Central Artery Hemodynamics in Angiotensin II-Induced Hypertension and Effects of Anesthesia.
Aorta
Hypertension
Isoflurane
Mouse
Pulse pressure
Stiffness
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:
21 Feb 2024
21 Feb 2024
Historique:
received:
22
08
2023
accepted:
30
12
2023
medline:
22
2
2024
pubmed:
22
2
2024
entrez:
22
2
2024
Statut:
aheadofprint
Résumé
Systemic hypertension is a strong risk factor for cardiovascular, neurovascular, and renovascular diseases. Central artery stiffness is both an initiator and indicator of hypertension, thus revealing a critical relationship between the wall mechanics and hemodynamics. Mice have emerged as a critical animal model for studying effects of hypertension and much has been learned. Regardless of the specific mouse model, data on changes in cardiac function and hemodynamics are necessarily measured under anesthesia. Here, we present a new experimental-computational workflow to estimate awake cardiovascular conditions from anesthetized data, which was then used to quantify effects of chronic angiotensin II-induced hypertension relative to normotension in wild-type mice. We found that isoflurane anesthesia had a greater impact on depressing hemodynamics in angiotensin II-infused mice than in controls, which led to unexpected results when comparing anesthetized results between the two groups of mice. Through comparison of the awake simulations, however, in vivo relevant effects of angiotensin II-infusion on global and regional vascular structure, properties, and hemodynamics were found to be qualitatively consistent with expectations. Specifically, we found an increased in vivo vascular stiffness in the descending thoracic aorta and suprarenal abdominal aorta, leading to increases in pulse pressure in the distal aorta. These insights allow characterization of the impact of regionally varying vascular remodeling on hemodynamics and mouse-to-mouse variations due to induced hypertension.
Identifiants
pubmed: 38383871
doi: 10.1007/s10439-024-03440-0
pii: 10.1007/s10439-024-03440-0
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : NHLBI NIH HHS
ID : R01 HL105297
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL155105
Pays : United States
Informations de copyright
© 2024. The Author(s) under exclusive licence to Biomedical Engineering Society.
Références
Alhakak, A. S., J. R. Teerlink, J. Lindenfeld, M. Böhm, G. M. C. Rosano, and T. Biering-Sørensen. The significance of left ventricular ejection time in heart failure with reduced ejection fraction. Eur. J. Heart Fail. 23:541–551, 2021. https://doi.org/10.1002/ejhf.2125 .
doi: 10.1002/ejhf.2125
pubmed: 33590579
Arthurs, C. J., R. Khlebnikov, A. Melville, M. Marčan, A. Gomez, D. Dillon-Murphy, F. Cuomo, M. Silva Vieira, J. Schollenberger, S. R. Lynch, C. Tossas-Betancourt, K. Iyer, S. Hopper, E. Livingston, P. Youssefi, A. Noorani, S. Ben Ahmed, F. J. H. Nauta, T. M. J. van Bakel, and C. A. Figueroa. CRIMSON: an open-source software framework for cardiovascular integrated modelling and simulation. PLoS Comput. Biol.17(5):e1008881, 2021. https://doi.org/10.1371/journal.pcbi.1008881 .
doi: 10.1371/journal.pcbi.1008881
pubmed: 33970900
pmcid: 8148362
Aslanidou, L., B. Trachet, P. Reymond, R. A. Fraga-Silva, P. Segers, and N. Stergiopulos. A 1D model of the arterial circulation in mice. ALTEX. 33(1):13–28, 2016. https://doi.org/10.14573/ALTEX.1507071 .
doi: 10.14573/ALTEX.1507071
pubmed: 26555250
Baek, S., R. L. Gleason, K. R. Rajagopal, and J. D. Humphrey. Theory of small on large: potential utility in computations of fluid-solid interactions in arteries. Comput. Methods Appl. Mech. Eng. 196(31–32):3070–3078, 2007. https://doi.org/10.1016/j.cma.2006.06.018 .
doi: 10.1016/j.cma.2006.06.018
Bersi, M. R., V. A. Acosta Santamaría, K. Marback, P. Di Achille, E. H. Phillips, C. J. Goergen, J. D. Humphrey, and S. Avril. Multimodality imaging-based characterization of regional material properties in a murine model of aortic dissection. Sci. Rep. 10(1):1–23, 2020. https://doi.org/10.1038/s41598-020-65624-7 .
