Changes in overall ventricular myocardial architecture in the setting of a porcine animal model of right ventricular dilation

Journal of Cardiovascular Magnetic Resonance

Volumn 19, Issue 1, 2017, Pages

  Agger, Peter ^a,c   Ilkjær, Christine ^a,c   Laustsen, Christoffer ^a,c   Smerup, Morten ^d   Frandsen, Jesper R ^a   Ringgaard, Steffen ^a,c   Pedersen, Michael ^a,c   Partridge, John B ^e   Anderson, Robert H ^b   Hjortdal, Vibeke ^a,c  

^a AARHUS UNIVERSITY HOSPITAL   (Denmark)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

^c AARHUS UNIVERSITY   (Denmark)

^d Rigshospitalet   (Denmark)

^e AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

Author keywords

Congenital heart disease; Diffusion tensor imaging; Heart failure; Myocardial remodeling

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CARDIAC MUSCLE CELL; CARDIOVASCULAR MAGNETIC RESONANCE; CONTROLLED STUDY; DIFFUSION TENSOR IMAGING; FEMALE; FOLLOW UP; HEART OUTPUT; HEART RIGHT VENTRICLE FUNCTION; IMAGE ANALYSIS; LIMIT OF QUANTITATION; NONHUMAN; PRIORITY JOURNAL; PULMONARY VALVE INSUFFICIENCY; RIGHT VENTRICULAR DILATION; THORACOTOMY; ANIMAL; COMPLICATION; DIAGNOSTIC IMAGING; DISEASE MODEL; HEART CONTRACTION; HEART LEFT VENTRICLE FUNCTION; HEART RIGHT VENTRICLE HYPERTROPHY; HEART VENTRICLE REMODELING; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; PATHOPHYSIOLOGY; PIG; TIME FACTOR;

ANIMALS; DIFFUSION TENSOR IMAGING; DISEASE MODELS, ANIMAL; FEMALE; HYPERTROPHY, RIGHT VENTRICULAR; MAGNETIC RESONANCE IMAGING; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; PULMONARY VALVE INSUFFICIENCY; SUS SCROFA; TIME FACTORS; VENTRICULAR FUNCTION, LEFT; VENTRICULAR FUNCTION, RIGHT; VENTRICULAR REMODELING;

EID: 85035212961     PISSN: 10976647     EISSN: 1532429X     Source Type: Journal    
DOI: 10.1186/s12968-017-0404-0     Document Type: Article

References (43)

