Impact of age and cardiac disease on regional left and right ventricular myocardial motion in healthy controls and patients with repaired tetralogy of fallot

  • Alexander RuhEmail author
  • Roberto Sarnari
  • Haben Berhane
  • Kenny Sidoryk
  • Kai Lin
  • Ryan Dolan
  • Arleen Li
  • Michael J. Rose
  • Joshua D. Robinson
  • James C. Carr
  • Cynthia K. Rigsby
  • Michael Markl
Original Paper


The assessment of both left (LV) and right ventricular (RV) motion is important to understand the impact of heart disease on cardiac function. The MRI technique of tissue phase mapping (TPM) allows for the quantification of regional biventricular three-directional myocardial velocities. The goal of this study was to establish normal LV and RV velocity parameters across a wide range of pediatric to adult ages and to investigate the feasibility of TPM for detecting impaired regional biventricular function in patients with repaired tetralogy of Fallot (TOF). Thirty-six healthy controls (age = 1–75 years) and 12 TOF patients (age = 5–23 years) underwent cardiac MRI including TPM in short-axis locations (base, mid, apex). For ten adults, a second TPM scan was used to assess test–retest reproducibility. Data analysis included the calculation of biventricular radial, circumferential, and long-axis velocity components, quantification of systolic and diastolic peak velocities in an extended 16 + 10 LV + RV segment model, and assessment of inter-ventricular dyssynchrony. Biventricular velocities showed good test–retest reproducibility (mean bias ≤ 0.23 cm/s). Diastolic radial and long-axis peak velocities for LV and RV were significantly reduced in adults compared to children (19–61%, p < 0.001–0.02). In TOF patients, TPM identified significantly reduced systolic and diastolic LV and RV long-axis peak velocities (20–50%, p < 0.001–0.05) compared to age-matched controls. In conclusion, tissue phase mapping enables comprehensive analysis of global and regional biventricular myocardial motion. Changes in myocardial velocities associated with age underline the importance of age-matched controls. This pilot study in TOF patients shows the feasibility to detect regionally abnormal LV and RV motion.


Cardiovascular magnetic resonance Tissue phase mapping Biventricular myocardial velocities Inter-ventricular dyssynchrony Repaired tetralogy of Fallot Children 



National Institute of Heart, Lung and Blood Disorders (NHLBI), R01 HL 117888.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This study was approved by the institutional review boards (IRB) at Northwestern University and Ann & Robert H. Lurie Children’s Hospital of Chicago.

Informed consent

All adults provided written informed consent for the MRI exam. For the children, written informed consent was obtained to add the TPM sequence to a clinically indicated MRI exam.


  1. 1.
    Apostolakis S, Konstantinides S (2012) The right ventricle in health and disease: insights into physiology, pathophysiology and diagnostic management. Cardiology 121:263–273Google Scholar
  2. 2.
    Pavlicek M, Wahl A, Rutz T, de Marchi SF, Hille R, Wustmann K et al (2011) Right ventricular systolic function assessment: rank of echocardiographic methods vs. cardiac magnetic resonance imaging. Eur J Echocardiogr 12:871–880Google Scholar
  3. 3.
    Mertens LL, Friedberg MK (2010) Imaging the right ventricle—current state of the art. Nat Rev Cardiol 7:551–563Google Scholar
  4. 4.
    Galea N, Carbone I, Cannata D, Cannavale G, Conti B, Galea R et al (2013) Right ventricular cardiovascular magnetic resonance imaging: normal anatomy and spectrum of pathological findings. Insights Imaging 4:213–223Google Scholar
  5. 5.
    Fayad ZA, Ferrari VA, Kraitchman DL, Young AA, Palevsky HI, Bloomgarden DC et al (1998) Right ventricular regional function using mr tagging: normals versus chronic pulmonary hypertension. Magn Reson Med 39:116–123Google Scholar
  6. 6.
    Kayser HW, van der Geest RJ, van der Wall EE, Duchateau C, de Roos A (2000) Right Ventricular function in patients after acute myocardial infarction assessed with phase contrast MR velocity mapping encoded in three directions. J Magn Reson Imaging 11:471–475Google Scholar
  7. 7.
    Auger DA, Zhong X, Epstein FH, Spottiswoode BS (2012) Mapping right ventricular myocardial mechanics using 3D cine DENSE cardiovascular magnetic resonance. J Cardiovasc Magn Reson 14:4Google Scholar
  8. 8.
