Biomechanical Evaluation of Aortic Valve Stenosis by Means of a Virtual Stress Test: A Fluid-Structure Interaction Study.
Aortic hemodynamics
Aortic valve stenosis
Exercise
Fluid–structure Interaction
Valve stress
Journal
Annals of biomedical engineering
ISSN: 1573-9686
Titre abrégé: Ann Biomed Eng
Pays: United States
ID NLM: 0361512
Informations de publication
Date de publication:
13 Nov 2023
13 Nov 2023
Historique:
received:
10
06
2023
accepted:
15
10
2023
medline:
14
11
2023
pubmed:
14
11
2023
entrez:
13
11
2023
Statut:
aheadofprint
Résumé
The impact of aortic valve stenosis (AS) extends beyond the vicinity of the narrowed leaflets into the left ventricle (LV) and into the systemic vasculature because of highly unpredictable valve behavior and complex blood flow in the ascending aorta that can be attributed to the strong interaction between the narrowed cusps and the ejected blood. These effects can become exacerbated during exercise and may have implications for disease progression, accurate diagnosis, and timing of intervention. In this 3-D patient-specific study, we employ strongly coupled fluid-structure interaction (FSI) modeling to perform a comprehensive biomechanical evaluation of systolic ejection dynamics in a stenosed aortic valve (AV) during increasing LV contraction. Our model predictions reveal that the heterogeneous ∆P vs. Q relationship that was observed in our previous clinical study can be attributed to a non-linear increase (by ~ 1.5-fold) in aortic valve area as LV heart rate increases from 70 to 115 bpm. Furthermore, our results show that even for a moderately stenotic valve, increased LV contraction during exercise can lead to high-velocity flow turbulence (Re = 11,700) in the aorta similar to that encountered with a severely stenotic valve (Re ~ 10,000), with concomitant greater viscous loss (~3-fold increase) and elevated wall stress in the ascending aorta. Our FSI predictions also reveal that individual valve cusps undergo distinct and highly non-linear increases (>100%) in stress during exercise, potentially contributing to progressive calcification. Such quantitative biomechanical evaluations from realistic FSI workflows provide insights into disease progression and can be integrated with current stress testing for AS patients to comprehensively predict hemodynamics and valve function under both baseline and exercise conditions.
Identifiants
pubmed: 37957528
doi: 10.1007/s10439-023-03389-6
pii: 10.1007/s10439-023-03389-6
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : American Heart Association
ID : 19TPA34860013
Informations de copyright
© 2023. The Author(s) under exclusive licence to Biomedical Engineering Society.
Références
Abusweireh, A. I., and H. A. Alzaeem. Stress echocardiogram in asymptomatic severe aortic stenosis. Heart Views. 23:33, 2022.
pubmed: 35757449
doi: 10.4103/heartviews.heartviews_37_22
Amindari, A., L. Saltik, K. Kirkkopru, M. Yacoub, and H. C. Yalcin. Assessment of calcified aortic valve leaflet deformations and blood flow dynamics using fluid-structure interaction modeling. Inf. Med. Unlocked. 9:191–199, 2017.
doi: 10.1016/j.imu.2017.09.001
Baek, H., and G. E. Karniadakis. A convergence study of a new partitioned fluid–structure interaction algorithm based on fictitious mass and damping. J. Computa. Phys. 231:629–652, 2012.
doi: 10.1016/j.jcp.2011.09.025
Bahlmann, E., E. Gerdts, D. Cramariuc, C. Gohlke-Baerwolf, C. A. Nienaber, K. Wachtell, R. Seifert, J. B. Chambers, K. H. Kuck, and S. Ray. Prognostic value of energy loss index in asymptomatic aortic stenosis. Circulation. 127:1149–1156, 2013.
pubmed: 23357717
doi: 10.1161/CIRCULATIONAHA.112.078857
Barker, A. J., C. Lanning, and R. Shandas. Quantification of hemodynamic wall shear stress in patients with bicuspid aortic valve using phase-contrast MRI. Ann Biomed. Eng. 38:788–800, 2010.
pubmed: 19953319
doi: 10.1007/s10439-009-9854-3
Barker, A. J., M. Markl, J. Bürk, R. Lorenz, J. Bock, S. Bauer, J. Schulz-Menger, and F. von Knobelsdorff-Brenkenhoff. Bicuspid aortic valve is associated with altered wall shear stress in the ascending aorta. Circulation. 5:457–466, 2012.