1. Chaturvedi RR, Redington AN. Pulmonary regurgitation in congenital heart disease. Heart. 2007, Jul;93:880-9.
2. Gatzoulis MA, Balaji S, Webber SA, et al. Risk factors for arrhythmia and sudden cardiac death late after repair of tetralogy of fallot: a multicentre study. Lancet. 2000;356:975-81.
3. Sorrell VL, Altbach MI, Kudithipudi V, Squire SW, Goldberg SJ, Klewer SE, Cardiac MRI. Is an important complementary tool to doppler echocardiography in the management of patients with pulmonary regurgitation. Echocardiography. 2007, Mar;24:316-28.
4. van Straten A, Vliegen HW, Hazekamp MG, de Roos A. Right ventricular function late after total repair of tetralogy of fallot. Eur Radiol. 2005, Apr;15:702-7.
5. Ferreira PF, Kilner PJ, McGill LA, et al. Vivo cardiovascular magnetic resonance diffusion tensor imaging shows evidence of abnormal myocardial laminar orientations and mobility in hypertrophic cardiomyopathy. J Cardiovasc Magn Reson. 2014;16:87.
6. Agger P, Lakshminrusimha S, Laustsen C, et al. The myocardial architecture changes in persistent pulmonary hypertension of the newborn in an ovine animal model. Pediatr Res. 2016, Dec 9;79:565-74.
7. Nielles-Vallespin S, Khalique Z, Ferreira PF, et al. Assessment of myocardial microstructural dynamics by in vivo diffusion tensor cardiac magnetic resonance. J Am Coll Cardiol. 2017, Feb 14;69:661-76.
8. Streeter DD, Spotnitz HM, Patel DP, Ross J, Sonnenblick EH. Fiber orientation in the canine left ventricle during diastole and systole. Circ Res. 1969;24:339-47.
9. Sanchez-Quintana D, Anderson RH, Ho SY. Ventricular myoarchitecture in tetralogy of fallot. Heart. 1996, Sep;76:280-6.
10. Harrington KB, Rodriguez F, Cheng A, et al. Direct measurement of transmural laminar architecture in the anterolateral wall of the ovine left ventricle: new implications for wall thickening mechanics. Am J Physiol Heart Circ Physiol. 2005, Mar;288:H1324-30.
11. Hsu EW, Muzikant AL, Matulevicius SA, Penland RC, Henriquez CS. Magnetic resonance myocardial fiber-orientation mapping with direct histological correlation. Am J Phys. 1998, May;274:H1627-34.
12. Edelman RR, Gaa J, Wedeen VJ, et al. Vivo measurement of water diffusion in the human heart. Magn Reson Med. 1994;32:423-8.
13. Smerup M, Nielsen E, Agger P, et al. The three-dimensional arrangement of the myocytes aggregated together within the mammalian ventricular myocardium. Anat Rec (Hoboken). 2009, Jan;292:1-11.
14. Mori S. Mathematics of diffusion tensor imaging. In: Introduction to diffusion tensor imaging. San Diego: academic press; 2014. p. 33-7.
15. Hales PW, Schneider JE, Burton RA, Wright BJ, Bollensdorff C, Kohl P. Histo-anatomical structure of the living isolated rat heart in two contraction states assessed by diffusion tensor MRI. Prog Biophys Mol Biol. 2012;110:319-30.
16. Lunkenheimer PP, Niederer P. Hierarchy and inhomogeneity in the systematic structure of the mammalian myocardium: towards a comprehensive view of cardiodynamics. Technol Health Care. 2012;20:423-34.
17. Stephenson RS, Agger P, Lunkenheimer PP, et al. The functional architecture of skeletal compared to cardiac musculature; myocyte orientation, lamellar unit morphology, and the helical ventricular myocardial band. Clin Anat. 2016;29(3):316-32.
18. LeGrice IJ, Hunter PJ, Smaill BH. Laminar structure of the heart: a mathematical model. Am J Phys Heart Circ Phys. 1997;272:H2466-76.
19. LeGrice IJ, Takayama Y, Covell JW. Transverse shear along myocardial cleavage planes provides a mechanism for normal systolic wall thickening. Circ Res. 1995;77:182-93.
20. Nielsen EA, Smerup M, Agger P, et al. Normal right ventricular three-dimensional architecture, as assessed with diffusion tensor magnetic resonance imaging, is preserved during experimentally induced right ventricular hypertrophy. Anat Rec (Hoboken). 2009, May;292:640-51.
21. Agger P, Hyldebrandt JA, Nielsen EA, Hjortdal V, Smerup MA. Novel porcine model for right ventricular dilatation by external suture plication of the pulmonary valve leaflets - practical and reproducible. Interact Cardiovasc Thorac Surg. 2010, Jun;10:962-6.
