Skip to main content

Magnetic Resonance Imaging for Aortic Function Evaluation in Thoracic Aortic Aneurysms

Abstract

Thoracic aortic aneurysm is a common cardiovascular disease consisting of marked dilation of the aorta. Aortic aneurysms carry a high risk of life-threatening complications such as aortic dissection or rupture. Classically, maximum aortic diameter has been used as the sole descriptor of aneurysm severity and is considered the main predictor of complications. However, maximum aortic diameter measurement is often poorly reproducible and about 60% of type A and 80% of type B aortic dissections occurred in patients with an aortic diameter inferior to that recommended for the indication of elective surgical treatment. Therefore, new biomarkers for risk stratification in thoracic aortic aneurysm are needed. Cardiovascular magnetic resonance (CMR) imaging is a non-invasive imaging technique widely used for diagnosis, clinical follow-up and research in thoracic aortic aneurysms. CMR applications to thoracic aortic aneurysms are generally based on either cine CMR images, which are time-resolved images providing dynamic structural visualization, or phase-contrast images, which utilise a flow-encoding gradient to assess time-resolved velocity data. Particularly with 3D velocity encoding (4D flow MRI), phase-contrast imaging permits detailed study of haemodynamic in thoracic aortic aneurysms while cine CMR is often used to assess aortic geometry and its changes through the cardiac cycle or during follow-up. The possibilities offered by CMR for studying thoracic aortic aneurysms and a description of their applications in Bicuspid Aortic Valve (BAV) and Marfan patients are here reviewed.

References

  1. Elefteriades JA, Farkas EA. Thoracic aortic aneurysm: clinically pertinent controversies and uncertainties. J Am Coll Cardiol 2010;55:841–57.

    Google Scholar 

  2. Erbel RA, Aboyans V, Boileau C, Bossone E, Bartolomeo RD, Eggebrecht H, et al. 2014 ESC guidelines on the diagnosis and treatment of aortic diseases: document covering acute and chronic aortic diseases of the thoracic and abdominal aorta of the adult. The Task Force for the Diagnosis and Treatment of Aortic Diseases of the European Society of Cardiology (ESC). Eur Heart J 2014;35:2873–9126.

    Google Scholar 

  3. Vis JC, RodrĂ­guez-Palomares JF, TeixidĂ³-Tura G, Galian-Gay L, Granato C, Guala A, et al. Implications of asymmetry and valvular morphotype on echocardiographic measurements of the aortic root in bicuspid aortic valve. J Am Soc Echocardiogr 2019; 32:105–12.

  4. RodrĂ­guez-Palomares JF, TeixidĂ³-Tura G, Galuppo V, CuĂ©llar H, Laynez A, et al. Multimodality assessment of ascending aortic diameters: comparison of different measurement methods. J Am Soc Echocardiogr 2016;29:819–26.e4.

    Google Scholar 

  5. Pape LA, Tsai TT, Isselbacher EM, Oh JK, O’gara PT, Evangelista A, et al. Aortic diameter 5.5 cm is not a good predictor of type A aortic dissection: observations from the International Registry of Acute Aortic Dissection (IRAD). Circulation 2007;116:1120–27.

    Google Scholar 

  6. Trimarchi S, Jonker FHW, Hutchison S, Isselbacher EM, Pape LA, Patel HJ, et al. Descending aortic diameter of 5.5 cm or greater is not an accurate predictor of acute type B aortic dissection. J Thorac Cardiovasc Surg 2011;142:e101–e7.

    Google Scholar 

  7. Nichols WW, O’Rourke MF, Vlachopoulos C. McDonald’s Blood Flow in Arteries: Theoretical, Experimental and Clinical Principles. 6th ed., London, UK: Hodder Arnold; 2011.

  8. Dogui A, Kachenoura N, Frouin F, Lefort M, De Cesare A, Mousseaux E, et al. Consistency of aortic distensibility and pulse wave velocity estimates with respect to the Bramwell-Hill theoretical model: a cardiovascular magnetic resonance study. J Cardiovasc Magn Reson 2011;13:11.

    Google Scholar 

  9. Guala A, TeixidĂ³-Tura G, RodrĂ­guez-Palomares JF, Ruiz-Muñoz A, Dux-Santoy L, Villalva N, et al. Proximal aorta longitudinal strain predicts aortic root dilation rate and aortic events in Marfan syndrome. Eur Heart J 2019;40:2047–55.