pubmed: 22730420
Barker, A. J., P. Van Ooij, K. Bandi, J. Garcia, M. Albaghdadi, P. McCarthy, R. O. Bonow, J. Carr, J. Collins, and S. C. Malaisrie. Viscous energy loss in the presence of abnormal aortic flow. Magn. Resonance Med. 72:620–628, 2014.
pubmed: 24122967
doi: 10.1002/mrm.24962
Brown, M. L., P. A. Pellikka, H. V. Schaff, C. G. Scott, C. J. Mullany, T. M. Sundt, J. A. Dearani, R. C. Daly, and T. A. Orszulak. The benefits of early valve replacement in asymptomatic patients with severe aortic stenosis. J. Thorac. Cardiovasc. Surg. 135:308–315, 2008.
pubmed: 18242258
doi: 10.1016/j.jtcvs.2007.08.058
Causin, P., J.-F. Gerbeau, and F. Nobile. Added-mass effect in the design of partitioned algorithms for fluid–structure problems. Comput. Method Appl. Mech. Eng. 194:4506–4527, 2005.
doi: 10.1016/j.cma.2004.12.005
Chen, J.-H., W. L. K. Chen, K. L. Sider, C. Y. Y. Yip, and C. A. Simmons. β-catenin mediates mechanically regulated, transforming growth factor-β1–induced myofibroblast differentiation of aortic valve interstitial cells. Arteriosclerosis Thrombosis Vascular Biol. 31:590–597, 2011.
pubmed: 21127288
doi: 10.1161/ATVBAHA.110.220061
Chen, Y., and H. Luo. A computational study of the three-dimensional fluid–structure interaction of aortic valve. J. Fluids Struct. 80:332–349, 2018.
doi: 10.1016/j.jfluidstructs.2018.04.009
Cibis, M., K. Jarvis, M. Markl, M. Rose, C. Rigsby, A. J. Barker, and J. J. Wentzel. The effect of resolution on viscous dissipation measured with 4D flow MRI in patients with Fontan circulation: Evaluation using computational fluid dynamics. J. Biomech. 48:2984–2989, 2015.
pubmed: 26298492
pmcid: 5096445
doi: 10.1016/j.jbiomech.2015.07.039
Dweck, M. R., N. A. Boon, and D. E. Newby. Calcific aortic stenosis: A disease of the valve and the myocardium. J. Am. Coll. Cardiol. 60:1854–1863, 2012.
pubmed: 23062541
doi: 10.1016/j.jacc.2012.02.093
Eerdekens, R., P. Tonino, J. Zelis, R. Adrichem, J.-M. Ahn, J. Demandt, A. Eftekhari, M. El Farissi, P. Freeman, and A. R. Ihdayhid. Rationale and design of SAVI-AoS: A physiologic study of patients with symptomatic moderate aortic valve stenosis and preserved left ventricular ejection fraction. IJC Heart Vasculature. 41:101063, 2022.
doi: 10.1016/j.ijcha.2022.101063
Espino, D. M., D. E. Shepherd, and D. W. Hukins. Evaluation of a transient, simultaneous, arbitrary Lagrange–Euler based multi-physics method for simulating the mitral heart valve. Comput. Methods Biomech. Biomedi. Eng. 17:450–458, 2014.
pubmed: 22640492
doi: 10.1080/10255842.2012.688818
Franke, B., J. Brüning, P. Yevtushenko, H. Dreger, A. Brand, B. Juri, A. Unbehaun, J. Kempfert, S. Sündermann, and A. Lembcke. Computed tomography-based assessment of transvalvular pressure gradient in aortic stenosis. Front. Cardiovasc. Med. 8:706628, 2021.
pubmed: 34568450
pmcid: 8457381
doi: 10.3389/fcvm.2021.706628
Gahl, B., M. Çelik, S. J. Head, J.-L. Vanoverschelde, P. Pibarot, M. J. Reardon, N. M. Van Mieghem, A. P. Kappetein, P. Jüni, and B. R. Da Costa. Natural history of asymptomatic severe aortic stenosis and the association of early intervention with outcomes: A systematic review and meta-analysis. JAMA Cardiol. 5:1102–1112, 2020.
