In Vivo Three-Dimensional Geometric Reconstruction of the Mouse Aortic Heart Valve.

Geometric anatomical models Heart valve disease In vivo ultrasound imaging Mouse animal models

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:
14 Jun 2024
Historique:
received: 30 04 2024
accepted: 26 05 2024
medline: 14 6 2024
pubmed: 14 6 2024
entrez: 14 6 2024
Statut: aheadofprint

Résumé

Aortic valve (AV) disease is a common valvular lesion in the United States, present in about 5% of the population at age 65 with increasing prevalence with advancing age. While current replacement heart valves have extended life for many, their long-term use remains hampered by limited durability. Non-surgical treatments for AV disease do not yet exist, in large part because our understanding of AV disease etiology remains incomplete. The direct study of human AV disease remains hampered by the fact that clinical data is only available at the time of treatment, where the disease is at or near end stage and any time progression information has been lost. Large animal models, long used to assess replacement AV devices, cannot yet reproduce AV disease processes. As an important alternative mouse animal models are attractive for their ability to perform genetic studies of the AV disease processes and test potential pharmaceutical treatments. While mouse models have been used for cellular and genetic studies of AV disease, their small size and fast heart rates have hindered their use for tissue- and organ-level studies. We have recently developed a novel ex vivo micro-CT-based methodology to 3D reconstruct murine heart valves and estimate the leaflet mechanical behaviors (Feng et al. in Sci Rep 13(1):12852, 2023). In the present study, we extended our approach to 3D reconstruction of the in vivo functional murine AV (mAV) geometry using high-frequency four-dimensional ultrasound (4DUS). From the resulting 4DUS images we digitized the mAV mid-surface coordinates in the fully closed and fully opened states. We then utilized matched high-resolution µCT images of ex vivo mouse mAV to develop mAV NURBS-based geometric model. We then fitted the mAV geometric model to the in vivo data to reconstruct the 3D in vivo mAV geometry in the closed and open states in n = 3 mAV. Results demonstrated high fidelity geometric results. To our knowledge, this is the first time such reconstruction was ever achieved. This robust assessment of in vivo mAV leaflet kinematics in 3D opens up the possibility for longitudinal characterization of murine models that develop aortic valve disease.

Identifiants

pubmed: 38874705
doi: 10.1007/s10439-024-03555-4
pii: 10.1007/s10439-024-03555-4
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : NHLBI NIH HHS
ID : National Institutes of Health grant HL142504
Pays : United States

Informations de copyright

© 2024. The Author(s) under exclusive licence to Biomedical Engineering Society.

