Advertisement

Pediatric Radiology

, Volume 44, Issue 4, pp 403–409 | Cite as

Diffuse myocardial fibrosis following tetralogy of Fallot repair: a T1 mapping cardiac magnetic resonance study

  • Marcelo F. Kozak
  • Andrew Redington
  • Shi-Joon Yoo
  • Mike Seed
  • Andreas Greiser
  • Lars Grosse-WortmannEmail author
Original Article

Abstract

Background

Adverse ventricular remodeling after tetralogy of Fallot (TOF) repair is associated with diffuse myocardial fibrosis.

Objective

The goal of this study was to measure post-contrast myocardial T1 in pediatric patients after TOF repair as surrogates of myocardial fibrosis.

Materials and methods

Children after TOF repair who underwent cardiac magnetic resonance imaging with T1 mapping using the modified look-locker inversion recovery (MOLLI) sequence were included. In addition to routine volumetric and flow data, we measured post-contrast T1 values of the basal interventricular septum, the left ventricular (LV) lateral wall, and the inferior and anterior walls of the right ventricle (RV). Results were compared to data from age-matched healthy controls.

Results

The scans of 18 children who had undergone TOF repair and 12 healthy children were included. Post-contrast T1 values of the left ventricular lateral wall (443 ± 54 vs. 510 ± 77 ms, P = 0.0168) and of the right ventricular anterior wall (333 ± 62 vs. 392 ± 72 ms, P = 0.0423) were significantly shorter in children with TOF repair than in controls, suggesting a higher degree of fibrosis. In children with TOF repair, but not in controls, post-contrast T1 values were shorter in the right ventricle than the left ventricle and shorter in the anterior wall of the right ventricle than in the inferior segments. In the TOF group, post-contrast T1 values of the RV anterior wall correlated with the RV end-systolic volume indexed to body surface area (r = 0.54; r2 = 0.30; P = 0.0238).

Conclusion

In children who underwent tetralogy of Fallot repair the myocardium of both ventricles appears to bear an abnormally high fibrosis burden.

Keywords

Tetralogy of Fallot T1 mapping Cardiac magnetic resonance Myocardial fibrosis Children 