    Kempny A, Fernández-Jiménez R, Orwat S, Schuler P, Bunck AC, Maintz D et al (2012) Quantification of biventricular myocardial function using cardiac magnetic resonance feature tracking, endocardial border delineation and echocardiographic speckle tracking in patients with repaired tetralogy of fallot and healthy controls. J Cardiovasc Magn Reson 14:32Google Scholar
  9. 9.
    Moon TJ, Choueiter N, Geva T, Valente AM, Gauvreau K, Harrild DM (2015) Relation of biventricular strain and dyssynchrony in repaired tetralogy of fallot measured by cardiac magnetic resonance to death and sustained ventricular tachycardia. Am J Cardiol 115:676–680Google Scholar
  10. 10.
    Nagao M, Yamasaki Y, Yonezawa M, Matsuo Y, Kamitani T, Yamamura K et al (2015) Interventricular dyssynchrony using tagging magnetic resonance imaging predicts right ventricular dysfunction in adult congenital heart disease. Congenit Heart Dis 10:271–280Google Scholar
  11. 11.
    Hoffman JIE, Kaplan S (2002) The incidence of congenital heart disease. J Am Coll Cardiol 39:1890–1900Google Scholar
  12. 12.
    Al Habib HF, Jacobs JP, Mavroudis C, Tchervenkov CI, O’Brien SM, Mohammadi S et al (2010) Contemporary patterns of management of tetralogy of fallot: data from the society of thoracic surgeons database. Ann Thorac Surg 90:813–819Google Scholar
  13. 13.
    Helbing WA, de Roos A (2000) Clinical applications of cardiac magnetic resonance imaging after repair of tetralogy of Fallot. Pediatr Cardiol 21:70–79Google Scholar
  14. 14.
    Geva T (2011) Repaired tetralogy of Fallot: the roles of cardiovascular magnetic resonance in evaluating pathophysiology and for pulmonary valve replacement decision support. J Cardiovasc Magn Reson 13:9Google Scholar
  15. 15.
    Bonello B, Kilner PJ (2012) Review of the role of cardiovascular magnetic resonance in congenital heart disease, with a focus on right ventricle assessment. Arch Cardiovasc Dis 105:605–613Google Scholar
  16. 16.
    Valente AM, Cook S, Festa P, Ko HH, Krishnamurthy R, Taylor AM et al (2014) Multimodality Imaging Guidelines for patients with repaired tetralogy of Fallot: a report from the American Society of Echocardiography—Developed in Collaboration with the Society for Cardiovascular Magnetic Resonance and the Society for Pediatric Radiol. J Am Soc Echocardiogr 27:111–141Google Scholar
  17. 17.
    Davlouros PA, Kilner PJ, Hornung TS, Li W, Francis JM, Moon JCC et al (2002) Right ventricular function in adults with repaired tetralogy of Fallot assessed with cardiovascular magnetic resonance imaging: detrimental role of right ventricular outflow aneurysms or akinesia and adverse right-to-left ventricular interaction. J Am Coll Cardiol 40:2044–2052Google Scholar
  18. 18.
    Oosterhof T, Tulevski II, Vliegen HW, Spijkerboer AM, Mulder BJM (2006) Effects of volume and/or pressure overload secondary to congenital heart disease (tetralogy of fallot or pulmonary stenosis) on right ventricular function using cardiovascular magnetic resonance and B-type natriuretic peptide levels. Am J Cardiol 97:1051–1055Google Scholar
  19. 19.
    Yoo BW, Kim JO, Kim YJ, Choi JY, Park HK, Park YH et al (2012) Impact of pressure load caused by right ventricular outflow tract obstruction on right ventricular volume overload in patients with repaired tetralogy of Fallot. J Thorac Cardiovasc Surg 143:1299–1304Google Scholar
  20. 20.
    Khalaf A, Tani D, Tadros S, Madan S (2013) Right- and left-ventricular strain evaluation in repaired pediatric tetralogy of fallot patients using magnetic resonance tagging. Pediatr Cardiol 34:1206–1211Google Scholar
  21. 21.
    Jing L, Haggerty CM, Suever JD, Alhadad S, Prakash A, Cecchin F et al (2014) Patients with repaired tetralogy of Fallot suffer from intra-and inter-ventricular cardiac dyssynchrony: a cardiacmagnetic resonance study. Eur Heart J Cardiovasc Imaging 15:1333–1343Google Scholar
  22. 22.