Références

Lerman, D. A., S. Prasad, and N. Alotti. Calcific aortic valve disease: molecular mechanisms and therapeutic approaches. Eur. Cardiol. Rev. 10(2):108, 2015.
doi: 10.15420/ecr.2015.10.2.108
Tasoudis, P. T., D. N. Varvoglis, E. Vitkos, K. S. Mylonas, M. P. Sa, J. S. Ikonomidis, T. G. Caranasos, and T. Athanasiou. Mechanical versus bioprosthetic valve for aortic valve replacement: systematic review and meta-analysis of reconstructed individual participant data. Eur. J. Cardio-Thorac. Surg. 62(1):ezac268, 2022.
doi: 10.1093/ejcts/ezac268
Kheradvar, A., R. Zareian, S. Kawauchi, R. L. Goodwin, and S. Rugonyi. Animal models for heart valve research and development. Drug Discov. Today. 24:55–62, 2017.
Cheek, J. D., E. E. Wirrig, C. M. Alfieri, J. F. James, and K. E. Yutzey. Differential activation of valvulogenic, chondrogenic, and osteogenic pathways in mouse models of myxomatous and calcific aortic valve disease. J. Mol. Cell. Cardiol. 52(3):689–700, 2012.
doi: 10.1016/j.yjmcc.2011.12.013 pubmed: 22248532 pmcid: 3294059
Lincoln, J., C. M. Alfieri, and K. E. Yutzey. Development of heart valve leaflets and supporting apparatus in chicken and mouse embryos. Dev. Dyn. 230(2):239–250, 2004. https://doi.org/10.1002/dvdy.20051 .
doi: 10.1002/dvdy.20051 pubmed: 15162503
Colvee, E., and J. M. Hurle. Maturation of the extracellular material of the semilunar heart valves in the mouse. Anatomy Embryol. 162:343–352, 1981.
doi: 10.1007/BF00299977
Rego, B. V., A. M. Pouch, J. H. Gorman, R. C. Gorman, and M. S. Sacks. Patient-specific quantification of normal and bicuspid aortic valve leaflet deformations from clinically derived images. Ann. Biomed. Eng. 50:1–15, 2022. https://doi.org/10.1007/s10439-021-02882-0 .
doi: 10.1007/s10439-021-02882-0 pubmed: 34993699 pmcid: 9084616
Rotman, O. M., M. Bianchi, R. P. Ghosh, B. Kovarovic, and D. Bluestein. Principles of tavr valve design, modelling, and testing. Expert Rev Med. Devices. 15:771–791, 2018. https://doi.org/10.1080/17434440.2018.1536427 .
doi: 10.1080/17434440.2018.1536427 pubmed: 30318937 pmcid: 6417919
Emendi, M., F. Sturla, R. P. Ghosh, M. Bianchi, F. Piatti, F. R. Pluchinotta, D. Giese, M. Lombardi, A. Redaelli, and D. Bluestein. Patient-specific bicuspid aortic valve biomechanics: a magnetic resonance imaging integrated fluid–structure interaction approach. Ann. Biomed. Eng. 49:627–641, 2021.
doi: 10.1007/s10439-020-02571-4 pubmed: 32804291
Lavon, K., A. Morany, R. Halevi, A. Hamdan, E. Raanani, D. Bluestein, and R. Haj-Ali. Progressive calcification in bicuspid valves: a coupled hemodynamics and multiscale structural computations. Ann. Biomed. Eng. 49:3310–3322, 2021.
doi: 10.1007/s10439-021-02877-x pubmed: 34708308 pmcid: 8862115
Pouch, A. M., B. M. Jackson, P. A. Yushkevich, J. H. Gorman 3rd., and R. C. Gorman. 4d-transesophageal echocardiography and emerging imaging modalities for guiding mitral valve repair. Ann. Cardiothorac. Surg. 4(5):461–462, 2015. https://doi.org/10.3978/j.issn.2225-319X.2015.02.01 .
doi: 10.3978/j.issn.2225-319X.2015.02.01 pubmed: 26539351 pmcid: 4598460
Pouch, A. M., C. Xu, P. A. Yushkevich, A. S. Jassar, M. Vergnat, J. H. Gorman 3rd., R. C. Gorman, C. M. Sehgal, and B. M. Jackson. Semi-automated mitral valve morphometry and computational stress analysis using 3d ultrasound. J. Biomech. 45(5):903–907, 2012. https://doi.org/10.1016/j.jbiomech.2011.11.033 .
doi: 10.1016/j.jbiomech.2011.11.033 pubmed: 22281408 pmcid: 3294138
Sewell-Loftin, M.-K., C. B. Brown, H. S. Baldwin, and W. D. Merryman. Novel technique for quantifying mouse heart valve leaflet stiffness with atomic force microscopy. J. Heart Valve Dis. 21(4):513, 2012.
pubmed: 22953681 pmcid: 3536027
Sacks, M. S., and A. P. Yoganathan. Heart valve function: a biomechanical perspective. Philos. Trans. R. Soc. B. 362(1484):1369–1391, 2007.
doi: 10.1098/rstb.2007.2122
Sacks, M. S., W. D. Merryman, and D. E. Schmidt. On the biomechanics of heart valve function. J. Biomech. 42:1804–1824, 2009.
doi: 10.1016/j.jbiomech.2009.05.015 pubmed: 19540499 pmcid: 2746960
Feng, X., Y. Liu, D. Kamensky, D. W. McComb, C. K. Breuer, and M. S. Sacks. Functional mechanical behavior of the murine pulmonary heart valve. Sci. Rep. 13(1):12852, 2023.
doi: 10.1038/s41598-023-40158-w pubmed: 37553466 pmcid: 10409802
Liu, Y., X. Feng, H. Liu, D. McComb, C. Breuer, and M. Sacks. On the shape and structure of the murine pulmonary heart valve. Sci. Rep. 11(1):14078, 2021.
doi: 10.1038/s41598-021-93513-0 pubmed: 34234231 pmcid: 8263753
