Abstract
Altered pressure in the develo** left ventricle (LV) results in altered morphology and tissue material properties. Mechanical stress and strain may play a role in the regulating process. This study showed that confocal microscopy, three-dimensional reconstruction, and finite element analysis can provide a detailed model of stress and strain in the trabeculated embryonic heart. The method was used to test the hypothesis that end-diastolic strains are normalized after altered loading of the LV during the stages of trabecular compaction and chamber formation. Stage-29 chick LVs subjected to pressure overload and underload at stage 21 were reconstructed with full trabecular morphology from confocal images and analyzed with finite element techniques. Measured material properties and intraventricular pressures were specified in the models. The results show volume-weighted end-diastolic von Mises stress and strain averaging 50–82 % higher in the trabecular tissue than in the compact wall. The volume-weighted-average stresses for the entire LV were 115, 64, and 147 Pa in control, underloaded, and overloaded models, while strains were 11, 7, and 4 %; thus, neither was normalized in a volume-weighted sense. Localized epicardial strains at mid-longitudinal level were similar among the three groups and to strains measured from high-resolution ultrasound images. Sensitivity analysis showed changes in material properties are more significant than changes in geometry in the overloaded strain adaptation, although resulting stress was similar in both types of adaptation. These results emphasize the importance of appropriate metrics and the role of trabecular tissue in evaluating the evolution of stress and strain in relation to pressure-induced adaptation.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10237-012-0461-0/MediaObjects/10237_2012_461_Fig1_HTML.gif)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10237-012-0461-0/MediaObjects/10237_2012_461_Fig2_HTML.gif)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10237-012-0461-0/MediaObjects/10237_2012_461_Fig3_HTML.jpg)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10237-012-0461-0/MediaObjects/10237_2012_461_Fig4_HTML.gif)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10237-012-0461-0/MediaObjects/10237_2012_461_Fig5_HTML.gif)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10237-012-0461-0/MediaObjects/10237_2012_461_Fig6_HTML.gif)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10237-012-0461-0/MediaObjects/10237_2012_461_Fig7_HTML.gif)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10237-012-0461-0/MediaObjects/10237_2012_461_Fig8_HTML.gif)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10237-012-0461-0/MediaObjects/10237_2012_461_Fig9_HTML.gif)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10237-012-0461-0/MediaObjects/10237_2012_461_Fig10_HTML.gif)
Similar content being viewed by others
References
Auerbach R, Kubai L, Knighton D, Folkman J (1974) A simple procedure for the long-term cultivation of chicken embryos. Dev Biol 41:391–394
Clark EB, Hu N, Turner DR, Litter JE, Hansen J (1991) Effect of chronic verapamil treatment on ventricular function and growth in chick embryos. Am J Physiol Heart Circ Physiol 261:H166–H171
Clark EB, Hu N, Frommelt P, Vandekieft GK, Dummett JL, Tomanek RJ (1989) Effect of increased pressure on ventricular growth in stage 21 chick embryos. Am J Physiol Heart Circ Physiol 257:H55–61
Clark EB, Hu N (1982) Developmental hemodynamic changes in the chick embryo from stage 18 to 27. Circ Res 51:810–815
Damon BJ, Remond MC, Bigelow MR, Trusk TC, **e W, Perucchio R, Sedmera D, Denslow S, Thompson RP (2009) Patterns of muscular strain in the embryonic heart wall. Dev Dyn 238:1535–1546
deAlmeida A, McQuinn T, Sedmera D (2007) Increased ventricular preload is compensated by myocyte proliferation in normal and hypoplastic fetal chick left ventricle. Circ Res 100:1363–1370
Douglas AS, Rodriguez EK, O’Dell W, Hunter WC (1991) Unique strain history during ejection in canine left ventricle. Am J Physiol Heart Circ Physiol 260:H1596–H1611
Emery JL, Omens JH (1997) Mechanical regulation of myocardial growth during volume-overload hypertrophy in the rat. Am J Physiol Heart Circ Physiol 273:H1198–H1204
Filas BA, Efimov IR, Taber LA (2007) Optical coherence tomography as a tool for measuring morphogenetic deformation of the loo** heart. Anat Rec 290:1057–1068
Florenzano F, Glantz SA (1987) Left ventricular mechanical adaptation to chronic aortic regurgitation in intact dogs. Am J Physiol Heart Circ Physiol 252:H969–H984
Grohmann D (1961) Mitotic growth potential of embryonic and fetal chicken hearts and its significance for the understanding of heart malformations. Z Zellforsch Mikrosk Anat 55:104–122
Guccione JM, Costa KD, McCulloch AD (1995) Finite element stress analysis of left ventricular mechanics in the beating dog heart. J Biomech 28:1167–1177
Guccione JM, Waldman LK, McCulloch AD (1993) Mechanics of active contraction in cardiac muscle: part II—cylindrical models of the systolic left ventricle. J Biomech Eng 115:82–90
Hamburger V, Hamilton HL (1992) A series of normal stages in the development of the chick embryo. Dev Dyn 195:231–272