    Google Scholar 

  10. Dyverfeldt P, Bissell MM, Barker AJ, Bolger AF, Carlhäll CJ, Ebbers T, et al. 4D flow cardiovascular magnetic resonance consensus statement. J Cardiovasc Magn Reson 2015;17:72.

    Google Scholar 

  11. Ebel S, HĂ¼bner L, Köhler B, Kropf S, Preim B, Jung B, et al. Validation of two accelerated 4D flow MRI sequences at 3 T: a phantom study. Eur Radiol Exp 2019;3:10.

    Google Scholar 

  12. RodrĂ­guez-Palomares JF, Dux-Santoy L, Guala A, Kale R, Maldonado G, TeixidĂ³-TurĂ  G, et al. Aortic flow patterns and wall shear stress maps by 4D-flow cardiovascular magnetic resonance in the assessment of aortic dilatation in bicuspid aortic valve disease. J Cardiovasc Magn Reson 2018;20:28.

    Google Scholar 

  13. Dux-Santoy L, Guala A, TeixidĂ³-TurĂ  G, Ruiz-Muñoz A, Maldonado G, Villalva N, et al. Increased rotational flow in the proximal aortic arch is associated with its dilation in bicuspid aortic valve disease. Eur Hear J Cardiovasc Imaging 2019;20:1407–17.

    Google Scholar 

  14. Mahadevia R, Barker AJ, Schnell S, Entezari P, Kansal P, Fedak PW, et al. Bicuspid aortic cusp fusion morphology alters aortic three-dimensional outflow patterns, wall shear stress, and expression of aortopathy. Circulation 2014;129:673–82.

    Google Scholar 

  15. Sigovan M, Hope MD, Dyverfeldt P, Saloner D. Comparison of four-dimensional flow parameters for quantification of flow eccentricity in the ascending aorta. J Magn Reson Imaging 2011;34:1226–30.

    Google Scholar 

  16. Bissell MM, Hess AT, Biasiolli L, Glaze SJ, Loudon M, Pitcher A, et al. Aortic dilation in bicuspid aortic valve disease: flow pattern is a major contributor and differs with valve fusion type. Circ Cardiovasc Imaging 2013;6:499–507.

    Google Scholar 

  17. Ha H, Kim GB, Kweon J, Lee SJ, Kim YH, Kim N, et al. The influence of the aortic valve angle on the hemodynamic features of the thoracic aorta. Sci Rep 2016;6:32316.

    Google Scholar 

  18. Bieging ET, Frydrychowicz A, Wentland AL, Landgraf BR, Johnson KM, Wieben O, et al. In vivo three-dimensional MR wall shear stress estimation in ascending aortic dilatation. J Magn Reson Imaging 2011;33:589–97.

    Google Scholar 

  19. Guala A, Dux-Santoy L, Teixido-Tura G, Johnson KM, Evangelista A, Rodríguez-Palomares J. Raphe in bicuspid aortic valve without significant aortic valve disease is unrelated to aortic hemodynamics and stiffness. Rev Española Cardiol (Engl Ed) 2020;73:89–90.

    Google Scholar 

  20. Morbiducci U, Ponzini R, Rizzo G, Cadioli M, Esposito A, De Cobelli F, et al. In vivo quantification of helical blood flow in human aorta by time-Resolved three-dimensional cine phase contrast magnetic resonance imaging. Ann Biomed Eng 2009;37:516–31.

    Google Scholar 

  21. Guzzardi DG, Barker AJ, van Ooij P, Malaisrie SC, Puthumana JJ, Belke DD, et al. Valve-related hemodynamics mediate human bicuspid aortopathy: insights from wall shear stress mapping. J Am Coll Cardiol 2015;66:892–900.

    Google Scholar 

  22. Bollache E, Guzzardi DG, Sattari S, Olsen KE, Di Martino ES, Malaisrie SC, et al. Aortic valve-mediated wall shear stress is heterogeneous and predicts regional aortic elastic fiber thinning in bicuspid aortic valve-associated aortopathy. J Thorac Cardiovasc Surg 2018;156:2112–20.e2.

    Google Scholar 

  23. Resnick N, Yahav H, Shay-Salit A, Shushy M, Schubert S, Zilberman LCM, et al. Fluid shear stress and the vascular endothelium: for better and for worse. Prog Biophys Mol Biol 2003;81:177–99.