Notes

Conflicts of interest

A. Greiser is a paid employee of the Siemens corporation.

M. F. Kozak, A. Redington, S.-J. Yoo, M. Seed, and L. Grosse-Wortmann have no conflict of interest.

References

  1. 1.
    Broberg CS, Chugh SS, Conklin C et al (2010) Quantification of diffuse myocardial fibrosis and its association with myocardial dysfunction in congenital heart disease. Circ Cardiovasc Imaging 3:727–734PubMedCentralPubMedCrossRefGoogle Scholar
  2. 2.
    Conrad CH, Brooks WW, Hayes JA et al (1995) Myocardial fibrosis and stiffness with hypertrophy and heart failure in the spontaneously hypertensive rat. Circulation 91:161–170PubMedCrossRefGoogle Scholar
  3. 3.
    Ellims AH, Iles LM, Ling LH et al (2012) Diffuse myocardial fibrosis in hypertrophic cardiomyopathy can be identified by cardiovascular magnetic resonance, and is associated with left ventricular diastolic dysfunction. J Cardiovasc Magn Reson 14:76PubMedCentralPubMedCrossRefGoogle Scholar
  4. 4.
    Ng AC, Auger D, Delgado V et al (2012) Association between diffuse myocardial fibrosis by cardiac magnetic resonance contrast-enhanced T(1) mapping and subclinical myocardial dysfunction in diabetic patients: a pilot study. Circ Cardiovasc Imaging 5:51–59PubMedCrossRefGoogle Scholar
  5. 5.
    Schwarz F, Mall G, Zebe H et al (1983) Quantitative morphologic findings of the myocardium in idiopathic dilated cardiomyopathy. Am J Cardiol 51:501–506PubMedCrossRefGoogle Scholar
  6. 6.
    Wong TC, Piehler K, Meier CG et al (2012) Association between extracellular matrix expansion quantified by cardiovascular magnetic resonance and short-term mortality. Circulation 126:1206–1216PubMedCentralPubMedCrossRefGoogle Scholar
  7. 7.
    Babu-Narayan SV, Kilner PJ, Li W et al (2006) Ventricular fibrosis suggested by cardiovascular magnetic resonance in adults with repaired tetralogy of Fallot and its relationship to adverse markers of clinical outcome. Circulation 113:405–413PubMedCrossRefGoogle Scholar
  8. 8.
    Chowdhury UK, Sathia S, Ray R et al (2006) Histopathology of the right ventricular outflow tract and its relationship to clinical outcomes and arrhythmias in patients with tetralogy of Fallot. J Thorac Cardiovasc Surg 132:270–277PubMedCrossRefGoogle Scholar
  9. 9.
    Bull S, White SK, Piechnik SK et al (2013) Human non-contrast T1 values and correlation with histology in diffuse fibrosis. Heart 99:932–937PubMedCentralPubMedCrossRefGoogle Scholar
  10. 10.
    Flacke SJ, Fischer SE, Lorenz CH (2001) Measurement of the gadopentetate dimeglumine partition coefficient in human myocardium in vivo: normal distribution and elevation in acute and chronic infarction. Radiology 218:703–710PubMedCrossRefGoogle Scholar
  11. 11.
    Flett AS, Hayward MP, Ashworth MT et al (2010) Equilibrium contrast cardiovascular magnetic resonance for the measurement of diffuse myocardial fibrosis: preliminary validation in humans. Circulation 122:138–144PubMedCrossRefGoogle Scholar
  12. 12.
    Iles L, Pfluger H, Phrommintikul A et al (2008) Evaluation of diffuse myocardial fibrosis in heart failure with cardiac magnetic resonance contrast-enhanced T1 mapping. J Am Coll Cardiol 52:1574–1580PubMedCrossRefGoogle Scholar
  13. 13.
    Kellman P, Wilson JR, Xue H et al (2012) Extracellular volume fraction mapping in the myocardium, part 2: initial clinical experience. J Cardiovasc Magn Reson 14:64PubMedCentralPubMedCrossRefGoogle Scholar
  14. 14.
    Messroghli DR, Nordmeyer S, Dietrich T et al (2011) Assessment of diffuse myocardial fibrosis in rats using small-animal look-locker inversion recovery T1 mapping. Circ Cardiovasc Imaging 4:636–640PubMedCrossRefGoogle Scholar
  15. 15.
    Plymen CM, Sado DM, Taylor AM et al (2013) Diffuse myocardial fibrosis in the systemic right ventricle of patients late after Mustard or Senning surgery: an equilibrium contrast cardiovascular magnetic resonance study. Eur Heart J Cardiovasc Imaging 14:963–968PubMedCrossRefGoogle Scholar
  16. 16.