doi: 10.1038/s41598-020-65624-7
Bersi, M. R., R. Khosravi, A. J. Wujciak, D. G. Harrison, and J. D. Humphrey. Differential cell-matrix mechanoadaptations and inflammation drive regional propensities to aortic fibrosis, aneurysm or dissection in hypertension. J. R. Soc. Interface. 14(136):20170327, 2017. https://doi.org/10.1098/rsif.2017.0327 .
doi: 10.1098/rsif.2017.0327
pubmed: 29118111
pmcid: 5721146
Charlson, M. E., C. R. MacKenzie, J. P. Gold, K. L. Ales, M. Topkins, and G. Tom Shires. Preoperative characteristics predicting intraoperative hypotension and hypertension among hypertensives and diabetics undergoing noncardiac surgery. Ann. Surg. 212(1):66, 1990. https://doi.org/10.1097/00000658-199007000-00010 .
doi: 10.1097/00000658-199007000-00010
pubmed: 2363606
pmcid: 1358076
Constantinides, C., and K. Murphy. Molecular and Integrative physiological effects of isoflurane anesthesia: the paradigm of cardiovascular studies in rodents using magnetic resonance imaging. Front. Cardiovasc. Med. 3:23, 2016. https://doi.org/10.3389/FCVM.2016.00023/BIBTEX .
doi: 10.3389/FCVM.2016.00023/BIBTEX
pubmed: 27525256
pmcid: 4965459
Cuomo, F., J. Ferruzzi, P. Agarwal, C. Li, Z. W. Zhuang, J. D. Humphrey, and C. Alberto Figueroa. Sex-dependent differences in central artery haemodynamics in normal and fibulin-5 deficient mice: implications for ageing. Proc. R. Soc. A. 475(2221):20180076, 2019. https://doi.org/10.1098/rspa.2018.0076 .
doi: 10.1098/rspa.2018.0076
pubmed: 30760948
pmcid: 6364598
Cuomo, F., J. Ferruzzi, J. D. Humphrey, and C. A. Figueroa. An experimental-computational study of catheter induced alterations in pulse wave velocity in anesthetized mice. Ann. Biomed. Eng. 43(7):1555–1570, 2015. https://doi.org/10.1007/s10439-015-1272-0 .
doi: 10.1007/s10439-015-1272-0
pubmed: 25698526
pmcid: 4497847
Ferruzzi, J., P. . Di. Achille, G. Tellides, and J. D. Humphrey. Combining in vivo and in vitro biomechanical data reveals key roles of perivascular tethering in central artery function. PLoS ONE. 13(9):1–21, 2018. https://doi.org/10.1371/journal.pone.0201379 .
doi: 10.1371/journal.pone.0201379
Ferruzzi, J., M. R. Bersi, and J. D. Humphrey. Biomechanical phenotyping of central arteries in health and disease: advantages of and methods for murine models. Ann. Biomed. Eng. 41(7):1311–1330, 2013. https://doi.org/10.1007/s10439-013-0799-1 .
doi: 10.1007/s10439-013-0799-1
pubmed: 23549898
pmcid: 3918742
Ferruzzi, J., M. R. Bersi, S. Uman, H. Yanagisawa, and J. D. Humphrey. Decreased elastic energy storage, not increased material stiffness, characterizes central artery dysfunction in fibulin-5 deficiency independent of sex. J. Biomech. Eng. 137(3):1–14, 2015. https://doi.org/10.1115/1.4029431 .
doi: 10.1115/1.4029431
Figueroa, C. A., I. E. Vignon-Clementel, K. E. Jansen, T. J. R. Hughes, and C. A. Taylor. A coupled momentum method for modeling blood flow in three-dimensional deformable arteries. Comput. Methods Appl. Mech. Eng. 195(41–43):5685–5706, 2006. https://doi.org/10.1016/j.cma.2005.11.011 .
doi: 10.1016/j.cma.2005.11.011
Fink, G. D. Does tail-cuff plethysmography provide a reliable estimate of central blood pressure in mice? J. Am. Heart Assoc.6(6):e006554, 2017. https://doi.org/10.1161/JAHA.117.006554 .
doi: 10.1161/JAHA.117.006554
pubmed: 28655736
pmcid: 5669206
Gleason, R. L., S. P. Gray, E. Wilson, and J. D. Humphrey. A multiaxial computer-controlled organ culture and biomechanical device for mouse carotid arteries. J. Biomech. Eng. 126(6):787–795, 2004. https://doi.org/10.1115/1.1824130 .
