Top

Journal of Cardiovascular Magnetic Resonance

Published in:

01-12-2020 | Ventricular Septal Defect | Research

Ex vivo cardiovascular magnetic resonance diffusion weighted imaging in congenital heart disease, an insight into the microstructures of tetralogy of Fallot, biventricular and univentricular systemic right ventricle

Authors: Cyril Tous, Thomas L. Gentles, Alistair A. Young, Beau P. Pontré

Published in: Journal of Cardiovascular Magnetic Resonance | Issue 1/2020

Abstract

Purpose

Common types of congenital heart disease exhibit a variety of structural and functional variations which may be accompanied by changes in the myocardial microstructure. We aimed to compare myocardial architecture from magnetic resonance diffusion tensor imaging (DTI) in preserved pathology specimens.

Materials and methods

Pathology specimens (n = 24) formalin-fixed for 40.8 ± 7.9 years comprised tetralogy of Fallot (TOF, n = 10), dextro-transposition of great arteries (D-TGA, n = 8) five with ventricular septal defect (VSD), systemic right ventricle (n = 4), situs inversus totalis (SIT, n = 1) and levo-TGA (L-TGA, n = 1). Specimens were imaged using a custom spin-echo sequence and segmented automatically according to tissue volume fraction. In each specimen T1, T2, fractional anisotropy, mean diffusivity, helix angle (HA) and sheet angle (E2A) were quantified. Pathologies were compared according to their HA gradient, HA asymmetry and E2A mean value in each myocardial segment (anterior, posterior, septal and lateral walls).

Results

TOF and D-TGA with VSD had decreased helix angle gradient by − 0.34°/% and remained symmetric in the septum in comparison to D-TGA without VSD. Helix angle range was decreased by 45°. It was associated with a decreased HA gradient in the right ventricular (RV) wall, i.e. predominant circumferential myocytes. The sheet angle in the septum of TOF was opposing those of the left ventricular (LV) free wall. Univentricular systemic RV had the lowest HA gradient (− 0.43°/%) and the highest HA asymmetry (75%). HA in SIT was linear, asymmetric, and reversed with a sign change at about 70% of the depth at mid-ventricle. In L-TGA with VSD, HA was asymmetric (90%) and its gradients were decreased in the septum, anterior and lateral wall.

Conclusion

The organization of the myocytes as determined by DTI differs between TOF, D-TGA, L-TGA, systemic RV and SIT specimens. These differences in cardiac structure may further enlighten our understanding of cardiac function in these diverse congenital heart diseases.

Available only for authorised users

Marelli AJ, Ionescu-Ittu R, Mackie AS, et al. Lifetime prevalence of congenital heart disease in the general population from 2000 to 2010. Circulation. 2014;130:749–56. https://doi.org/10.1161/CIRCULATIONAHA.113.008396..CrossRefPubMed

Ou P, Iserin L, Raisky O, et al. Post-operative cardiac lesions after cardiac surgery in childhood. Pediatr Radiol. 2010;40:885–94. https://doi.org/10.1007/s00247-010-1622-x.CrossRefPubMed

Popelová JR, Gebauer R, Černý Š, et al. Operations of adults with congenital heart disease – single center experience with 10 years results. Cor Vasa. 2016;58:e317–27. https://doi.org/10.1016/J.CRVASA.2015.12.005.CrossRef

Putman LM, van Gameren M, Meijboom FJ, et al. Seventeen years of adult congenital heart surgery: a single Centre experience. Eur J Cardiothorac Surg. 2009;36:96–104; discussion 104. https://doi.org/10.1016/j.ejcts.2009.01.046.CrossRefPubMed

Bolger AP, Coats AJS, Gatzoulis MA. Congenital heart disease: the original heart failure syndrome. Eur Heart J. 2003;24:970–6. https://doi.org/10.1016/S0195-668X(03)00005-8.CrossRefPubMed

Hein S, Arnon E, Kostin S, et al. Progression from compensated hypertrophy to failure in the pressure-overloaded human: heart structural deterioration and compensatory mechanisms. Circulation. 2003;107:984–91. https://doi.org/10.1161/01.CIR.0000051865.66123.B7.CrossRefPubMed