Hoshijima M (2006) Mechanical stress–strain sensors embedded in cardiac cytoskeleton: Z disk, titin, and associated structures. Am J Physiol Heart Circ Physiol 290:H1313–H1325
Jeter JR Jr, Cameron IL (1971) Cell proliferation patterns during cytodifferentiation in embryonic chick tissues: liver, heart and erythrocytes. J Embryol Exp Morphol 25:405–422
Keller BB, Yoshigi M, Tinney JP (1997) Ventricular-vascular uncoupling by acute conotruncal occlusion in the stage 21 chick embryo. Am J Physiol Heart Circ Physiol 273:H2861–H2866
Lin IE, Taber LA (1995) A model for stress-induced growth in the develo** heart. J Biomech Eng 117:343–349
Linke WA (2008) Sense and stretchability: the role of titin and titin-associated proteins in myocardial stress-sensing and mechanical dysfunction. Cardiovasc Res 77:637–648
Martinsen BJ (2005) Reference guide to the stages of chick heart embryology. Dev Dyn 233:1217–1237. doi:10.1002/dvdy.20468
McQuinn TC, Bratoeva M, Dealmeida A, Remond M, Thompson RP, Sedmera D (2007) High-frequency ultrasonographic imaging of avian cardiovascular development. Dev Dyn 236:3503–3513. doi:10.1002/dvdy.21357
Miller CE, Thompson RP, Bigelow MR, Gittinger G, Trusk TC, Sedmera D (2005) Confocal imaging of the embryonic heart: how deep? Microsc Microanal 11:216–223
Miller CE, Wong CL, Sedmera D (2003) Pressure overload alters stress–strain properties of the develo** chick heart. Am J Physiol Heart Circ Physiol 285:H1849–H1856
Nguyen TN, Chagas AC, Glantz SA (1993) Left ventricular adaptation to gradual renovascular hypertension in dogs. Am J Physiol Heart Circ Physiol 265:H22–H38
O’Dell WG, Schoeniger JS, Blackband SJ, McVeigh ER (1994) A modified quadrupole gradient set for use in high resolution MRI tagging. Magn Reson Med 32:246–250
Omens JH (1998) Stress and strain as regulators of myocardial growth. Prog Biophys Mol Biol 69:559–572
Poelma C, Van der Heiden K, Hierck BP, Poelmann RE, Westerweel J (2009) Measurements of the wall shear stress distribution in the outflow tract of an embryonic chicken heart. J R Soc Interface 7:91–103
Reckova M, Rosengarten C, deAlmeida A, Stanley CP, Wessels A, Gourdie RG, Thompson RP, Sedmera D (2003) Hemodynamics is a key epigenetic factor in development of the cardiac conduction system. Circ Res 93:77–85
Rychter Z, Rychterova V, Lemez L (1979) Formation of the heart loop and proliferation structure of its wall as a base for ventricular septation. Herz 4:86–90
Sedmera D, Pexieder T, Rychterova V, Hu N, Clark EB (1999) Remodeling of chick embryonic ventricular myoarchitecture under experimentally changed loading conditions. Anat Rec 254: 238–252
Sedmera D, Pexieder T, Hu N, Clark EB (1998) A quantitative study of the ventricular myoarchitecture in the stage 21–29 chick embryo following decreased loading. Eur J Morphol 36: 105–119
Taber LA (2001) Biomechanics of cardiovascular development. Annu Rev Biomed Eng 3:1–25
Taber LA, Chabert S (2002) Theoretical and experimental study of growth and remodeling in the develo** heart. Biomech Model Mechanobiol 1:29–43
Taber LA, Hu N, Pexieder T, Clark EB, Keller BB (1993) Residual strain in the ventricle of the stage 16–24 chick embryo. Circ Res 72:455–462
Tobita K, Garrison JB, Liu LJ, Tinney JP, Keller BB (2005) Three-dimensional myofiber architecture of the embryonic left ventricle during normal development and altered mechanical loads. Anat Rec 283:193–201
Tobita K, Schroder EA, Tinney JP, Garrison JB, Keller BB (2002) Regional passive ventricular stress–strain relations during development of altered loads in chick embryo. Am J Physiol Heart Circ Physiol 282:H2386–H2396
Tobita K, Keller BB (2000) Right and left ventricular wall deformation patterns in normal and left heart hypoplasia chick embryos. Am J Physiol Heart Circ Physiol 279:H959–H969
Tuan RS (1983) Supplemented eggshell restores calcium transport in chorioallantoic membrane of cultured shell-less chick embryos. J Embryol Exp Morphol 74:119–131
Wenink AC, Knaapen MW, Vrolijk BC, VanGroningen JP (1996) Development of myocardial fiber organization in the rat heart. Anat Embryol 193:559–567
Wong CL, Miller CE (2002) Residual strain changes with left ventricular pressure in the develo** heart. In: 2nd Joint conference of the IEEE engineering in medicine and biology society and the biomedical engineering society, Oct. 23–26, 2002, Houston, TX
**e W, Perucchio R (2001) Multiscale finite element modeling of the trabeculated embryonic heart: numerical evaluation of the constitutive relations for the trabeculated myocardium. Comput Methods Biomech 4:231–248
Acknowledgments
This work was supported by grants from the National Institute of Biomedical Imaging and Bioengineering, National Institutes of Health (EB002077); National Center for Research Resources, National Institutes of Health (RR16434); Academy of Sciences of the Czech Republic Purkinje Fellowship (D.S.); Ministry of Education, Youth and Sports of the Czech Republic (VZ 0021620806); and Grant Agency of the Czech Republic (304/08/0615).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Buffinton, C.M., Faas, D. & Sedmera, D. Stress and strain adaptation in load-dependent remodeling of the embryonic left ventricle. Biomech Model Mechanobiol 12, 1037–1051 (2013). https://doi.org/10.1007/s10237-012-0461-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10237-012-0461-0