doi: 10.1115/1.1824130
pubmed: 15796337
Hoppe, P., C. Burfeindt, P. C. Reese, L. Briesenick, M. Flick, K. Kouz, H. Pinnschmidt, A. Hapfelmeier, D. I. Sessler, and B. Saugel. Chronic arterial hypertension and nocturnal non-dipping predict postinduction and intraoperative hypotension: a secondary analysis of a prospective study. J. Clin. Anesth.79:110715, 2022. https://doi.org/10.1016/J.JCLINANE.2022.110715 .
doi: 10.1016/J.JCLINANE.2022.110715
pubmed: 35306353
Hopper, S. E., F. Cuomo, J. Ferruzzi, N. S. Burris, S. Roccabianca, J. D. Humphrey, and C. A. Figueroa. Comparative study of human and murine aortic biomechanics and hemodynamics in vascular aging. Front. Physiol. 12:1889, 2021. https://doi.org/10.3389/FPHYS.2021.746796/BIBTEX .
doi: 10.3389/FPHYS.2021.746796/BIBTEX
Howell, S. J., J. W. Sear, and P. Föex. Hypertension, hypertensive heart disease and perioperative cardiac risk. Br. J. Anaesth. 92(4):570–583, 2004. https://doi.org/10.1093/BJA/AEH091 .
doi: 10.1093/BJA/AEH091
pubmed: 15013960
Humphrey, J. D. Mechanisms of arterial remodeling in hypertension. Hypertension. 52(2):195–200, 2008. https://doi.org/10.1161/HYPERTENSIONAHA.107.103440 .
doi: 10.1161/HYPERTENSIONAHA.107.103440
pubmed: 18541735
Humphrey, J. D., D. G. Harrison, C. A. Figueroa, P. Lacolley, and S. Laurent. Central artery stiffness in hypertension and aging a problem with cause and consequence. Circ. Res. 118(3):379–381, 2016. https://doi.org/10.1161/circresaha.115.307722 .
doi: 10.1161/circresaha.115.307722
pubmed: 26846637
pmcid: 4745997
Ioannou, C. V., N. Stergiopulos, E. Georgakarakos, E. Chatzimichali, A. N. Katsamouris, and D. R. Morel. Effects of isoflurane anesthesia on aortic compliance and systemic hemodynamics in compliant and noncompliant aortas. J. Cardiothorac. Vasc. Anesth. 27(6):1282–1288, 2013. https://doi.org/10.1053/J.JVCA.2013.04.015 .
doi: 10.1053/J.JVCA.2013.04.015
pubmed: 24035064
Irons, L., M. Latorre, and J. D. Humphrey. From transcript to tissue: multiscale modeling from cell signaling to matrix remodeling. Ann. Biomed. Eng. 49(7):1701–1715, 2021. https://doi.org/10.1007/S10439-020-02713-8/FIGURES/8 .
doi: 10.1007/S10439-020-02713-8/FIGURES/8
pubmed: 33415527
pmcid: 8260704
Ishikawa, A., K. Ogawa, Y. Tokinaga, N. Uematsu, K. Mizumoto, and Y. Hatano. The mechanism behind the inhibitory effect of isoflurane on angiotensin II-induced vascular contraction is different from that of sevoflurane. Anesth. Analgesia. 105(1):97–102, 2007. https://doi.org/10.1213/01.ANE.0000265851.37923.EC .
doi: 10.1213/01.ANE.0000265851.37923.EC
Jung, S., P. I. Zimin, C. B. Woods, E. B. Kayser, D. Haddad, C. R. Reczek, K. Nakamura, J. M. Ramirez, M. M. Sedensky, and P. G. Morgan. Isoflurane inhibition of endocytosis is an anesthetic mechanism of action. Curr. Biol. 32(14):3016–3032, 2022. https://doi.org/10.1016/J.CUB.2022.05.037 .
doi: 10.1016/J.CUB.2022.05.037
pubmed: 35688155
pmcid: 9329204
Korneva, A., and J. D. Humphrey. Maladaptive aortic remodeling in hypertension associates with dysfunctional smooth muscle contractility. Am. J. Physiol.-Heart Circ. Physiol. 316(2):H265–H278, 2019. https://doi.org/10.1152/AJPHEART.00503.2017 .
doi: 10.1152/AJPHEART.00503.2017
pubmed: 30412437
Laurent, S., and P. Boutouyrie. The structural factor of hypertension. Circ. Res. 116(6):1007–1021, 2015. https://doi.org/10.1161/CIRCRESAHA.116.303596 .
