibrillation induced remodeling in a computational electrophysiological model , 2014 .

[2]  Gernot Plank,et al.  Efficient computation of electrograms and ECGs in human whole heart simulations using a reaction-eikonal model☆ , 2017, J. Comput. Phys..

[3]  A. Loewe Modeling Human Atrial Patho-Electrophysiology from Ion Channels to ECG - Substrates, Pharmacology, Vulnerability, and P-Waves , 2016 .

[4]  Christophe Geuzaine,et al.  Gmsh: A 3‐D finite element mesh generator with built‐in pre‐ and post‐processing facilities , 2009 .

[5]  U. Schotten,et al.  Beat-to-beat P-wave morphological variability in patients with paroxysmal atrial fibrillation: an in silico study. , 2018, Europace : European pacing, arrhythmias, and cardiac electrophysiology : journal of the working groups on cardiac pacing, arrhythmias, and cardiac cellular electrophysiology of the European Society of Cardiology.

[6]  Olaf Dössel,et al.  Modelling of patient-specific Purkinje activation based on measured ECGs , 2017 .

[7]  Douglas W Mahoney,et al.  Left atrial volume as an index of left atrial size: a population-based study. , 2003, Journal of the American College of Cardiology.

[8]  Anders Logg,et al.  The FEniCS Project Version 1.5 , 2015 .

[9]  S. Schuler,et al.  A Bi-atrial Statistical Shape Model and 100 Volumetric Anatomical Models of the Atria , 2020 .

[10]  Jürgen Weese,et al.  Benchmark for Algorithms Segmenting the Left Atrium From 3D CT and MRI Datasets , 2015, IEEE Transactions on Medical Imaging.

[11]  Armin Luik,et al.  Non-Invasive Characterization of Atrial Flutter Mechanisms Using Recurrence Quantification Analysis on the ECG: A Computational Study , 2020, IEEE Transactions on Biomedical Engineering.

[12]  G. Plank,et al.  openCARP: An Open Sustainable Framework for In-Silico Cardiac Electrophysiology Research , 2020, 2020 Computing in Cardiology.

[13]  Ali Bahrami Rad,et al.  Classification of 12-lead ECGs: the PhysioNet/Computing in Cardiology Challenge 2020 , 2020, 2020 Computing in Cardiology.

[14]  Masoumeh Haghpanahi,et al.  Cardiologist-level arrhythmia detection and classification in ambulatory electrocardiograms using a deep neural network , 2019, Nature Medicine.

[15]  Alejandro F Frangi,et al.  Computational Anatomy Atlas of the Heart , 2007, 2007 5th International Symposium on Image and Signal Processing and Analysis.

[16]  Alfio Quarteroni,et al.  The Impact of Left Atrium Appendage Morphology on Stroke Risk Assessment in Atrial Fibrillation: A Computational Fluid Dynamics Study , 2019, Front. Physiol..

[17]  Cesare Corrado,et al.  CemrgApp: An interactive medical imaging application with image processing, computer vision, and machine learning toolkits for cardiovascular research , 2020, SoftwareX.

[18]  Matti Stenroos,et al.  A Matlab library for solving quasi-static volume conduction problems using the boundary element method , 2007, Comput. Methods Programs Biomed..

[19]  Qianqian Fang,et al.  Improving model-based functional near-infrared spectroscopy analysis using mesh-based anatomical and light-transport models , 2020, Neurophotonics.

[20]  Juha Koikkalainen,et al.  Statistical shape model of atria, ventricles and epicardium from short- and long-axis MR images , 2004, Medical Image Anal..

[21]  Rhodri H. Davies,et al.  Learning Shape: Optimal Models for Analysing Natural Variability , 2004 .

[22]  O. Dössel,et al.  Automatic ECG-based Discrimination of 20 Atrial Flutter Mechanisms: Influence of Atrial and Torso Geometries , 2020, 2020 Computing in Cardiology.

[23]  Børge G Nordestgaard,et al.  P-wave duration and the risk of atrial fibrillation: Results from the Copenhagen ECG Study. , 2015, Heart rhythm.

[24]  Pablo Lamata,et al.  Novel Computational Analysis of Left Atrial Anatomy Improves Prediction of Atrial Fibrillation Recurrence after Ablation , 2017, Frontiers in physiology.

[25]  Oscar Camara,et al.  In silico Optimization of Left Atrial Appendage Occluder Implantation Using Interactive and Modeling Tools , 2019, Front. Physiol..

[26]  Nassir Marrouche,et al.  Computational Shape Models Characterize Shape Change of the Left Atrium in Atrial Fibrillation , 2014, Clinical Medicine Insights. Cardiology.

[27]  Richard James Housden,et al.  Algorithms for left atrial wall segmentation and thickness – Evaluation on an open-source CT and MRI image database , 2018, Medical Image Anal..

[28]  E. Soliman,et al.  The Influence of Left Atrial Enlargement on the Relationship between Atrial Fibrillation and Stroke. , 2016, Journal of stroke and cerebrovascular diseases : the official journal of National Stroke Association.

[29]  Olaf Dössel,et al.  Influence of the earliest right atrial activation site and its proximity to interatrial connections on P-wave morphology. , 2016, Europace : European pacing, arrhythmias, and cardiac electrophysiology : journal of the working groups on cardiac pacing, arrhythmias, and cardiac cellular electrophysiology of the European Society of Cardiology.

