Top

Journal of Cardiovascular Magnetic Resonance

Published in:

Open Access 01-12-2017 | Research

Altered aortic 3D hemodynamics and geometry in pediatric Marfan syndrome patients

Authors: Roel L. F. van der Palen, Alex J. Barker, Emilie Bollache, Julio Garcia, Michael J. Rose, Pim van Ooij, Luciana T. Young, Arno A. W. Roest, Michael Markl, Joshua D. Robinson, Cynthia K. Rigsby

Published in: Journal of Cardiovascular Magnetic Resonance | Issue 1/2017

Abstract

Background

Blood flow dynamics make it possible to better understand the development of aortopathy and cardiovascular events in patients with Marfan syndrome (MFS). Aortic 3D blood flow characteristics were investigated in relation to aortic geometry in children and adolescents with MFS.

Methods

Twenty-five MFS patients (age 15.6 ± 4.0 years; 11 females) and 21 healthy controls (age 16.0 ± 2.6 years; 12 females) underwent magnetic resonance angiography and 4D flow CMR for assessment of thoracic aortic size and 3D blood flow velocities. Data analysis included calculation of aortic diameter and BSA-indexed aortic dimensions (Z-score) along the thoracic aorta, 3D mean systolic wall shear stress (WSS_mean) in ten aortic segments and assessment of aortic blood flow patterns.

Results

Aortic root (root), ascending (AAo) and descending (DAo) aortic size was significantly larger in MFS patients than healthy controls (Root Z-score: 3.56 ± 1.45 vs 0.49 ± 0.78, p < 0.001; AAo Z-score 0.21 ± 0.95 vs −0.54 ± 0.64, p = 0.004; proximal DAo Z-score 2.02 ± 1.60 vs 0.56 ± 0.66, p < 0.001). A regional variation in prevalence and severity of flow patterns (vortex and helix flow patterns) was observed, with the aortic root and the proximal DAo (pDAo) being more frequently affected in MFS. MFS patients had significantly reduced WSS_mean in the proximal AAo (pAAo) outer segment (0.65 ± 0.12 vs. 0.73 ± 0.14 Pa, p = 0.029) and pDAo inner segment (0.74 ± 0.17 vs. 0.87 ± 0.21 Pa, p = 0.021), as well as higher WSS_mean in the inner segment of the distal AAo (0.94 ± 0.14 vs. 0.84 ± 0.15 Pa, p = 0.036) compared to healthy subjects. An inverse relationship existed between pDAo WSS_mean and both pDAo diameter (R = −0.53, p < 0.001) and % diameter change along the pDAo segment (R = −0.64, p < 0.001).

Conclusions

MFS children and young adults have altered aortic flow patterns and differences in aortic WSS that were most pronounced in the pAAo and pDAo, segments where aortic dissection or rupture often originate. The presence of vortex flow patterns and abnormal WSS correlated with regional size of the pDAo and are potentially valuable additional markers of disease severity.

Alpendurada F, Mohiaddin R. Prevalence of cardiovascular manifestations in patients with Marfan syndrome: a cardiovascular magnetic resonance stud. J Cardiovasc Magn Reson. 2008;10 Suppl 1:A164.CrossRef

Engelfriet PM, Boersma E, Tijssen JG, Bouma BJ, Mulder BJ. Beyond the root: dilatation of the distal aorta in Marfan's syndrome. Heart. 2006;92:1238–43.CrossRefPubMedPubMedCentral

Mariucci EM, Lovato L, Rosati M, Palena LM, Bonvicini M, Fattori R. Dilation of peripheral vessels in Marfan syndrome: importance of thoracoabdominal MR angiography. Int J Cardiol. 2013;167:2928–31.CrossRefPubMed