    Jing L, Wehner GJ, Suever JD, Charnigo RJ, Alhadad S, Stearns E et al (2016) Left and right ventricular dyssynchrony and strains from cardiovascular magnetic resonance feature tracking do not predict deterioration of ventricular function in patients with repaired tetralogy of Fallot. J Cardiovasc Magn Reson 18:49Google Scholar
  23. 23.
    Orwat S, Diller G-P, Kempny A, Radke R, Peters B, Kühne T et al (2016) Myocardial deformation parameters predict outcome in patients with repaired tetralogy of Fallot. Heart 102:209–215Google Scholar
  24. 24.
    Hennig J, Schneider B, Peschl S, Markl M, Laubenberger TKJ (1998) Analysis of myocardial motion based on velocity measurements with a black blood prepared segmented gradient-echo sequence: methodology and applications to normal volunteers and patients. J Magn Reson Imaging 8:868–877Google Scholar
  25. 25.
    Jung B, Föll D, Böttler P, Petersen S, Hennig J, Markl M (2006) Detailed analysis of myocardial motion in volunteers and patients using high-temporal-resolution MR tissue phase mapping. J Magn Reson Imaging 24:1033–1039Google Scholar
  26. 26.
    Petersen SE, Jung BA, Wiesmann F, Selvanayagam JB, Francis JM, Hennig J et al (2006) Myocardial tissue phase mapping with cine phase-contrast MR imaging: regional wall motion analysis in healthy volunteers. Radiology 238:816–826Google Scholar
  27. 27.
    Föll D, Jung B, Staehle F, Schilli E, Bode C, Hennig J et al (2009) Visualization of multidirectional regional left ventricular dynamics by high-temporal-resolution tissue phase mapping. J Magn Reson Imaging 29:1043–1052Google Scholar
  28. 28.
    Föll D, Jung B, Schilli E, Staehle F, Geibel A, Hennig J et al (2010) Magnetic resonance tissue phase mapping of myocardial motion: new insight in age and gender. Circ Cardiovasc Imaging 3:54–64Google Scholar
  29. 29.
    Föll D, Jung B, Germann E, Staehle F, Bode C, Markl M (2013) Hypertensive heart disease: MR tissue phase mapping reveals altered left ventricular rotation and regional myocardial long-axis velocities. Eur Radiol 23:339–347Google Scholar
  30. 30.
    Markl M, Rustogi R, Galizia M, Goyal A, Collins J, Usman A et al (2013) Myocardial T2-mapping and velocity mapping: changes in regional left ventricular structure and function after heart transplantation. Magn Reson Med 70:517–526Google Scholar
  31. 31.
    Simpson R, Keegan J, Gatehouse P, Hansen M, Firmin D (2014) Spiral tissue phase velocity mapping in a breath-hold with non-Cartesian sense. Magn Reson Med 72:659–668Google Scholar
  32. 32.
    Codreanu I, Pegg TJ, Selvanayagam JB, Robson MD, Rider OJ, Dasanu CA et al (2014) Normal values of regional and global myocardial wall motion in young and elderly individuals using navigator gated tissue phase mapping. Age 36:231–241Google Scholar
  33. 33.
    Collins J, Sommerville C, Magrath P, Spottiswoode B, Freed BH, Benzuly KH et al (2015) Extracellular volume fraction is more closely associated with altered regional left ventricular velocities than left ventricular ejection fraction in nonischemic cardiomyopathy. Circ Cardiovasc Imaging 8:e001998Google Scholar
  34. 34.
    Knight DS, Steeden JA, Moledina S, Jones A, Coghlan JG, Muthurangu V (2015) Left ventricular diastolic dysfunction in pulmonary hypertension predicts functional capacity and clinical worsening: A tissue phase mapping study. J Cardiovasc Magn Reson 17:116Google Scholar
  35. 35.
    Lin K, Chowdhary V, Benzuly KH, Yancy CW, Lomasney JW, Rigolin VH et al (2016) Reproducibility and observer variability of tissue phase mapping for the quantification of regional myocardial velocities. Int J Cardiovasc Imaging 32:1227–1234Google Scholar
  36. 36.
    von Knobelsdorff-Brenkenhoff F, Hennig P, Menza M, Dieringer MA, Föll D, Jung B et al (2016) Myocardial dysfunction in patients with aortic stenosis and hypertensive heart disease assessed by MR tissue phase mapping. J Magn Reson Imaging 44:168–177Google Scholar
  37. 37.