    Puntmann VO, Voigt T, Chen Z et al (2013) Native T1 mapping in differentiation of normal myocardium from diffuse disease in hypertrophic and dilated cardiomyopathy. JACC Cardiovasc Imaging 6:475–484PubMedCrossRefGoogle Scholar
  17. 17.
    Sibley CT, Noureldin RA, Gai N et al (2012) T1 mapping in cardiomyopathy at cardiac MR: comparison with endomyocardial biopsy. Radiology 265:724–732PubMedCentralPubMedCrossRefGoogle Scholar
  18. 18.
    Sparrow P, Messroghli DR, Reid S et al (2006) Myocardial T1 mapping for detection of left ventricular myocardial fibrosis in chronic aortic regurgitation: pilot study. AJR Am J Roentgenol 187:W630–W635PubMedCrossRefGoogle Scholar
  19. 19.
    Ugander M, Oki AJ, Hsu LY et al (2012) Extracellular volume imaging by magnetic resonance imaging provides insights into overt and sub-clinical myocardial pathology. Eur Heart J 33:1268–1278PubMedCentralPubMedCrossRefGoogle Scholar
  20. 20.
    White SK, Sado DM, Flett AS et al (2012) Characterizing the myocardial interstitial space: the clinical relevance of non-invasive imaging. Heart 98:773–779PubMedCrossRefGoogle Scholar
  21. 21.
    Marcus FI, McKenna WJ, Sherril D et al (2010) Diagnosis of arrhythmogenic right ventricular cardiomyopathy/dysplasia (ARVC/D). Circulation 121:1533–1541PubMedCentralPubMedCrossRefGoogle Scholar
  22. 22.
    Fernandes FP, Manlhiot C, Roche SL et al (2012) Impaired left ventricular myocardial mechanics and their relation to pulmonary regurgitation, right ventricular enlargement and exercise capacity in asymptomatic children after repair of tetralogy of Fallot. J Am Soc Echocardiogr 25:518–523CrossRefGoogle Scholar
  23. 23.
    Sun AM, AlHabshan F, Cheung M et al (2011) Delayed onset of tricuspid valve flow in repaired tetralogy of Fallot: an additional mechanism of diastolic dysfunction and interventricular dyssynchrony. J Cardiovasc Magn Reson 13:43PubMedCentralPubMedCrossRefGoogle Scholar
  24. 24.
    Kim WY, Danias PG, Stuber M et al (2001) Coronary magnetic resonance angiography for the detection of coronary stenosis. N Engl J Med 345:1863–1869PubMedCrossRefGoogle Scholar
  25. 25.
    Messroghli DR, Radjenovic A, Kozerke S et al (2004) Modified look-locker inversion recovery (MOLLI) for high-resolution T1 mapping of the heart. Magn Reson Med 52:141–146PubMedCrossRefGoogle Scholar
  26. 26.
    Oosterhof T, Mulder BJM, Vliegen HW et al (2005) Corrected tetralogy of Fallot: delayed enhancement in right ventricular outflow tract. Radiology 237:868–871PubMedCrossRefGoogle Scholar
  27. 27.
    Farah MC, Castro CRP, Moreira VM et al (2010) The impact of preexisting myocardial remodeling on ventricular function early after tetralogy of Fallot repair. J Am Soc Echocardiogr 23:912–918PubMedCrossRefGoogle Scholar
  28. 28.
    Wald RM, Haber I, Wald R et al (2009) Effects of regional dysfunction and late gadolinium enhancement on global right ventricular function and exercise capacity in patients with repaired tetralogy of Fallot. Circulation 119:1370–1377PubMedCentralPubMedCrossRefGoogle Scholar
  29. 29.
    Schwartz SM, Gordon D, Mosca RS et al (1996) Collagen content in normal, pressure, and pressure-volume overloaded developing human hearts. Am J Cardiol 77:734–738PubMedCrossRefGoogle Scholar
  30. 30.
    Farah MC, Castro CRP, Moreira VM et al (2009) The myocardium in tetralogy of Fallot: a histological and morphometric study. Arq Bras Cardiol 92:160–171PubMedCrossRefGoogle Scholar
  31. 31.
    Fontana M, White SK, Banypersad SM et al (2012) Comparison of T1 mapping techniques for ECV quantification. Histological validation and reproducibility of ShMOLLI versus multibreath-hold T1 quantification equilibrium contrast CMR. J Cardiovasc Magn Reson 14:88PubMedCentralPubMedCrossRefGoogle Scholar
  32. 32.
    Wang ZF, Wang NP, Harmouche S et al (2013) Postconditioning promotes the cardiac repair through balancing collagen degradation and synthesis after myocardial infarction in rats. Basic Res Cardiol 108:318PubMedCrossRefGoogle Scholar
  33. 33.