pubmed: 32639521
doi: 10.1001/jamacardio.2020.2497
Gnyaneshwar, R., R. K. Kumar, and K. R. Balakrishnan. Dynamic analysis of the aortic valve using a finite element model. Ann. Thorac. Surg. 73:1122–1129, 2002.
pubmed: 11996252
doi: 10.1016/S0003-4975(01)03588-3
Govindarajan, V., A. Kolanjiyil, N. P. Johnson, H. Kim, K. B. Chandran, and D. D. McPherson. Improving transcatheter aortic valve interventional predictability via fluid–structure interaction modelling using patient-specific anatomy. R. Soc. Open Sci. 9:211694, 2022.
pubmed: 35154799
pmcid: 8826300
doi: 10.1098/rsos.211694
Govindarajan, V., J. Mousel, H. Udaykumar, S. C. Vigmostad, D. D. McPherson, H. Kim, and K. B. Chandran. Synergy between diastolic mitral valve function and left ventricular flow aids in valve closure and blood transport during systole. Sci. Rep. 8:1–14, 2018.
doi: 10.1038/s41598-018-24469-x
Johnson, N. P., J. M. Zelis, P. A. Tonino, P. Houthuizen, R. A. Bouwman, G. R. Brueren, D. T. Johnson, J. J. Koolen, H. H. Korsten, and I. F. Wijnbergen. Pressure gradient vs flow relationships to characterize the physiology of a severely stenotic aortic valve before and after transcatheter valve implantation. Eur. Heart J. 39:2646–2655, 2018.
pubmed: 29617762
pmcid: 6055586
doi: 10.1093/eurheartj/ehy126
Kaden, J. J., S. Bickelhaupt, R. Grobholz, K. K. Haase, A. Sarιkoç, M. Brueckmann, S. Lang, I. Zahn, C. Vahl, and S. Hagl. Receptor activator of nuclear factor κB ligand and osteoprotegerin regulate aortic valve calcification. J. Mol. Cell. Cardiol. 36:57–66, 2004.
pubmed: 14734048
doi: 10.1016/j.yjmcc.2003.09.015
Kapahi, A., J. Mousel, S. Sambasivan, and H. Udaykumar. Parallel, sharp interface Eulerian approach to high-speed multi-material flows. Comput. Fluids. 83:144–156, 2013.
doi: 10.1016/j.compfluid.2012.06.024
Kivi, A. R., N. Sedaghatizadeh, B. S. Cazzolato, A. C. Zander, R. Roberts-Thomson, A. J. Nelson, and M. Arjomandi. Fluid structure interaction modelling of aortic valve stenosis: Effects of valve calcification on coronary artery flow and aortic root hemodynamics. Comput. Methods Programs Biomed. 196:105647, 2020.
pubmed: 32688138
doi: 10.1016/j.cmpb.2020.105647
Kvaslerud, A. B., E. Gude, G. Eriksen, A. K. Andreassen, L. Gullestad, and K. Broch. Diastolic dysfunction is unmasked on exercise in patients with asymptomatic, severe aortic stenosis: An invasive hemodynamic study. Circulation. 15:e009253, 2022.
pubmed: 35137599
Lancellotti, P., J. Magne, and L. A. Piérard. The role of stress testing in evaluation of asymptomatic patients with aortic stenosis. Curr. Opin. Cardiol. 28:531–539, 2013.
pubmed: 23835948
doi: 10.1097/HCO.0b013e3283632b41
Magne, J., P. Lancellotti, and L. A. Piérard. Exercise testing in asymptomatic severe aortic stenosis. JACC Cardiovasc. Imaging. 7:188–199, 2014.
pubmed: 24524744
doi: 10.1016/j.jcmg.2013.08.011
Marechaux, S., Z. Hachicha, A. Bellouin, J. G. Dumesnil, P. Meimoun, A. Pasquet, S. Bergeron, M. Arsenault, T. Le Tourneau, and P. V. Ennezat. Usefulness of exercise-stress echocardiography for risk stratification of true asymptomatic patients with aortic valve stenosis. Eur. Heart J. 31:1390–1397, 2010.