22. Hyldebrandt JA, Agger P, Sivén E, et al. Effects of milrinone and epinephrine or dopamine on biventricular function and hemodynamics in right heart failure after pulmonary regurgitation. Am J Physiol Heart Circ Physiol. 2015, Sep;309:H860-6.
23. Jones DK. The effect of gradient sampling schemes on measures derived from diffusion tensor MRI: a monte carlo study. Magn Reson Med. 2004, Apr;51:807-15.
24. Heiberg E, Sjögren J, Ugander M, Carlsson M, Engblom H, Arheden H. Design and validation of segment - freely available software for cardiovascular image analysis. BMC Med Imaging. 2010;10:1.
25. Mori S, Crain BJ, Chacko VP, van Zijl PC. Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Ann Neurol. 1999, Feb;45:265-9.
26. Wakana S, Jiang H, Nagae-Poetscher LM, van Zijl PC, Mori S. Fiber tract-based atlas of human white matter anatomy. Radiology. 2004, Jan;230:77-87.
27. Rollins N, Reyes T, Chia J. Diffusion tensor imaging in lissencephaly. AJNR Am J Neuroradiol. 2005;26:1583-6.
28. Ruetten H, Dimmeler S, Gehring D, Ihling C, Zeiher AM. Concentric left ventricular remodeling in endothelial nitric oxide synthase knockout mice by chronic pressure overload. Cardiovasc Res. 2005, Jun 1;66:444-53.
29. Zhang L, Allen J, Hu L, Caruthers SD, Wickline SA, Chen J. Cardiomyocyte architectural plasticity in fetal, neonatal, and adult pig hearts delineated with diffusion tensor MRI. Am J Physiol Heart Circ Physiol. 2013, Jan 15;304:H246-52.
30. Hyldebrandt JA, Sivén E, Agger P, et al. Effects of milrinone, epinephrine and dopamine on biventricular function and hemodynamics in an animal model with right ventricular failure after pulmonary artery banding. Am J Physiol heart Circ Physiol. 2015, May 8:ajpheart00921.2014.
31. Li W, Lu M, Banerjee S, et al. Ex vivo diffusion tensor MRI reflects microscopic structural remodeling associated with aging and disease progression in normal and cardiomyopathic syrian hamsters. NMR Biomed. 2009, Oct;22:819-25.
32. Deuster CV, Sammut E, Asner L, et al. Studying dynamic myofiber aggregate reorientation in dilated cardiomyopathy using in vivo magnetic resonance diffusion tensor imaging. Circ Cardiovasc Imaging. 2016, Oct;9:e005018.
33. Streeter DD, Hanna WT. Engineering mechanics for successive states in canine left ventricular myocardium: II. Fiber angle and sarcomere length. Circ Res. 1973, Dec 1;33:656-64.
34. Partridge JB, Smerup MH, Petersen SE, Niederer PF, Anderson RH. Linking left ventricular function and mural architecture: what does the clinician need to know? Heart 2013, Dec 5.
35. Mekkaoui C, Reese TG, Jackowski MP, et al. Diffusion tractography of the entire left ventricle by using free-breathing accelerated simultaneous multisection imaging. Radiology. 2017, Mar;282:850-6.
36. Kiernan JA. Formaldehyde, formalin, paraformaldehyde and glutaraldehyde: What they are and what they do. Microscopy Today. 2000;00-1:8-12.
37. Scollan DF, Holmes A, Winslow R, Forder J. Histological validation of myocardial microstructure obtained from diffusion tensor magnetic resonance imaging. Am J Physiol Heart Circ Physiol. 1998;275:H2308-18.
38. Holmes AA, Scollan DF, Winslow RL. Direct histological validation of diffusion tensor MRI in formaldehyde-fixed myocardium. Magn Reson Med. 2000;44:157-61.
39. Agger P, Lass T, Smerup M, Frandsen J, Pedersen M. Optimal preservation of cardiac tissue prior to DTMRI. J Anat. 2015, Sep 22;227:695-701.
40. Sallin EA. Fiber orientation and ejection fraction in the human left ventricle. Biophys J. 1969;9:954-64.
41. Smerup M, Partridge J, Agger P, et al. A mathematical model of the mechanical link between shortening of the cardiomyocytes and systolic deformation of the left ventricular myocardium. Technol Health Care. 2013;21:63-79.
42. Khalique Z, Ferreira PF, Scott AD, Nielles-Vallespin S, Firmin DN, Pennell DJ. Diffusion tensor CMR in situs inversus: insights into the deranged microstructure and how it affects cardiac function. Eur Heart J. 2017, Aug;38
43. MacIver DH, Dayer MJ. An alternative approach to understanding the pathophysiological mechanisms of chronic heart failure. Int J Cardiol. 2012, Jan 26;154:102-10.