    Dass S, Suttie JJ, Piechnik SK et al (2012) Myocardial tissue characterization using magnetic resonance noncontrast T1 mapping in hypertrophic and dilated cardiomyopathy. Circ Cardiovasc Imaging 5:726–733PubMedCrossRefGoogle Scholar
  34. 34.
    Karamitsos TD, Piechnik SK, Banypersad SM et al (2013) Noncontrast T1 mapping for the diagnosis of cardiac amyloidosis. JACC Cardiovasc Imaging 6:488–497PubMedCrossRefGoogle Scholar
  35. 35.
    Puntmann VO, D’Cruz D, Smith Z et al (2013) Native myocardial T1 mapping by cardiovascular magnetic resonance imaging in subclinical cardiomyopathy in patients with systemic lupus erythematosus. Circ Cardiovasc Imaging 6:295–301PubMedCrossRefGoogle Scholar
  36. 36.
    Reddy S, Osorio JC, Duque AM et al (2006) Failure of right ventricular adaptation in children with tetralogy of Fallot. Circulation 114:I37–I42PubMedCrossRefGoogle Scholar
  37. 37.
    Jeewa A, Manickaraj AK, Mertens L et al (2012) Genetic determinants of right-ventricular remodeling after tetralogy of Fallot repair. Pediatr Res 72:407–413PubMedCrossRefGoogle Scholar
  38. 38.
    Friedberg MK, Fernandes FP, Roche SL et al (2012) Impaired right and left ventricular diastolic myocardial mechanics and filling in asymptomatic children and adolescents after repair of tetralogy of fallot. Eur Heart J Cardiovasc Imaging 13:905–913PubMedCrossRefGoogle Scholar
  39. 39.
    Ortega M, Triedman JK, Geva T et al (2011) Relation of left ventricular dyssynchrony measured by cardiac magnetic resonance tissue tracking in repaired tetralogy of Fallot to ventricular tachycardia and death. Am J Cardiol 107:1535–1540PubMedCrossRefGoogle Scholar
  40. 40.
    Tzemos N, Harris L, Carasso S et al (2009) Adverse left ventricular mechanics in adults with repaired tetralogy of fallot. Am J Cardiol 103:420–425PubMedCrossRefGoogle Scholar
  41. 41.
    Redington AN (2006) Physiopathology of right ventricular failure. Semin Thorac Cardiovasc Surg Pediatr Card Surg Ann 2006:3–10CrossRefGoogle Scholar
  42. 42.
    Apitz C, Honjo O, Humpl T et al (2012) Biventricular structural and functional responses to aortic constriction in a rabbit model of chronic right ventricular pressure overload. J Thorac Cardiovasc Surg 144:1494–1501PubMedCrossRefGoogle Scholar
  43. 43.
    Anderson RH, Ho SH, Redmann K et al (2005) The anatomical arrangement of the myocardial cells making up the ventricular mass. Eur J Cardiothorac Surg 28:517–525PubMedCrossRefGoogle Scholar
  44. 44.
    Ho SH, Jackson M, Kilpatrick L et al (1996) Fibrous matrix of ventricular myocardium in tricuspid atresia compared with normal heart. Circulation 94:1642–1646PubMedCrossRefGoogle Scholar
  45. 45.
    Kawel N, Nacif M, Zavodni A et al (2012) T1 mapping of the myocardium: intra-individual assessment of the effect of field strength, cardiac cycle and variation by myocardial region. J Cardiovasc Magn Reson 14:27PubMedCentralPubMedCrossRefGoogle Scholar
  46. 46.
    Miller CA, Naish JH, Bishop P et al (2013) Comprehensive validation of cardiovascular magnetic resonance techniques for the assessment of myocardial extracellular volume. Circulation 6:373–383PubMedGoogle Scholar
  47. 47.
    Park SJ, On YK, Kim JS et al (2012) Relation of fragmented QRS complex to right ventricular fibrosis detected by late gadolinium enhancement cardiac magnetic resonance in adults with repaired tetralogy of Fallot. Am J Cardiol 109:110–115PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Marcelo F. Kozak
    • 1
  • Andrew Redington
    • 2
  • Shi-Joon Yoo
    • 1
  • Mike Seed
    • 1
  • Andreas Greiser
    • 3
  • Lars Grosse-Wortmann
    • 1
    Email author
  1. 1.Labatt Family Heart Centre in the Department of Paediatrics and Department of Diagnostic ImagingThe Hospital for Sick Children, University of TorontoTorontoCanada
  2. 2.Labatt Family Heart Centre in the Department of PaediatricsThe Hospital for Sick Children, University of TorontoTorontoCanada
  3. 3.Siemens AG Healthcare SectorErlangenGermany

Personalised recommendations