Damen, F. W., A. G. Berman, A. H. Soepriatna, J. M. Ellis, S. D. Buttars, K. L. Aasa, and C. J. Goergen. High-frequency 4-dimensional ultrasound (4dus): a reliable method for assessing murine cardiac function. Tomography. 3(4):180–187, 2017.
doi: 10.18383/j.tom.2017.00016 pubmed: 29308434 pmcid: 5749424
Aggarwal, A. An improved parameter estimation and comparison for soft tissue constitutive models containing an exponential function. Biomech. Model. Mechanobiol. 16(4):1309–1327, 2017. https://doi.org/10.1007/s10237-017-0889-3 .
doi: 10.1007/s10237-017-0889-3 pubmed: 28251368 pmcid: 5511618
Aggarwal, A., A. M. Pouch, E. Lai, J. Lesicko, P. A. Yushkevich, J. H. Gorman III., R. C. Gorman, and M. S. Sacks. In-vivo heterogeneous functional and residual strains in human aortic valve leaflets. J. Biomech. 2016. https://doi.org/10.1016/j.jbiomech.2016.04.038 .
doi: 10.1016/j.jbiomech.2016.04.038 pubmed: 27207385 pmcid: 5028253
Aggarwal, A., and M. S. Sacks. An inverse modeling approach for semilunar heart valve leaflet mechanics: exploitation of tissue structure. Biomech. Model. Mechanobiol. 1–24, 2005.
Damen, F., A. Adelsperger, K. Wilson, and C. Goergen. Comparison of traditional and integrated digital anesthetic vaporizers. J. Am. Assoc. Lab. Anim. 54(756–762):390, 2015.
Damen, F. W., J. P. Salvas, A. S. Pereyra, J. M. Ellis, and C. J. Goergen. Muscle mechanics and ventricular function: Improving characterization of hypertrophy-induced murine cardiac dysfunction using four-dimensional ultrasound-derived strain mapping. Am. J. Physiol.-Heart Circ. Physiol. 321(1):H197, 2021.
doi: 10.1152/ajpheart.00133.2021 pubmed: 34085843 pmcid: 8321816
Piegl, L., and W. Tiller. The NURBS Book. New York: Springer, 2012.
Aggarwal, A., A. M. Pouch, E. Lai, J. Lesicko, P. A. Yushkevich, J. H. GormanIii, R. C. Gorman, and M. S. Sacks. In-vivo heterogeneous functional and residual strains in human aortic valve leaflets. J. Biomech. 49:2481–2490, 2016. https://doi.org/10.1016/j.jbiomech.2016.04.038 .
doi: 10.1016/j.jbiomech.2016.04.038 pubmed: 27207385 pmcid: 5028253
Aggarwal, A., and M. S. Sacks. An inverse modeling approach for semilunar heart valve leaflet mechanics: exploitation of tissue structure. Biomech. Model. Mechanobiol. 15:909–932, 2016. https://doi.org/10.1007/s10237-015-0732-7 .
doi: 10.1007/s10237-015-0732-7 pubmed: 26449480
Otto, C. M. Calcific aortic valve disease: new concepts. Semin. Thorac. Cardiovasc. Surg. 22(4):276–284, 2010. https://doi.org/10.1053/j.semtcvs.2011.01.009 .
doi: 10.1053/j.semtcvs.2011.01.009 pubmed: 21549267
Freeman, R. V., and C. M. Otto. Spectrum of calcific aortic valve disease: pathogenesis, disease progression, and treatment strategies. Circulation. 111(24):3316–3326, 2005. https://doi.org/10.1161/circulationaha.104.486738 .
doi: 10.1161/circulationaha.104.486738 pubmed: 15967862
Freeman, R. V., and C. M. Otto. Management of asymptomatic valvular aortic stenosis. Indian Heart J. 54(1):31–38, 2002.
pubmed: 11999085
Kurtz, C. E., and C. M. Otto. Aortic stenosis: clinical aspects of diagnosis and management, with 10 illustrative case reports from a 25-year experience. Medicine. 89(6):349–379, 2010. https://doi.org/10.1097/MD.0b013e3181fe5648 .
doi: 10.1097/MD.0b013e3181fe5648 pubmed: 21057260
Beckmann, E., J. B. Grau, R. Sainger, P. Poggio, and G. Ferrari. Insights into the use of biomarkers in calcific aortic valve disease. J. Heart Valve Dis. 19(4):441–452, 2010.
pubmed: 20845891 pmcid: 2941903
Grau, J. B., P. Poggio, R. Sainger, W. J. Vernick, W. F. Seefried, E. Branchetti, B. C. Field, J. E. Bavaria, M. A. Acker, and G. Ferrari. Analysis of osteopontin levels for the identification of asymptomatic patients with calcific aortic valve disease. Ann. Thorac. Surg. 93(1):79–86, 2012. https://doi.org/10.1016/j.athoracsur.2011.08.036 .
doi: 10.1016/j.athoracsur.2011.08.036 pubmed: 22093695
Yu, P.-J., A. Skolnick, G. Ferrari, K. Heretis, P. Mignatti, G. Pintucci, B. Rosenzweig, J. Diaz-Cartelle, I. Kronzon, G. Perk, H. I. Pass, A. C. Galloway, E. A. Grossi, and J. B. Grau. Correlation between plasma osteopontin levels and aortic valve calcification: potential insights into the pathogenesis of aortic valve calcification and stenosis. J. Thorac. Cardio-Vasc. Surg. 138(1):196–199, 2009. https://doi.org/10.1016/j.jtcvs.2008.10.045 .
doi: 10.1016/j.jtcvs.2008.10.045
Parolari, A., E. Tremoli, L. Cavallotti, M. Trezzi, S. Kassem, C. Loardi, F. Veglia, G. Ferrari, D. Pacini, and F. Alamanni. Do statins improve outcomes and delay the progression of non-rheumatic calcific aortic stenosis? Heart. 97(7):523–529, 2011. https://doi.org/10.1136/hrt.2010.215046 .