    Google Scholar 

  24. Stalder AF, Russe MF, Frydrychowicz A, Bock J, Hennig J, Markl M. Quantitative 2D and 3D phase contrast MRI: Optimized analysis of blood flow and vessel wall parameters. Magn Reson Med 2008;60:1218–31.

    Google Scholar 

  25. Sotelo J, Dux-Santoy L, Guala A, Rodríguez-Palomares J, Evangelista A, Sing-Long C, et al. 3D axial and circumferential wall shear stress from 4D flow MRI data using a finite element method and a laplacian approach. Magn Reson Med 2018;79:2816–23.

    Google Scholar 

  26. Wentland AL, Wieben O, François CJ, Boncyk C, Munoz Del Rio A, Johnson KM, et al. Aortic pulse wave velocity measurements with undersampled 4D flow-sensitive MRI: comparison to 2D and algorithm determination. J Magn Reson Imaging 2013;37:853–9.

    Google Scholar 

  27. Guala A, Rodríguez-Palomares J, Dux-Santoy L, Teixido-Tura G, Maldonado G, Galian L, et al. Influence of aortic dilation on the regional aortic stiffness of bicuspid aortic valve assessed by 4- dimensional flow cardiac magnetic resonance: comparison With Marfan syndrome and degenerative aortic aneurysm. JACC Cardiovasc Imaging 2019;12:1020–9.

    Google Scholar 

  28. Bargiotas I, Mousseaux E, Yu WC, Venkatesh BA, Bollache E, de Cesare A, et al. Estimation of aortic pulse wave transit time in cardiovascular magnetic resonance using complex wavelet cross-spectrum analysis. J Cardiovasc Magn Reson 2015;17:65.

    Google Scholar 

  29. Verma S, Siu SC. Aortic dilatation in patients with bicuspid aortic valve. N Engl J Med 2014;370:1920–9.

    Google Scholar 

  30. Ward C. Clinical significance of the bicuspid aortic valve. Heart 2000;83:81–5.

    Google Scholar 

  31. Sievers HH, Schmidtke C. A classification system for the bicuspid aortic valve from 304 surgical specimens. J Thorac Cardiovasc Surg 2007;133:1226–33.

    Google Scholar 

  32. Nistri S, Sorbo MD, Marin M, Palisi M, Scognamiglio R, Thiene G. Aortic root dilatation in young men with normally functioning bicuspid aortic valves. Heart 1999;82:19–22.

    Google Scholar 

  33. Carro A, TeixidĂ³-Tura G, Evangelista A. Aortic dilatation in bicuspid aortic valve disease. Rev Esp Cardiol (Engl Ed) 2012;65: 977–81.

    Google Scholar 

  34. Hope MD, Hope TA, Meadows AK, Ordovas KG, Urbania TH, Alley MT, et al. Bicuspid aortic valve: four-dimensional MR evaluation of ascending aortic systolic flow patterns. Radiology 2010;255:53–61.

    Google Scholar 

  35. Nataatmadja M, West M, West J, Summers K, Walker P, Nagata M, et al. Abnormal extracellular matrix protein transport associated with increased apoptosis of vascular smooth muscle cells in Marfan syndrome and bicuspid aortic valve thoracic aortic aneurysm. Circulation 2003;108:II329–II34.

    Google Scholar 

  36. Fedak PW, de Sa MP, Verma S, Nili N, Kazemian P, Butany J, et al. Vascular matrix remodeling in patients with bicuspid aortic valve malformations: implications for aortic dilatation. J Thorac Cardiovasc Surg 2003;126:797–806.

    Google Scholar 

  37. Biner S, Rafique AM, Ray I, Cuk O, Siegel RJ, Tolstrup K. Aortopathy is prevalent in relatives of bicuspid aortic valve patients. J Am Coll Cardiol 2009;53:2288–95.

    Google Scholar 

  38. Loscalzo ML, Goh DLM, Loeys B, Kent KC, Spevak PJ, Dietz HC. Familial thoracic aortic dilation and bicommissural aortic valve: a prospective analysis of natural history and inheritance. Am J Med Genet A 2007;143A:1960–7.

  39. Andrus BW, O’Rourke DJ, Dacey LJ, Palac RT. Stability of ascending aortic dilatation following aortic valve replacement. Circulation 2003;108:II-295–II-9.

    Google Scholar 

  40. Nistri S, Grande-Allen J, Noale M, Basso C, Siviero P, Maggi S, et al. Aortic elasticity and size in bicuspid aortic valve syndrome. Eur Heart J 2008;29:472–9.