    Paul J, Wundrak S, Bernhardt P, Rottbauer W, Neumann H, Rasche V (2016) Self-gated tissue phase mapping using golden angle radial sparse SENSE. Magn Reson Med 75:789–800Google Scholar
  38. 38.
    Gimpel C, Jung BA, Jung S, Brado J, Schwendinger D, Burkhardt B et al (2017) Magnetic resonance tissue phase mapping demonstrates altered left ventricular diastolic function in children with chronic kidney disease. Pediatr Radiol 47:169–177Google Scholar
  39. 39.
    Brado J, Dechant MJ, Menza M, Komancsek A, Lang CN, Bugger H et al (2017) Phase-contrast magnet resonance imaging reveals regional, transmural, and base-to-apex dispersion of mechanical dysfunction in patients with long QT syndrome. Heart Rhythm 14:1388–1397Google Scholar
  40. 40.
    Chang M-C, Wu M-T, Weng K-P, Su M-Y, Menza M, Huang H-C et al (2018) Left ventricular regional myocardial motion and twist function in repaired tetralogy of Fallot evaluated by magnetic resonance tissue phase mapping. Eur Radiol 28:104–114Google Scholar
  41. 41.
    Dolan RS, Rahsepar AA, Blaisdell J, Lin K, Suwa K, Ghafourian K et al (2018) Cardiac structure-function MRI in patients after heart transplantation. J Magn Reson Imaging. Google Scholar
  42. 42.
    Menza M, Föll D, Hennig J, Jung B (2018) Segmental biventricular analysis of myocardial function using high temporal and spatial resolution tissue phase mapping. Magn Reson Mater Phy 31:61–73Google Scholar
  43. 43.
    Steeden JA, Knight DS, Bali S, Atkinson D, Taylor AM, Muthurangu V (2014) Self-navigated tissue phase mapping using a golden-angle spiral acquisition—proof of concept in patients with pulmonary hypertension. Magn Reson Med 71:145–155Google Scholar
  44. 44.
    Jung B, Ullmann P, Honal M, Bauer S, Hennig J, Markl M (2008) Parallel MRI With extended and averaged GRAPPA Kernels (PEAK-GRAPPA): optimized spatiotemporal dynamic imaging. J Magn Reson Imaging 28:1226–1232Google Scholar
  45. 45.
    Bauer S, Markl M, Föll D, Russe M, Stankovic Z, Jung B (2013) K–t GRAPPA accelerated phase contrast mri: improved assessment of blood flow and 3-directional myocardial motion during breath-hold. J Magn Reson Imaging 38:1054–1062Google Scholar
  46. 46.
    Cerqueira MD, Weissman NJ, Dilsizian V, Jacobs AK, Kaul S, Laskey WK et al (2002) Standardized myocardial segmentation and nomenclature for tomographic imaging of the heart: a statement for healthcare professionals from the Cardiac Imaging Committee of the Council on Clinical Cardiology of the American Heart Association. Circulation 105:539–542Google Scholar
  47. 47.
    Walker PG, Cranney GB, Scheidegger MB, Waseleski G, Pohost GM, Yoganathan AP (1993) Semiautomated method for noise reduction and background phase error correction in MR phase velocity data. J Magn Reson Imaging 3:521–530Google Scholar
  48. 48.
    Donekal S, Ambale-Venkatesh B, Berkowitz S, Wu CO, Choi EY, Fernandes V et al (2013) Inter-study reproducibility of cardiovascular magnetic resonance tagging. J Cardiovasc Magn Reson 15:37Google Scholar
  49. 49.
    Maceira AM, Tuset-Sanchis L, López-Garrido M, San Andres M, López-Lereu MP, Monmeneu JV et al (2018) Feasibility and reproducibility of feature-tracking-based strain and strain rate measures of the left ventricle in different diseases and genders. J Magn Reson Imaging 47:1415–1425Google Scholar
  50. 50.
    Lin K, Meng L, Collins JD, Chowdhary V, Markl M, Carr JC (2017) Reproducibility of cine displacement encoding with stimulated echoes (DENSE) in human subjects. Magn Reson Imaging 35:148–153Google Scholar
  51. 51.