doi: 10.1136/hrt.2010.215046 pubmed: 21270077
Cowell, S. J., D. E. Newby, R. J. Prescott, P. Bloomfield, J. Reid, D. B. Northridge, and N. A. Boon. A randomized trial of intensive lipid-lowering therapy in calcific aortic stenosis. N. Engl. J. Med. 352(23):2389–2397, 2005. https://doi.org/10.1056/NEJMoa043876 .
doi: 10.1056/NEJMoa043876 pubmed: 15944423
Benton, J. A., H. B. Kern, L. A. Leinwand, P. D. Mariner, and K. S. Anseth. Statins block calcific nodule formation of valvular interstitial cells by inhibiting alpha-smooth muscle actin expression. Arterioscler. Thromb. Vasc. Biol. 29(11):1950–1957, 2009. https://doi.org/10.1161/atvbaha.109.195271 .
doi: 10.1161/atvbaha.109.195271 pubmed: 19679827
Rossebo, A. B., T. R. Pedersen, K. Boman, P. Brudi, J. B. Chambers, K. Egstrup, E. Gerdts, C. Gohlke-Barwolf, I. Holme, Y. A. Kesaniemi, W. Malbecq, C. A. Nienaber, S. Ray, T. Skjaerpe, K. Wachtell, and R. Willenheimer. Intensive lipid lowering with simvastatin and ezetimibe in aortic stenosis. N. Engl. J. Med. 359(13):1343–1356, 2008. https://doi.org/10.1056/NEJMoa0804602 .
doi: 10.1056/NEJMoa0804602 pubmed: 18765433
Rajamannan, N. M. Calcific aortic stenosis: medical and surgical management in the elderly. Curr. Treat. Options Cardiovasc. Med. 7(6):437–442, 2005. https://doi.org/10.1007/s11936-005-0028-9 .
doi: 10.1007/s11936-005-0028-9 pubmed: 16283970
Mulholland, D. L., and A. I. Gotlieb. Cell biology of valvular interstitial cells. Can. J. Cardiol. 12(3):231–236, 1996.
pubmed: 8624972
Schoen, F. J. Cardiac valves and valvular pathology: update on function, disease, repair, and replacement. Cardiovasc. Pathol. 14(4):189–194, 2005.
doi: 10.1016/j.carpath.2005.03.005 pubmed: 16009317
Vesely, I., J. E. Barber, and N. B. Ratliff. Tissue damage and calcification may be independent mechanisms of bioprosthetic heart valve failure. J. Heart Valve Dis. 10(4):471–477, 2001.
pubmed: 11499593
Sacks, M. S., and F. J. Schoen. Collagen fiber disruption occurs independent of calcification in clinically explanted bioprosthetic heart valves. J. Biomed. Mater. Res. 62(3):359–371, 2002.
doi: 10.1002/jbm.10293 pubmed: 12209921
Bonow, R. O., B. A. Carabello, K. Chatterjee, A. C. de Leon, Jr., D. P. Faxon, M. D. Freed, W. H. Gaasch, B. W. Lytle, R. A. Nishimura, P. T. O’Gara, R. A. O’Rourke, C. M. Otto, P. M. Shah, J. S. Shanewise, S. C. Smith, Jr., A. K. Jacobs, C. D. Adams, J. L. Anderson, E. M. Antman, V. Fuster, J. L. Halperin, L. F. Hiratzka, S. A. Hunt, R. Nishimura, R. L. Page, B. Riegel, ACC/AHA 2006 guidelines for the management of patients with valvular heart disease: a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines (writing Committee to Revise the 1998 guidelines for the management of patients with valvular heart disease) developed in collaboration with the Society of Cardiovascular Anesthesiologists endorsed by the Society for Cardiovascular Angiography and Interventions and the Society of Thoracic Surgeons. J. Am. Coll. Cardiol. 48(3):e1–148, 2006. https://doi.org/10.1016/j.jacc.2006.05.021
Guidoin, R., Y. Douville, M. A. Clavel, Z. Zhang, M. Nutley, P. Pibarot, and G. Dionne. The marvel of percutaneous cardiovascular devices in the elderly. Ann. N. Y. Acad. Sci. 1197:188–199, 2010. https://doi.org/10.1111/j.1749-6632.2010.05517.x .
doi: 10.1111/j.1749-6632.2010.05517.x pubmed: 20536849
Sider, K. L., M. C. Blaser, C. A. Simmons, et al. Animal models of calcific aortic valve disease. Int. J. Inflamm.2011(1):364310, 2011.
Kaplan, S. R., G. Bashein, F. H. Sheehan, M. E. Legget, B. Munt, X. N. Li, M. Sivarajan, E. L. Bolson, M. Zeppa, M. Z. Arch, and R. W. Martin. Three-dimensional echocardiographic assessment of annular shape changes in the normal and regurgitant mitral valve. Am. Heart J. 139(3):378–387, 2000.
doi: 10.1016/S0002-8703(00)90077-2 pubmed: 10689248
Chakraborty, S., J. Cheek, B. Sakthivel, B. J. Aronow, and K. E. Yutzey. Shared gene expression profiles in developing heart valves and osteoblast progenitor cells. Physiol. Genomics. 35(1):75–85, 2008. https://doi.org/10.1152/physiolgenomics.90212.2008 .
doi: 10.1152/physiolgenomics.90212.2008 pubmed: 18612084 pmcid: 2536828
Hinton, R. B., Jr., J. Lincoln, G. H. Deutsch, H. Osinska, P. B. Manning, D. W. Benson, and K. E. Yutzey. Extracellular matrix remodeling and organization in developing and diseased aortic valves. Circ. Res. 98(11):1431–1438, 2006. https://doi.org/10.1161/01.RES.0000224114 .
doi: 10.1161/01.RES.0000224114 pubmed: 16645142