doi: 10.1161/CIRCRESAHA.116.303596
pubmed: 25767286
Lerman, L. O., T. W. Kurtz, R. M. Touyz, D. H. Ellison, A. R. Chade, S. D. Crowley, D. L. Mattson, J. J. Mullins, J. Osborn, A. Eirin, J. F. Reckelhoff, C. Iadecola, and T. M. Coffman. Animal models of hypertension: a scientific statement from the american heart association. Hypertension. 73(6):e87–e120, 2019. https://doi.org/10.1161/HYP.0000000000000090 .
doi: 10.1161/HYP.0000000000000090
pubmed: 30866654
Low, L. A., L. C. Bauer, and B. A. Klaunberg. Comparing the effects of isoflurane and alpha chloralose upon mouse physiology. PLoS ONE.11(5):e0154936, 2016. https://doi.org/10.1371/JOURNAL.PONE.0154936 .
doi: 10.1371/JOURNAL.PONE.0154936
pubmed: 27148970
pmcid: 4858227
Lu, H., D. L. Rateri, D. Bruemmer, L. A. Cassis, and A. Daugherty. Involvement of the renin–angiotensin system in abdominal and thoracic aortic aneurysms. Clin. Sci. 123(9):531–543, 2012. https://doi.org/10.1042/CS20120097 .
doi: 10.1042/CS20120097
Moireau, P., N. Xiao, M. Astorino, C. A. Figueroa, D. Chapelle, C. A. Taylor, and J.-F. Gerbeau. External tissue support and fluid-structure simulation in blood flows. Biomech. Model. Mechanobiol. 11:1–18, 2012. https://doi.org/10.1007/s10237-011-0289-z .
doi: 10.1007/s10237-011-0289-z
pubmed: 21308393
Navarro, K. L., M. Huss, J. C. Smith, P. Sharp, J. O. Marx, and C. Pacharinsak. Mouse anesthesia: the art and science. ILAR J. 62(1–2):238–273, 2021. https://doi.org/10.1093/ILAR/ILAB016 .
doi: 10.1093/ILAR/ILAB016
pubmed: 34180990
pmcid: 9236661
Phillips, E. H., P. Di Achille, M. R. Bersi, J. D. Humphrey, and C. J. Goergen. Multi-modality imaging enables detailed hemodynamic simulations in dissecting aneurysms in mice. IEEE Trans. Med. Imaging. 36(6):1297–1305, 2017. https://doi.org/10.1109/TMI.2017.2664799 .
doi: 10.1109/TMI.2017.2664799
pubmed: 28186882
pmcid: 5505237
Sahni, O., J. Müller, K. E. Jansen, M. S. Shephard, and C. A. Taylor. Efficient anisotropic adaptive discretization of the cardiovascular system. Comput. Methods Appl. Mech. Eng. 195(41–43):5634–5655, 2006. https://doi.org/10.1016/J.CMA.2005.10.018 .
doi: 10.1016/J.CMA.2005.10.018
Samain, E., H. Bouillier, C. Rucker-Martin, J. X. Mazoit, J. Marty, J. F. Renaud, and G. Dagher. Isoflurane alters angiotensin II–induced Ca2+mobilization in aortic smooth muscle cells from hypertensive ratsimplication of cytoskeleton. Anesthesiology. 97(3):642–651, 2002. https://doi.org/10.1097/00000542-200209000-00019 .
doi: 10.1097/00000542-200209000-00019
pubmed: 12218532
Seyde, W. C., and D. E. Longnecker. Anesthetic influences on regional hemodynamics in normal and hemorrhaged rats. Anesthesiology. 61(6):686–698, 1984. https://doi.org/10.1097/00000542-198412000-00010 .
doi: 10.1097/00000542-198412000-00010
pubmed: 6439073
Simon, A. C., M. E. Safar, J. A. Levenson, G. M. London, B. I. Levy, N. P. Chau, M. E. Safar, and J. A. Levenson. An evaluation of large arteries compliance in man. Am. J. Physiol.-Heart Circ. Physiol. 237(5):H550–H554, 1979.
doi: 10.1152/ajpheart.1979.237.5.H550
Sparks, M. A., S. D. Crowley, S. B. Gurley, M. Mirotsou, and T. M. Coffman. Classical Renin-Angiotensin system in kidney physiology. Compr. Physiol. 4(3):1201–1228, 2014. https://doi.org/10.1002/CPHY.C130040 .