Reynolds HR, Tunick PA, Grossi EA, et al. Paradoxical septal motion after cardiac surgery: a review of 3,292 cases. Clin Cardiol. 2007;30:621–3. https://doi.org/10.1002/clc.20201.CrossRefPubMedPubMedCentral

LeGrice IJ, Smaill BH, Chai LZ, et al. Laminar structure of the heart: ventricular myocyte arrangement and connective tissue architecture in the dog. Am J Phys. 1995;269:H571–82.

Scollan DF, Holmes A, Zhang J, Winslow RL. Reconstruction of cardiac ventricular geometry and Fiber orientation using magnetic resonance imaging. Ann Biomed Eng. 2000;28:934–44. https://doi.org/10.1114/1.1312188.CrossRefPubMedPubMedCentral

10.

Basser PJ, Mattiello J, LeBihan D. MR diffusion tensor spectroscopy and imaging. Biophys J. 1994;66:259–67. https://doi.org/10.1016/S0006-3495(94)80775-1.CrossRefPubMedPubMedCentral

11.

Le Bihan D, Mangin JF, Poupon C, et al. Diffusion tensor imaging: concepts and applications. J Magn Reson Imaging. 2001;13:534–46. https://doi.org/10.1002/jmri.1076.CrossRefPubMed

12.

Reese TG, Weisskoff RM, Smith RN, et al. Imaging myocardial fiber architecture in vivo with magnetic resonance. Magn Reson Med. 1995;34:786–91. https://doi.org/10.1002/mrm.1910340603.CrossRefPubMed

13.

Scollan DF, Holmes A, Winslow R, Forder J. Histological validation of myocardial microstructure obtained from diffusion tensor magnetic resonance imaging. Am J Phys. 1998;275:H2308–18.

14.

Hsu EW, Muzikant AL, Matulevicius SA, et al. Magnetic resonance myocardial fiber-orientation mapping with direct histological correlation. Am J Phys. 1998;274:H1627–34.

15.

Lombaert H. Statistical Atlas of Human Cardiac Fibers Comparison with Abnormal Hearts; 2012.CrossRef

16.

Lombaert H, Peyrat JM, Fanton L, Cheriet F (2012) Variability of the Human Cardiac Laminar Structure. http://www.springerlink.com/index/D371724626245740.pdf. Accessed 26 May 2016.

17.

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;69:661–76. https://doi.org/10.1016/j.jacc.2016.11.051.CrossRefPubMedPubMedCentral

18.

Ferreira P, Kilner PJ, McGill L-A, et al. Aberrant myocardial sheetlet mobility in hypertrophic cardiomyopathy detected using in vivo cardiovascular magnetic resonance diffusion tensor imaging. J Cardiovasc Magn Reson. 2014;16:P338. https://doi.org/10.1186/1532-429X-16-S1-P338.CrossRefPubMedCentral

19.

Khalique Z, Ferreira PF, Scott AD, et al. Diffusion tensor cardiovascular magnetic resonance of microstructural recovery in dilated cardiomyopathy. JACC Cardiovasc Imaging. 2018. https://doi.org/10.1016/j.jcmg.2018.01.025.

20.

Cheng J, Shen D, Yap P-T, Basser PJ. Novel single and multiple Shell uniform sampling schemes for diffusion MRI using spherical codes. Cham: Springer; 2015. p. 28–36.

21.

Conturo TE, McKinstry RC, Aronovitz JA, Neil JJ. Diffusion MRI: precision, accuracy and flow effects. NMR Biomed. 1995;8:307–32. https://doi.org/10.1002/nbm.1940080706.CrossRefPubMed

22.

Jones DK, Horsfield MA, Simmons A. Optimal strategies for measuring diffusion in anisotropic systems by magnetic resonance imaging. Magn Reson Med. 1999;42:515–25. https://doi.org/10.1002/(SICI)1522-2594(199909)42:3<515::AID-MRM14>3.0.CO;2-Q.CrossRefPubMed

23.

