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Imaging and Modeling the Cardiovascular System

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Imaging and Modeling the Cardiovascular System Imaging and modeling the cardiovascular system Elira Maksuti Doctoral Thesis KTH Royal Institute of Technology School of Technology and Health Department of Medical Engineering SE-141 57 Huddinge, Sweden Karolinska Institutet Department of Molecular Medicine and Surgery Clinical Physiology SE-171 76 Stockholm, Sweden TRITA-STH Report 2016:9 ISSN: 1653-3836 ISRN/KTH/STH/2016:9-SE ISBN: 978-91-7729-192-3 © Elira Maksuti, 2016 Printed in Sweden by Universitetsservice US-AB, Stockholm 2016 Preface This thesis is submitted to the KTH Royal Institute of Technology and Karolinska Institutet (KI) in partial fulfillment of the requirements for the Joint Doctoral Degree in Medical Technology. The work has mainly been performed at KTH School of Technology and Health in Huddinge, Sweden, and KI, Department of Clinical Physiology in Stockholm, Sweden, with Associate Professor Michael Broomé as main supervisor, Associate Professor Anna Bjällmark, Associate Professor Matilda Larsson and Associate Professor Martin Ugander as cosupervisors. Six months were spent at the Laboratory of Hemodynamics and Cardiovascular Technology at the École polytechnique fédérale de Lausanne (EPFL) in Lausanne, Switzerland, where Study III was performed, under the supervision of Professor Nikos Stergiopulos. The research projects were supported by grants from the Swedish Research Council (2012-2800, 2012-2795), VINNOVA VINNMER Marie Curie International Qualification Grant (2011-01365) and the Hans Werthén scholarship from The Royal Swedish Academy of Engineering Sciences (IVA). The thesis will be publicly defended at 10 am, December 9, 2016, in the T2 lecture hall, Hälsovägen 11C, Huddinge, Sweden. i ii Abstract Understanding cardiac pumping function is crucial to guiding diagnosis, predicting outcomes of interventions, and designing medical devices that interact with the cardiovascular system. In turn, better diagnostics and treatment of cardiovascular function would improve the prognosis of cardiovascular diseases, which account for 31% of all global deaths. The heart and the vascular system are strongly coupled, and changes in arterial properties that occur with age and in the presence of pathologies have a significant impact on cardiac function. Because of the complexity of the cardiovascular system and the diversity of disease processes, it is not always possible to understand the role played by each part of the system in the final outcome. Computer simulations of hemodynamics can show how the system is influenced by changes in single or multiple cardiovascular parameters and can be used to test clinically relevant hypotheses. In addition, methods for the detection and quantification of important markers such as elevated arterial stiffness would help reduce the morbidity and mortality related to cardiovascular disease. The general aim of this thesis work was to improve understanding of cardiovascular physiology and develop new methods for assisting clinicians during diagnosis and follow- up of treatment in cardiovascular disease. Both computer simulations and medical imaging were used to reach this goal. In the first study, a new cardiac model based on piston-like motions of the atrioventricular plane was developed in order to deepen the understanding of the forces responsible for filling and emptying of the cardiac chambers. In the second study, the presence of the anatomical basis needed to generate hydraulic forces during diastole was assessed in heathy volunteers. In the third study, a previously validated lumped-parameter model was used to quantify the contribution of arterial and cardiac changes to blood pressure during aging. In the fourth study, in-house software that measures arterial stiffness by ultrasound shear wave elastography (SWE) was developed and validated against mechanical testing. The studies showed that longitudinal movements of the atrioventricular plane can well explain cardiac pumping and that the macroscopic geometry of the heart enables the generation of hydraulic forces that aid ventricular filling. Additionally, simulations showed that structural changes in both the heart and the arterial system contribute to the progression of blood pressure with age. Finally, the SWE technique was validated to accurately measure stiffness in arterial phantoms. Future ex vivo and in vivo studies are needed to determine the technique’s sensitivity and applicability to clinical measurements. Keywords: cardiac pumping, diastolic function, hemodynamics, modeling, simulation, arterial stiffness, ultrasound, shear wave elastography. iii iv Sammanfattning Förståelsen av hjärtats pumpmekanism är central för att kunna ställa diagnos, förutsäga behandlingseffekter och