    Google Scholar 

  41. Santarpia G, Scognamiglio G, Di Salvo G, D’Alto M, Sarubbi B, Romeo E, et al. Aortic and left ventricular remodeling in patients with bicuspid aortic valve without significant valvular dysfunction: a prospective study. Int J Cardiol 2012;158:347–52.

    Google Scholar 

  42. Li Y, Deng YB, Bi XJ, Liu YN, Zhang J, Li L. Evaluation of myocardial strain and artery elasticity using speckle tracking echocardiography and high-resolution ultrasound in patients with bicuspid aortic valve. Int J Cardiovasc Imaging 2016;32:1063–9.

    Google Scholar 

  43. Kurt M, Tanboga IH, Bilen E, Isik T, Kaya A, Karakaş MF, et al. Abnormal left ventricular mechanics in isolated bicuspid aortic valve disease may be independent of aortic distensibility: 2D strain imaging study. J Heart Valve Dis 2012;21:608–14.

    Google Scholar 

  44. Grotenhuis HB, Ottenkamp J, Westenberg JJM, Bax JJ, Kroft LJM, de Roos A. Reduced aortic elasticity and dilatation are associated with aortic regurgitation and left ventricular hypertrophy in nonstenotic bicuspid aortic valve patients. J Am Coll Cardiol 2007;49:1660–5.

    Google Scholar 

  45. Tzemos N, Lyseggen E, Silversides C, Jamorski M, Tong JH, Harvey P, et al. Endothelial function, carotid-femoral stiffness, and plasma matrix metalloproteinase-2 in men with bicuspid aortic valve and dilated aorta. J Am Coll Cardiol 2010;55:660–8.

    Google Scholar 

  46. Shim CY, Cho IJ, Yang WI, Kang MK, Park S, Ha JW, et al. Central aortic stiffness and its association with ascending aorta dilation in subjects with a bicuspid aortic valve. J Am Soc Echocardiogr 2011;24:847–52.

    Google Scholar 

  47. Warner PJ, Al-Quthami A, Brooks EL, Kelley-Hedgepeth A, Patvardhan E, Kuvin JT, et al. Augmentation index and aortic stiffness in bicuspid aortic valve patients with non-dilated proximal aortas. BMC Cardiovasc Disord 2013;13:19.

    Google Scholar 

  48. Hiratzka LF, Bakris GL, Beckman JA, Bersin RM, Carr VF, Casey DE, et al. 2010 ACCF/AHA/AATS/ACR/ASA/SCA/SCAI/SIR/STS/SVM guidelines for the diagnosis and management of patients with Thoracic Aortic Disease: a report of the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines, American Association for Thoracic Surgery, American College of Radiology, American Stroke Association, Society of Cardiovascular Anesthesiologists, Society for Cardiovascular Angiography and Interventions, Society of Interventional Radiology, Society of Thoracic Surgeons, and Society for Vascular Medicine. Circulation 2010;121:e266–e369.

    Google Scholar 

  49. Nishimura RA, Otto CM, Bonow RO, Carabello BA, Erwin JP, Guyton RA, et al. 2014 AHA/ACC Guideline for the Management of Patients With Valvular Heart Disease: a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines. J Am Coll Cardiol 2014;e57–e185.

  50. Galian-Gay L, Carro Hevia A, Teixido-Turà G, Rodríguez Palomares J, Gutiérrez-Moreno L, Maldonado G, et al. Familial clustering of bicuspid aortic valve and its relationship with aortic dilation in first-degree relatives. Heart 2019;105:603–8.

    Google Scholar 

  51. Huntington AK, Hunter AGW, Chan KL. A prospective study to assess the frequency of familial clustering of congenital bicuspid aortic valve. J Am Coll Cardiol 1997;30:1809–12.

    Google Scholar 

  52. Cripe L, Andelfinger G, Martin LJ, Shooner K, Benson DW. Bicuspid aortic valve is heritable. J Am Coll Cardiol 2004;44: 138–43.

    Google Scholar 

  53. Guala A, Rodríguez-Palomares J, Galian-Gay L, Teixido-Tura G, Johnson KM, Wieben O, et al. Partial aortic valve leaflet fusion is related to deleterious alteration of proximal aorta hemody-namics: a 4-dimensional flow magnetic resonance imaging study. Circulation 2019;139:2707–9.

    Google Scholar 

  54. Schnell S, Smith DA, Barker AJ, Entezari P, Honarmand AR, Carr ML, et al. Altered aortic shape in bicuspid aortic valve relatives influences blood flow patterns. Eur Heart J Cardiovasc Imaging 2016;17:1239–47.