pubmed: 20308041
pmcid: 2878968
doi: 10.1093/eurheartj/ehq076
Mousel, J. A. A massively parallel adaptive sharp interface solver with application to mechanical heart valve simulations. The University of Iowa, 2012.
doi: 10.17077/etd.4htli577
Nigam, V., and D. Srivastava. Notch1 represses osteogenic pathways in aortic valve cells. J. Mol. Cell. Cardiol. 47:828–834, 2009.
pubmed: 19695258
pmcid: 2783189
doi: 10.1016/j.yjmcc.2009.08.008
O’Brien, K. D., D. D. Reichenbach, S. M. Marcovina, J. Kuusisto, C. E. Alpers, and C. M. Otto. Apolipoproteins B,(a), and E accumulate in the morphologically early lesion of ‘degenerative’valvular aortic stenosis. Arteriosclerosis Thrombosis Vascular Biol. 16:523–532, 1996.
pubmed: 8624774
doi: 10.1161/01.ATV.16.4.523
Olsson, M., J. Thyberg, and J. Nilsson. Presence of oxidized low density lipoprotein in nonrheumatic stenotic aortic valves. Arteriosclerosis Thrombosis Vascular Biol. 19:1218–1222, 1999.
pubmed: 10323772
doi: 10.1161/01.ATV.19.5.1218
Otto, C. M., R. A. Nishimura, R. O. Bonow, B. A. Carabello, J. P. Erwin III., F. Gentile, H. Jneid, E. V. Krieger, M. Mack, and C. McLeod. 2020 ACC/AHA guideline for the management of patients with valvular heart disease: Executive summary: A report of the American College of Cardiology/American Heart Association Joint Committee on Clinical Practice Guidelines. J. Am. Coll. Cardiol. 77:450–500, 2021.
pubmed: 33342587
doi: 10.1016/j.jacc.2020.11.035
Otto, C. M., and B. Prendergast. Aortic-valve stenosis—From patients at risk to severe valve obstruction. N. Engl. J. Med. 371:744–756, 2014.
pubmed: 25140960
doi: 10.1056/NEJMra1313875
Pibarot, P., and J. G. Dumesnil. Improving assessment of aortic stenosis. J. Am. Coll. Cardiol. 60:169–180, 2012.
pubmed: 22789881
doi: 10.1016/j.jacc.2011.11.078
Qin, T., A. Caballero, W. Mao, B. Barrett, N. Kamioka, S. Lerakis, and W. Sun. The role of stress concentration in calcified bicuspid aortic valve. J. R. Soc. Interface. 17:20190893, 2020.
pubmed: 32517630
pmcid: 7328384
doi: 10.1098/rsif.2019.0893
Salatzki, J., A. Ochs, N. Kirchgäßner, J. Heins, S. Seitz, H. Hund, D. Mereles, M. G. Friedrich, H. A. Katus, and N. Frey. Safety of stress cardiovascular magnetic resonance in patients with moderate to severe aortic valve stenosis. J. Cardiovasc. Imaging. 3:26–38, 2023.
doi: 10.4250/jcvi.2022.0063
Sethian, J. A. Theory, algorithms, and applications of level set methods for propagating interfaces. Acta Numerica. 5:309–395, 1996.
doi: 10.1017/S0962492900002671
Stein, P. D., and H. N. Sabbah. Turbulent blood flow in the ascending aorta of humans with normal and diseased aortic valves. Circ. Res. 39:58–65, 1976.
pubmed: 776437
doi: 10.1161/01.RES.39.1.58
Tanase, D. M., E. Valasciuc, E. M. Gosav, M. Floria, C. F. Costea, N. Dima, I. Tudorancea, M. A. Maranduca, and I. L. Serban. Contribution of oxidative stress (OS) in calcific aortic valve disease (CAVD): From pathophysiology to therapeutic targets. Cells. 11:2663, 2022.
pubmed: 36078071
pmcid: 9454630
doi: 10.3390/cells11172663
Taylor R. FEAP—A finite element analysis program: Theory manual, version 7.5. Structural Engineering, Mechanics and Materials, Department of Civil and Environmental Engineering, University of California, Berkeley, 2003.