Garrido L, Wedeen VJ, Kwong KK, et al. Anisotropy of water diffusion in the myocardium of the rat. Circ Res. 1994;74:789–93. https://doi.org/10.1161/01.RES.74.5.789.CrossRefPubMed

24.

Holmes AA, Scollan DF, Winslow RL. Direct histological validation of diffusion tensor MRI in formaldehyde- fixed myocardium. Magn Reson Med. 2000;44:157–61. https://doi.org/10.1002/1522-2594(200007)44:1<157::AID-MRM22>3.0.CO;2-F.CrossRefPubMed

25.

Colombo NM. Numerical modelling of ventricular mechanics : role of the myofibre architecture; 2014.

26.

Zomer AC, Uiterwaal CSPM, Der Velde ET Van, et al (2011) Mortality in adult congenital heart disease: are national registries reliable for cause of death? Int J Cardiol 152:212–217. https://doi.org/10.1016/j.ijcard.2010.07.018.

27.

Engelings CC, Helm PC, Abdul-Khaliq H, et al. Cause of death in adults with congenital heart disease - an analysis of the German National Register for congenital heart defects. Int J Cardiol. 2016;211:31–6. https://doi.org/10.1016/j.ijcard.2016.02.133.CrossRefPubMed

28.

Brickner ME, Hillis LD, Lange RA. Congenital heart disease in adults. N Engl J Med. 2000;342:256–63. https://doi.org/10.1056/NEJM200001273420407.CrossRefPubMed

29.

Hoffman JI, Kaplan S, Liberthson RR. Prevalence of congenital heart disease. Am Heart J. 2004;147:425–39. https://doi.org/10.1016/J.AHJ.2003.05.003.CrossRefPubMed

30.

Sanchez-Quintana. Ventricular myoarchitecture in tetralogy of Fallot. Heart. 1996;76:280–6. https://doi.org/10.1136/hrt.76.3.280.CrossRefPubMedPubMedCentral

31.

Varray F, Mirea I, Langer M, et al. Extraction of the 3D local orientation of myocytes in human cardiac tissue using X-ray phase-contrast micro-tomography and multi-scale analysis. Med Image Anal. 2017;38:117–32. https://doi.org/10.1016/J.MEDIA.2017.02.006.CrossRefPubMed

32.

Jouk P-S, Usson Y, Michalowicz G, Grossi L. Three-dimensional cartography of the pattern of the myofibres in the second trimester fetal human heart. Anat Embryol (Berl). 2000;202:103–18. https://doi.org/10.1007/s004290000103.CrossRef

33.

Sheehan FH, Ge S, Vick GW III, et al. Three-dimensional shape analysis of right ventricular remodeling in repaired tetralogy of Fallot. Am J Cardiol. 2008;101:107–13. https://doi.org/10.1016/j.amjcard.2007.07.080.CrossRefPubMed

34.

Smerup M, Nielsen E, Agger P, et al. The three-dimensional arrangement of the myocytes aggregated together within the mammalian ventricular myocardium. Anat Rec. 2009;292:1–11. https://doi.org/10.1002/ar.20798.CrossRef

35.

Bovendeerd PHM, Huyghe JM, Arts T, et al. Influence of endocardial-epicardial crossover of muscle fibers on left ventricular wall mechanics. J Biomech. 1994;27:941–51. https://doi.org/10.1016/0021-9290(94)90266-6.CrossRefPubMed

36.

Greenbaum RA, Ho SY, Gibson DG, et al. Left ventricular fibre architecture in man. Heart. 1981;45:248–63. https://doi.org/10.1136/hrt.45.3.248.CrossRef

37.

Helm PA, Younes L, Beg MF, et al. Evidence of structural remodeling in the dyssynchronous failing heart. Circ Res. 2006;98:125–32. https://doi.org/10.1161/01.RES.0000199396.30688.eb.CrossRefPubMed

38.