doi: 10.1002/CPHY.C130040
pubmed: 24944035
pmcid: 4137912
Swaney, J. S. Impact of anesthesia on cardiac function during echocardiography in mice. Am. J. Physiol. Heart Circ. Physiol. 282(6):H2134–H2140, 2002. https://doi.org/10.1152/ajpheart.00845.2001 .
doi: 10.1152/ajpheart.00845.2001
pubmed: 12003821
Takuma, S., K. Suehiro, C. Cardinale, T. Hozumi, H. Yano, J. Shimizu, S. Mullis-Jansson, R. Sciacca, J. Wang, D. Burkhoff, M. R. di Tullio, and S. Homma. Anesthetic inhibition in ischemic and nonischemic murine heart: comparison with conscious echocardiographic approach. Am. J. Physiol.-Heart Circ. Physiol. 280(5):H2364–H2370, 2001. https://doi.org/10.1152/AJPHEART.2001.280.5.H2364/ASSET/IMAGES/LARGE/H40510763003.JPEG .
doi: 10.1152/AJPHEART.2001.280.5.H2364/ASSET/IMAGES/LARGE/H40510763003.JPEG
pubmed: 11299243
Tan, T. P., X. M. Gao, M. Krawczyszyn, X. Feng, H. Kiriazis, A. M. Dart, and X. J. Du. Assessment of cardiac function by echocardiography in conscious and anesthetized mice: importance of the autonomic nervous system and disease state. J. Cardiovasc. Pharmacol. 42(2):182–190, 2003. https://doi.org/10.1097/00005344-200308000-00005 .
doi: 10.1097/00005344-200308000-00005
pubmed: 12883320
Trachet, B., J. Bols, J. Degroote, B. Verhegghe, N. Stergiopulos, J. Vierendeels, and P. Segers. An animal-specific FSI model of the abdominal aorta in anesthetized mice. Ann. Biomed. Eng. 43(6):1298–1309, 2015. https://doi.org/10.1007/s10439-015-1310-y .
doi: 10.1007/s10439-015-1310-y
pubmed: 25824368
Ullman, J., R. Härgestam, S. Lindahl, S. H. H. Chan, S. Eriksson, and M. Rundgren. Circulatory effects of angiotensin II during anaesthesia, evaluated by real-time spectral analysis. Acta Anaesth. Scand. 47(5):532–540, 2003. https://doi.org/10.1034/J.1399-6576.2003.00114.X .
doi: 10.1034/J.1399-6576.2003.00114.X
pubmed: 12699509
Weiss, D., A. S. Long, G. Tellides, S. Avril, J. D. Humphrey, and M. R. Bersi. Evolving mural defects, dilatation, and biomechanical dysfunction in angiotensin II-induced thoracic aortopathies. Arteriosclerosis Thromb. Vasc. Biol. 42(8):973–986, 2022. https://doi.org/10.1161/ATVBAHA.122.317394 .
doi: 10.1161/ATVBAHA.122.317394
Wilde, E., A. A. Aubdool, P. Thakore, L. Baldissera, K. M. Alawi, J. Keeble, M. Nandi, and S. D. Brain. Tail-cuff technique and its influence on central blood pressure in the mouse. J. Am. Heart Assoc.6(6):e005204, 2017. https://doi.org/10.1161/JAHA.116.005204 .
doi: 10.1161/JAHA.116.005204
pubmed: 28655735
pmcid: 5669161
Wu, J., S. R. Thabet, A. Kirabo, D. W. Trott, M. A. Saleh, L. Xiao, M. S. Madhur, W. Chen, and D. G. Harrison. Inflammation and mechanical stretch promote aortic stiffening in hypertension through activation of p38 mitogen-activated protein kinase. Circ. Res. 114(4):616–625, 2014. https://doi.org/10.1161/CIRCRESAHA.114.302157 .
doi: 10.1161/CIRCRESAHA.114.302157
pubmed: 24347665
Xiao, N., J. Alastruey, and C. Alberto Figueroa. A systematic comparison between 1-D and 3-D hemodynamics in compliant arterial models. Int. J. Numer. Methods Biomed. Eng. 30(2):204–231, 2014. https://doi.org/10.1002/cnm.2598 .
doi: 10.1002/cnm.2598
Yu, J., K. Ogawa, Y. Tokinaga, S. Iwahashi, and Y. Hatano. The vascular relaxing effects of sevoflurane and isoflurane are more important in hypertensive than in normotensive rats. Can. J. Anesth. 51(10):979–985, 2014. https://doi.org/10.1007/BF03018483 .
doi: 10.1007/BF03018483