    Kawel-Boehm N, Maceira A, Valsangiacomo-Buechel ER, Vogel-Claussen J, Turkbey EB, Williams R et al (2015) Normal values for cardiovascular magnetic resonance in adults and children. J Cardiovasc Magn Reson 17:29Google Scholar
  52. 52.
    Dallaire F, Slorach C, Hui W, Sarkola T, Friedberg MK, Bradley TJ et al (2015) Reference values for pulse wave Doppler and tissue Doppler imaging in pediatric echocardiography. Circ Cardiovasc Imaging 8:e002167Google Scholar
  53. 53.
    Friedberg MK, Fernandes FP, Roche SL, Grosse-Wortmann L, Manlhiot C, Fackoury C 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 13:905–913Google Scholar
  54. 54.
    Friedberg MK, Fernandes FP, Roche SL, Slorach C, Grosse-Wortmann L, Manlhiot C et al (2013) Relation of right ventricular mechanics to exercise tolerance in children after tetralogy of Fallot repair. Am Heart J 165:551–557Google Scholar
  55. 55.
    Dragulescu A, Friedberg MK, Grosse-Wortmann L, Redington A, Mertens L (2014) Effect of chronic right ventricular volume overload on ventricular interaction in patients after tetralogy of Fallot repair. J Am Soc Echocardiogr 27:896–902Google Scholar
  56. 56.
    Chitiboi T, Hennemuth A, Schnell S, Chowdhary V, Honarmand A, Markl M et al (2016) Contour tracking and probabilistic segmentation of tissue phase mapping MRI. Proc SPIE 9784:978404Google Scholar
  57. 57.
    Espe EKS, Skårdal K, Aronsen JM, Zhang L, Sjaastad I (2017) A semiautomatic method for rapid segmentation of velocity-encoded myocardial magnetic resonance imaging data. Magn Reson Med 78:1199–1207Google Scholar
  58. 58.
    Suever JD, Fornwalt BK, Neuman LR, Delfino JG, Lloyd MS, Oshinski JN (2014) Method to create regional mechanical dyssynchrony maps from short-axis cine steady-state free-precession images. J Magn Reson Imaging 39:958–965Google Scholar
  59. 59.
    Simpson RM, Keegan J, Firmin DN (2013) MR assessment of regional myocardial mechanics. J Magn Reson Imaging 37:576–599Google Scholar
  60. 60.
    Jung B, Schneider B, Markl M, Saurbier B, Geibel A, Hennig J (2004) Measurement of left ventricular velocities: phase contrast MRI velocity mapping versus tissue-Doppler-ultrasound in healthy volunteers. J Cardiovasc Magn Reson 6:777–783Google Scholar
  61. 61.
    Geyer H, Caracciolo G, Abe H, Wilansky S, Carerj S, Gentile F et al (2010) Assessment of myocardial mechanics using speckle tracking echocardiography: fundamentals and clinical applications. J Am Soc Echocardiogr 23:351–369Google Scholar
  62. 62.
    Schuster A, Hor KN, Kowallick JT, Beerbaum P, Kutty S (2016) Cardiovascular magnetic resonance myocardial feature tracking: concepts and clinical applications. Circ Cardiovasc Imaging 9:e004077Google Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Alexander Ruh
    • 1
    Email author
  • Roberto Sarnari
    • 1
  • Haben Berhane
    • 2
  • Kenny Sidoryk
    • 1
  • Kai Lin
    • 1
  • Ryan Dolan
    • 1
  • Arleen Li
    • 3
  • Michael J. Rose
    • 2
  • Joshua D. Robinson
    • 1
    • 4
    • 5
  • James C. Carr
    • 1
  • Cynthia K. Rigsby
    • 1
    • 2
    • 5
  • Michael Markl
    • 1
    • 6
  1. 1.Department of Radiology, Feinberg School of MedicineNorthwestern UniversityChicagoUSA
  2. 2.Department of Medical ImagingAnn & Robert H. Lurie Children’s Hospital of ChicagoChicagoUSA
  3. 3.Feinberg School of MedicineNorthwestern UniversityChicagoUSA
  4. 4.Division of Pediatric Cardiology, Department of PediatricsAnn & Robert H. Lurie Children’s Hospital of ChicagoChicagoUSA
  5. 5.Department of Pediatrics, Feinberg School of MedicineNorthwestern UniversityChicagoUSA
  6. 6.Department of Biomedical Engineering, McCormick School of EngineeringNorthwestern UniversityEvanstonUSA

Personalised recommendations