för att kunna utveckla medicinteknisk utrustning inom kardiovaskulär sjukvård. I sin tur skulle bättre diagnostik och behandling kunna förbättra prognosen för hjärt- och kärlsjukdomar, vilka orsakar 31 % av alla dödsfall i världen. Hjärtat och kärlsystemet är sammankopplade och förändringar i blodkärlens egenskaper i samband med åldrande och sjukdom påverkar hjärtats funktion signifikant. Det kardiovaskulära systemets komplexitet och mångfalden av sjukdomar gör att det inte alltid är möjligt att förstå hur en enskild del av systemet påverkar helheten. Datorbaserade simulering av hemodynamik har förmågan att visa hur hela systemet påverkas av förändringar i en enskild eller flera kardiovaskulära parametrar samtidigt. På så sätt kan man testa kliniska hypoteser om sjukdomar eller deras behandling. På liknande sätt kan nya metoder för att detektera och kvantifiera kärlstyvhet också tänkas bidra till att minska sjuklighet och dödlighet relaterad till hjärt- och kärlsjukdomar. Det allmänna syftet med denna avhandling är att förbättra förståelsen av hjärt- och kärlsystemets fysiologi samt att utveckla nya metoder för att kunna stödja klinikerna med diagnostik, behandling och uppföljning av hjärt- och kärlsjukdomar. Både datorbaserade simuleringar och medicinsk bildteknik användes för att nå detta mål. I den första studien utvecklades en modell av hjärtats pumpmekanism baserad på den kolvliknande rörelsen av det atrioventrikulära planet (AV-planet) mellan hjärtats bägge förmak och kammare. Syftet med modellen var att utveckla förståelsen av krafterna som verkar när hjärtrummen fylls och töms. I den andra studien utvärderades om hjärtats anatomi skapar förutsättningar för att generera en hydraulisk kraft under hjärtats fyllnadsfas (diastole) hos friska frivilliga försökspersoner. I den tredje studien användes en tidigare validerad modell för att bestämma hur mycket förändringar i hjärtat och kärlsystemet medverkar till blodtryckets förändringar under åldrande. I fjärde studien utvecklades en egen mjukvara för att kunna mäta kärlstelhet med användning av den ultraljudsbaserade tekniken skjuvvågselastografi (Shear wave elastography − SWE), som sedan validerades med experimentell mekanisk testning. Studierna visade att de longitudinella rörelserna hos AV-planet väl kan förklara hjärtats pumpförmåga och att hjärtats egen geometri ger förutsättningar för att generera hydrauliska krafter som understödjer kammarens fyllnad. Dessutom visade simuleringar att strukturella förändringar i hjärtat och kärlsystemet bägge påverkar ändringar i blodtryck med ålder. Till sist, visades att SWE-tekniken med noggrannhet kunde mäta stelheten i kärlfantomer. Ytterligare ex vivo- och in vivo-studier behövs för att avgöra om tekniken kan användas kliniskt. v vi Riassunto Comprendere il meccanismo attraverso il quale il cuore assolve la sua funzione di pompaggio è fondamentale per poter aiutare la diagnostica, predire il risultato dei trattamenti e progettare strumentazioni biomedicali che interagiscano opportunamente con il sistema cardiovascolare. Migliori strumenti di diagnosi e per il trattamento della funzione cardiovascolare possono migliorare la prognosi delle malattie cardiovascolari, le quali causano il 31% delle morti a livello globale. Il cuore e il sistema vascolare sono fortemente interconnessi. Di conseguenza cambiamenti strutturali delle proprietà delle arterie, che occorrono con l’età e in presenza di patologie, hanno un impatto importante sulla funzione cardiaca. A causa della complessità del sistema cardiovascolare e della varietà dei processi patologici, non è sempre possibile comprendere il ruolo di ciascuna parte del sistema nel funzionamento complessivo. Simulazioni al computer di emodinamica hanno la capacità di mostrare come il sistema sia influenzato dal cambiamento di un singolo o di molteplici parametri cardiovascolari. Le simulazioni permettono anche di testare ipotesi di rilievo clinico. In aggiunta, metodi per misurare marker importanti, come un’elevata rigidezza delle arterie, possono aiutare a ridurre la morbilità e la mortalità associate alle malattie cardiovascolari. L’obiettivo generale del lavoro presentato in questa tesi è stato quello di migliorare la comprensione della fisiologia dell’apparato cardiocircolatorio e sviluppare nuovi metodi per aiutare i medici durante il processo di diagnosi e di monitoraggio dei trattamenti delle malattie cardiovascolari. Per raggiungere quest’obiettivo sono state utilizzate sia simulazioni al computer che tecniche di diagnostica per immagini. Nel primo studio è stato sviluppato un modello cardiaco basato sui movimenti del piano atrioventricolare, i quali possono essere paragonati a quelli di un pistone. L’obiettivo del modello è stato quello di migliorare la comprensione delle forze responsabili del riempimento e dello svuotamento dei ventricoli.
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