Towler, D. A. Molecular and cellular aspects of calcific aortic valve disease. Circ. Res. 113:198–208, 2013.
pubmed: 23833294
pmcid: 4057916
doi: 10.1161/CIRCRESAHA.113.300155
Tretjakovs, P., J. Lurins, S. Svirskis, G. Gersone, D. Lurina, U. Rozenberga, L. Blumfelds, G. Bahs, A. Lejnieks, and V. Mackevics. Thioredoxin-1 and correlations of the plasma cytokines regarding aortic valve stenosis severity. Biomedicines. 9:1041, 2021.
pubmed: 34440245
pmcid: 8391645
doi: 10.3390/biomedicines9081041
Vahanian, A., F. Beyersdorf, F. Praz, M. Milojevic, S. Baldus, J. Bauersachs, D. Capodanno, L. Conradi, M. De Bonis, and R. De Paulis. 2021 ESC/EACTS Guidelines for the management of valvular heart disease: developed by the task force for the management of valvular heart disease of the European Society of Cardiology (ESC) and the European Association for Cardio-Thoracic Surgery (EACTS). Eur. Heart J. 43:561–632, 2022.
pubmed: 34453165
doi: 10.1093/eurheartj/ehab395
Vahanian, A., and C. M. Otto. Risk stratification of patients with aortic stenosis. Eur. Heart J. 31:416–423, 2010.
pubmed: 20047994
doi: 10.1093/eurheartj/ehp575
Van Ooij, P., J. Garcia, W. V. Potters, S. C. Malaisrie, J. D. Collins, J. C. Carr, M. Markl, and A. J. Barker. Age-related changes in aortic 3D blood flow velocities and wall shear stress: implications for the identification of altered hemodynamics in patients with aortic valve disease. J. Magne. Resonance Imaging. 43:1239–1249, 2016.
pubmed: 26477691
doi: 10.1002/jmri.25081
Van Ooij, P., W. V. Potters, A. J. Nederveen, B. D. Allen, J. Collins, J. Carr, S. C. Malaisrie, M. Markl, and A. J. Barker. A methodology to detect abnormal relative wall shear stress on the full surface of the thoracic aorta using four-dimensional flow MRI. Magn. Resonance Med. 73:1216–1227, 2015.
pubmed: 24753241
doi: 10.1002/mrm.25224
Vigmostad, S. C., H. S. Udaykumar, J. Lu, and K. B. Chandran. Fluid–structure interaction methods in biological flows with special emphasis on heart valve dynamics. Int. J. Numerical Methods Biomed. Eng. 26:435–470, 2010.
doi: 10.1002/cnm.1340
von Knobelsdorff-Brenkenhoff, F., A. Karunaharamoorthy, R. F. Trauzeddel, A. J. Barker, E. Blaszczyk, M. Markl, and J. Schulz-Menger. Evaluation of aortic blood flow and wall shear stress in aortic stenosis and its association with left ventricular remodeling. Circ. Cardiovasc. Imaging. 9:e004038, 2016.
doi: 10.1161/CIRCIMAGING.115.004038
Wallby, L., B. Janerot-Sjöberg, T. Steffensen, and M. Broqvist. T lymphocyte infiltration in non-rheumatic aortic stenosis: A comparative descriptive study between tricuspid and bicuspid aortic valves. Heart. 88:348–351, 2002.
pubmed: 12231589
pmcid: 1767380
doi: 10.1136/heart.88.4.348
Wiener, P. C., A. Darwish, E. Friend, L. Kadem, and G. S. Pressman. Energy loss associated with in-vitro modeling of mitral annular calcification. Plos One. 16:e0246701, 2021.
pubmed: 33591991
pmcid: 7886214
doi: 10.1371/journal.pone.0246701
Yu, Y., H. Baek, and G. E. Karniadakis. Generalized fictitious methods for fluid–structure interactions: Analysis and simulations. J. Comput. Phys. 245:317–346, 2013.
doi: 10.1016/j.jcp.2013.03.025
Zelis, J. M., P. A. Tonino, D. T. Johnson, P. Balan, G. R. Brueren, I. Wijnbergen, R. L. Kirkeeide, N. H. Pijls, K. L. Gould, and N. P. Johnson. Stress aortic valve index (SAVI) with dobutamine for low-gradient aortic stenosis: A pilot study. Struct. Heart. 4:53–61, 2020.
doi: 10.1080/24748706.2019.1690180