    Google Scholar 

  55. Dietz HC, Cutting CR, Pyeritz RE, Maslen CL, Sakai LY, Corson GM, et al. Marfan syndrome caused by a recurrent de novo missense mutation in the fibrillin gene. Nature 1991;352:337–9.

    Google Scholar 

  56. Silverman DI, Burton KJ, Gray J, Bosner MS, Kouchoukos NT, Roman MJ, et al. Life expectancy in the Marfan syndrome. Am J Cardiol 1995;75:157–60.

    Google Scholar 

  57. Teixido-Tura G, Redheuil A, RodrĂ­guez-Palomares J, GutiĂ©rrez L, SĂ¡nchez V, Forteza A, et al. Aortic biomechanics by magnetic resonance: early markers of aortic disease in Marfan syndrome regardless of aortic dilatation? Int J Cardiol 2014;171:56–61.

  58. Fattori R, Bacchi Reggiani L, Pepe G, Napoli G, Bnà C, Celletti F, et al. Magnetic resonance imaging evaluation of aortic elastic properties as early expression of Marfan syndrome. J Cardiovasc Magn Reson 2000;2:251–6.

    Google Scholar 

  59. Jeremy RW, Huang H, Hwa J, McCarron H, Hughes CF, Richards JG. Relation between age, arterial distensibility, and aortic dilatation in the Marfan syndrome. Am J Cardiol 1994;74:369–73.

    Google Scholar 

  60. Groenink M, de Roos A, Mulder BJ, Verbeeten B, Timmermans J, Zwinderman AH, et al. Biophysical properties of the normal-sized aorta in patients with Marfan syndrome: evaluation with MR flow mapping. Radiology 2001;219:535–40.

    Google Scholar 

  61. Prakash A, Adlakha H, Rabideau N, Hass CJ, Morris SA, Geva T, et al. Segmental aortic stiffness in children and young adults with connective tissue disorders: relationships with age, aortic size, rate of dilation, and surgical root replacement. Circulation 2015;132:595–602.

    Google Scholar 

  62. Guala A, Teixido-Tura G, Dux-Santoy L, Granato C, Ruiz-Muñoz A, Valente F, et al. Decreased rotational flow and circumferential wall shear stress as early markers of descending aorta dilation in Marfan syndrome: a 4D flow CMR study. J Cardiovasc Magn Reson 2019;21:63.

    Google Scholar 

  63. Nollen GJ, Groenink M, Tijssen JGP, van der Wall EE, Mulder BJM. Aortic stiffness and diameter predict progressive aortic dilatation in patients with Marfan syndrome. Eur Heart J 2004; 25:1146–52.

  64. Geiger J, Markl M, Herzer L, Hirtler D, Loeffelbein F, Stiller B, et al. Aortic flow patterns in patients with Marfan syndrome assessed by flow-sensitive four-dimensional MRI. J Magn Reson Imaging 2012;35:594–600.

    Google Scholar 

  65. Geiger J, Arnold R, Herzer L, Hirtler D, Stankovic Z, Russe M, et al. Aortic wall shear stress in Marfan syndrome. Magn Reson Med 2013;70:1137–44.

    Google Scholar 

  66. Geiger J, Hirtler D, Gottfried K, Rahman O, Bollache E, Barker AJ, et al. Longitudinal evaluation of aortic hemodynamics in Marfan syndrome: new insights from a 4D flow cardiovascular magnetic resonance multi-year follow-up study. J Cardiovasc Magn Reson 2017;19:33.

    Google Scholar 

  67. Wang HH, Chiu HH, Tseng WYI, Peng HH. Does altered aortic flow in Marfan syndrome relate to aortic root dilatation? J Magn Reson Imaging 2016;44:500–8.

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Andrea Guala.

Additional information

Peer review under responsibility of the Association for Research into Arterial Structure and Physiology

Rights and permissions

This is an open access article distributed under the CC BY-NC 4.0 license (http://creativecommons.org/licenses/by-nc/4.0/).

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Guala, A., Teixido-TurĂ¡, G., Evangelista, A. et al. Magnetic Resonance Imaging for Aortic Function Evaluation in Thoracic Aortic Aneurysms. Artery Res 26, 65–70 (2020). https://doi.org/10.2991/artres.k.200322.001

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.2991/artres.k.200322.001

Keywords