[30]  Daniel J. Perry,et al.  Evaluation of current algorithms for segmentation of scar tissue from late Gadolinium enhancement cardiovascular magnetic resonance of the left atrium: an open-access grand challenge , 2013, Journal of Cardiovascular Magnetic Resonance.

[31]  Joshua Cates,et al.  Left atrial shape predicts recurrence after atrial fibrillation catheter ablation , 2018, Journal of cardiovascular electrophysiology.

[32]  Gérard G. Medioni,et al.  Object modelling by registration of multiple range images , 1992, Image Vis. Comput..

[33]  Vincent Jacquemet,et al.  Changes in P-wave morphology after pulmonary vein isolation: insights from computer simulations. , 2016, Europace : European pacing, arrhythmias, and cardiac electrophysiology : journal of the working groups on cardiac pacing, arrhythmias, and cardiac cellular electrophysiology of the European Society of Cardiology.

[34]  S. Prat-Gonzalez,et al.  Accuracy of left atrial fibrosis detection with cardiac magnetic resonance: correlation of late gadolinium enhancement with endocardial voltage and conduction velocity. , 2020, Europace : European pacing, arrhythmias, and cardiac electrophysiology : journal of the working groups on cardiac pacing, arrhythmias, and cardiac cellular electrophysiology of the European Society of Cardiology.

[35]  Daniel Rueckert,et al.  A bi-ventricular cardiac atlas built from 1000+ high resolution MR images of healthy subjects and an analysis of shape and motion , 2015, Medical Image Anal..

[36]  J A Sethian,et al.  A fast marching level set method for monotonically advancing fronts. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[37]  Olga Sorkine-Hornung,et al.  Instant field-aligned meshes , 2015, ACM Trans. Graph..

[38]  Alejandro F. Frangi,et al.  A High-Resolution Atlas and Statistical Model of the Human Heart From Multislice CT , 2013, IEEE Transactions on Medical Imaging.

[39]  Y. Chun,et al.  Left atrial enlargement is an independent predictor of stroke and systemic embolism in patients with non-valvular atrial fibrillation , 2016, Scientific Reports.

[40]  Mark Potse,et al.  Anatomically-Induced Fibrillation in a 3D Model of the Human Atria , 2018, 2018 Computing in Cardiology Conference (CinC).

[41]  Wojciech Samek,et al.  Deep Learning for ECG Analysis: Benchmarks and Insights from PTB-XL , 2020, IEEE Journal of Biomedical and Health Informatics.

[42]  Mert R. Sabuncu,et al.  Robust Atlas-Based Segmentation of Highly Variable Anatomy: Left Atrium Segmentation , 2010, STACOM/CESC.

[43]  Olaf Dössel,et al.  Spatial Downsampling of Surface Sources in the Forward Problem of Electrocardiography , 2019, FIMH.

[44]  J. Hsu,et al.  Left Atrial Appendage Electrical Isolation as a Target in Atrial Fibrillation. , 2019, JACC. Clinical electrophysiology.

[45]  Olaf Dössel,et al.  Influence of left atrial size on P-wave morphology: differential effects of dilation and hypertrophy. , 2018, Europace : European pacing, arrhythmias, and cardiac electrophysiology : journal of the working groups on cardiac pacing, arrhythmias, and cardiac cellular electrophysiology of the European Society of Cardiology.

[46]  Timothy F. Cootes,et al.  Active Shape Models-Their Training and Application , 1995, Comput. Vis. Image Underst..

[47]  Olaf Dössel,et al.  Mesh structure-independent modeling of patient-specific atrial fiber orientation , 2015 .

[48]  Thomas Gerig,et al.  Gaussian Process Morphable Models , 2016, IEEE Transactions on Pattern Analysis and Machine Intelligence.

[49]  M. Courtemanche,et al.  Ionic mechanisms underlying human atrial action potential properties: insights from a mathematical model. , 1998, The American journal of physiology.

[50]  Hrvoje Jasak,et al.  OpenFOAM: Open source CFD in research and industry , 2009 .

[51]  Bernt Schiele,et al.  Building statistical shape spaces for 3D human modeling , 2015, Pattern Recognit..

[52]  Olaf Dössel,et al.  Patient-Specific Identification of Atrial Flutter Vulnerability–A Computational Approach to Reveal Latent Reentry Pathways , 2019, Front. Physiol..

[53]  Olivier Ecabert,et al.  Automatic Model-Based Segmentation of the Heart in CT Images , 2008, IEEE Transactions on Medical Imaging.

[54]  Mathias Unberath,et al.  Open-source 4D statistical shape model of the heart for x-ray projection imaging , 2015, 2015 IEEE 12th International Symposium on Biomedical Imaging (ISBI).

[55]  Sébastien Ourselin,et al.  A Registration-Based Propagation Framework for Automatic Whole Heart Segmentation of Cardiac MRI , 2010, IEEE Transactions on Medical Imaging.

[56]  B. Chow,et al.  Validation of Two‐Dimensional Methods for Left Atrial Volume Measurement: A Comparison of Echocardiography with Cardiac Computed Tomography , 2013, Echocardiography.

[57]  O. Dössel,et al.  Influence of Gradient and Smoothness of Atrial Wall Thickness on Initiation and Maintenance of Atrial Fibrillation , 2020, 2020 Computing in Cardiology.

[58]  Cesare Corrado,et al.  Quantifying atrial anatomy uncertainty from clinical data and its impact on electro-physiology simulation predictions , 2020, Medical Image Anal..