Sanchez-Quintana D, Garcia-Martinez V, Climent V, et al. Morphological changes in the normal pattern of ventricular myoarchitecture in the developing human heart. Anat Rec. 1995;243:483–95. https://doi.org/10.1002/ar.1092430411.CrossRefPubMed

39.

Trzebiatowska-Krzynska A, Swahn E, Wallby L, et al. Afterload dependence of right ventricular myocardial deformation: a comparison between tetralogy of Fallot and atrially corrected transposition of the great arteries in adult patients. PLoS One. 2018;13:e0204435. https://doi.org/10.1371/journal.pone.0204435.CrossRefPubMedPubMedCentral

40.

Young AA, Cowan BR. Evaluation of left ventricular torsion by cardiovascular magnetic resonance. J Cardiovasc Magn Reson. 2012;14:49. https://doi.org/10.1186/1532-429X-14-49.CrossRefPubMedPubMedCentral

41.

Corno AF, Kocica MJ. Potential implications of the helical heart in congenital heart defects. Semin Thorac Cardiovasc Surg Pediatr Card Surg Annu. 2007;10:61–7. https://doi.org/10.1053/j.pcsu.2007.01.001.CrossRef

42.

Harmer J, Toussaint N, Pushparajah K, Stoeck CT, Chan RW, Razavi R, Kozerke S. In-vivo Diffusion Tensor Imaging of the Systemic Right Ventricle at 3T. Salt Lake City. Proc Intl Soc Mag Reson Med. 2013;21(3098).

43.

Chang M-C, Wu M-T, Weng K-P, et al. Left ventricular regional myocardial motion and twist function in repaired tetralogy of Fallot evaluated by magnetic resonance tissue phase mapping. Eur Radiol. 2018;28:104–14. https://doi.org/10.1007/s00330-017-4908-7.CrossRefPubMed

44.

Colli Franzone P, Guerri L, Pennacchio M, Taccardi B. Spread of excitation in 3-D models of the anisotropic cardiac tissue. II. Effects of fiber architecture and ventricular geometry. Math Biosci. 1998;147:131–71. https://doi.org/10.1016/S0025-5564(97)00093-X.CrossRef

45.

Roberts D, Hersh L, Scher A. Influence of cardiac Fiber orientation on Wavefront voltage, conduction velocity, and tissue resistivity in the dog. Circ Res. 1979;44:701–12. https://doi.org/10.1161/01.RES.44.5.701.CrossRefPubMed

46.

Aumentado-Armstrong T, Kadivar A, Savadjiev P, et al. Conduction in the Heart Wall: Helicoidal fibers minimize diffusion Bias. Sci Rep. 2018;8:7165. https://doi.org/10.1038/s41598-018-25334-7.CrossRefPubMedPubMedCentral

47.

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. https://doi.org/10.1016/S0140-6736(00)02714-8.CrossRefPubMed

48.

Uebing A, Gibson DG, Babu-Narayan SV, et al. Right ventricular mechanics and QRS duration in patients with repaired tetralogy of Fallot implications of Infundibular disease. Circulation. 2007;116:1532–9. https://doi.org/10.1161/CIRCULATIONAHA.107.688770.CrossRefPubMed

49.

Baillie M (1789) An account of a remarkable transposition of the viscera in the human body. London Med J 10:178–197.

50.

Taussig HB. The anatomy of the heart in two cases of situs transversus. Bull Johns Hopkins Hosp. 1926;39:199–202. .

51.

Matsumura H, Aizawa Y, Kumaki K. Myocardial architecture in situs inversus viscerum totalis. In: Developmental Cardiology: Morphogenesis and Function, edited by Clark EB and Takao A. Mount Kisco: Futura; 1990. p. 605–24.

52.

Asami I, Koizumi K. The vortex cordis is never reversely directed, even in situs inversus and L-loop anomaly. Kaibogaku Zasshi. 1989;64:36–45.PubMed

53.

Khalique Z, Ferreira PF, Scott AD, et al. Deranged Myocyte microstructure in Situs Inversus Totalis demonstrated by diffusion tensor cardiac magnetic resonance. JACC Cardiovasc Imaging. 2018. https://doi.org/10.1016/J.JCMG.2017.11.014.