Auteurs

Daniel P Gramling (DP)

Weldon School of Biomedical Engineering, Purdue University, West Lafayette, IN, USA.

Aletea L van Veldhuisen (AL)

Weldon School of Biomedical Engineering, Purdue University, West Lafayette, IN, USA.

Frederick W Damen (FW)

Weldon School of Biomedical Engineering, Purdue University, West Lafayette, IN, USA.

Kaitlyn Thatcher (K)

Department of Pediatrics, Medical College of Wisconsin, Herma Heart Institute, Children's Wisconsin Milwaukee, Milwaukee, WI, USA.

Felix Liu (F)

Center for Electron Microscopy and Analysis, The Ohio State University, Columbus, OH, USA.

David McComb (D)

Center for Electron Microscopy and Analysis, The Ohio State University, Columbus, OH, USA.

Joy Lincoln (J)

Department of Pediatrics, Medical College of Wisconsin, Herma Heart Institute, Children's Wisconsin Milwaukee, Milwaukee, WI, USA.

Christopher K Breuer (CK)

Tissue Engineering and Surgical Research, Nationwide Children's Hospital, Columbus, OH, USA.

Craig J Goergen (CJ)

Weldon School of Biomedical Engineering, Purdue University, West Lafayette, IN, USA.

Michael S Sacks (MS)

Department of Biomedical Engineering, James T. Willerson Center for Cardiovascular Modeling and Simulation, Oden Institute for Computational Engineering and Sciences, The University of Texas at Austin, Austin, TX, USA. msacks@oden.utexas.edu.

Classifications MeSH