54.

Delhaas T, Decaluwe W, Rubbens M, et al. Cardiac fiber orientation and the left-right asymmetry determining mechanism. Ann N Y Acad Sci. 2004;1015:190–201. https://doi.org/10.1196/annals.1302.016.CrossRefPubMed

55.

Delhaas T, Kroon W, Decaluwe W, et al. Structure and torsion of the normal and situs inversus totalis cardiac left ventricle. I. Experimental data in humans. Am J Physiol Circ Physiol. 2008;295:H197–201. https://doi.org/10.1152/ajpheart.00876.2007.CrossRef

56.

Kroon W, Delhaas T, Arts T, Bovendeerd P. Constitutive modeling of cardiac tissue growth. In: Functional imaging and modeling of the heart. Berlin Heidelberg, Berlin, Heidelberg: Springer; 2007. p. 340–9.CrossRef

57.

Rossi AC, Pluijmert M, Bovendeerd PHM, et al. Assessment and comparison of left ventricular shear in normal and situs inversus totalis hearts by means of magnetic resonance tagging. Am J Physiol Circ Physiol. 2015;308:H416–23. https://doi.org/10.1152/ajpheart.00502.2014.CrossRef

58.

Pluijmert M, Kroon W, Delhaas T, Bovendeerd PHM. Adaptive reorientation of cardiac myofibers: the long-term effect of initial and boundary conditions. Mech Res Commun. 2012;42:60–7. https://doi.org/10.1016/J.MECHRESCOM.2011.11.011.CrossRef

59.

Vaujois L, Gorincour G, Alison M, et al. Imaging of postoperative tetralogy of Fallot repair. Diagn Interv Imaging. 2016;97:549–60. https://doi.org/10.1016/j.diii.2016.02.007.CrossRefPubMed

Title: Ex vivo cardiovascular magnetic resonance diffusion weighted imaging in congenital heart disease, an insight into the microstructures of tetralogy of Fallot, biventricular and univentricular systemic right ventricle
Authors: Cyril Tous
Thomas L. Gentles
Alistair A. Young
Beau P. Pontré
Publication date: 01-12-2020
Publisher: BioMed Central
Keywords: Ventricular Septal Defect
Tetralogy of Fallot
Tetralogy of Fallot
Transposition of the Great Artery
Ventricular Septal Defect
Published in: Journal of Cardiovascular Magnetic Resonance / Issue 1/2020
Electronic ISSN: 1532-429X
DOI: https://doi.org/10.1186/s12968-020-00662-8

At a glance: The STEP trials

Springer Medicine

Ex vivo cardiovascular magnetic resonance diffusion weighted imaging in congenital heart disease, an insight into the microstructures of tetralogy of Fallot, biventricular and univentricular systemic right ventricle

Abstract

Purpose

Materials and methods

Results

Conclusion

At a glance: The STEP trials

Springer Medicine

Abstract

Purpose

Materials and methods

Results

Conclusion

Please log in to get access to this content

Other articles of this Issue 1/2020

Correction to: Cardiovascular magnetic resonance native T2 and T2* quantitative values for cardiomyopathies and heart transplantations: a systematic review and meta-analysis

A direct comparison of 3 T contrast-enhanced whole-heart coronary cardiovascular magnetic resonance angiography to dual-source computed tomography angiography for detection of coronary artery stenosis: a single-center experience

Society for Cardiovascular Magnetic Resonance (SCMR) recommended CMR protocols for scanning patients with active or convalescent phase COVID-19 infection

Quantitative evaluation of carotid atherosclerotic vulnerable plaques using in vivo T1 mapping cardiovascular magnetic resonaonce: validation by histology

Incremental prognostic value of coronary flow reserve determined by phase-contrast cine cardiovascular magnetic resonance of the coronary sinus in patients with diabetes mellitus

Prognostic value of mean velocity at the pulmonary artery estimated by cardiovascular magnetic resonance as a prognostic predictor in a cohort of patients with new-onset heart failure with reduced ejection fraction