Mimoun L, Detaint D, Hamroun D, Arnoult F, Delorme G, Gautier M, Milleron O, Meuleman C, Raoux F, Boileau C, et al. Dissection in Marfan syndrome: the importance of the descending aorta. Eur Heart J. 2011;32:443–9.CrossRefPubMed

den Hartog AW, Franken R, Zwinderman AH, Timmermans J, Scholte AJ, van den Berg MP, de Waard V, Pals G, Mulder BJ, Groenink M. The risk for type B aortic dissection in Marfan syndrome. J Am Coll Cardiol. 2015;65:246–54.CrossRef

Erbel R, Aboyans V, Boileau C, Bossone E, Bartolomeo RD, Eggebrecht H, Evangelista A, Falk V, Frank H, Gaemperli O, et al. 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;2014(35):2873–926.

van Ooij P, Potters WV, Collins J, Carr M, Carr J, Malaisrie SC, Fedak PW, McCarthy PM, Markl M, Barker AJ. Characterization of abnormal wall shear stress using 4D flow MRI in human bicuspid aortopathy. Ann Biomed Eng. 2015;43:1385–97.CrossRefPubMed

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

Wang HH, Chiu HH, Tseng WI, Peng HH. Does altered aortic flow in marfan syndrome relate to aortic root dilatation? J Magn Reson Imaging. 2016;44:500–08.

10.

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

11.

Wigstrom L, Ebbers T, Fyrenius A, Karlsson M, Engvall J, Wranne B, Bolger AF. Particle trace visualization of intracardiac flow using time-resolved 3D phase contrast MRI. Magn Reson Med. 1999;41:793–9.CrossRefPubMed

12.

Buonocore MH. Visualizing blood flow patterns using streamlines, arrows, and particle paths. Magn Reson Med. 1998;40:210–26.CrossRefPubMed

13.

Markl M, Frydrychowicz A, Kozerke S, Hope M, Wieben O. 4D flow MRI. J Magn Reson Imaging. 2012;36:1015–36.CrossRefPubMed

14.

Markl M, Schnell S, Wu C, Bollache E, Jarvis K, Barker AJ, Robinson JD, Rigsby CK. Advanced flow MRI: emerging techniques and applications. Clin Radiol. 2016;71:779–95.

15.

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

16.

Loeys BL, Dietz HC, Braverman AC, Callewaert BL, De Backer J, Devereux RB, Hilhorst-Hofstee Y, Jondeau G, Faivre L, Milewicz DM, et al. The revised Ghent nosology for the Marfan syndrome. J Med Genet. 2010;47:476–85.CrossRefPubMed

17.

Hiratzka LF, Bakris GL, Beckman JA, Bersin RM, Carr VF, Casey Jr DE, Eagle KA, Hermann LK, Isselbacher EM, Kazerooni EA, et al. 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. J Am Coll Cardiol. 2010;55:e27–e129.CrossRefPubMed

18.

Burman ED, Keegan J, Kilner PJ. Aortic root measurement by cardiovascular magnetic resonance: specification of planes and lines of measurement and corresponding normal values. Circ Cardiovasc Imaging. 2008;1:104–13.CrossRefPubMed

19.

Nejatian A, Yu J, Geva T, White MT, Prakash A. Aortic measurements in patients with aortopathy are larger and more reproducible by cardiac magnetic resonance compared with echocardiography. Pediatr Cardiol. 2015;36:1761–73.CrossRefPubMed

20.

Mosteller RD. Simplified calculation of body-surface area. N Engl J Med. 1987;317:1098.PubMed

21.

Chubb H, Simpson JM. The use of Z-scores in paediatric cardiology. Ann Pediatr Cardiol. 2012;5:179–84.CrossRefPubMedPubMedCentral

22.

Johnson RK, Premraj S, Patel SS, Wahle A, Stolpen A, Sonka M, Scholz TD. Quantitative assessment of the entire thoracic aorta from magnetic resonance images. Cardiol Young. 2011;21:170–7.CrossRefPubMed

23.

Allen BD, van Ooij P, Barker AJ, Carr M, Gabbour M, Schnell S, Jarvis KB, Carr JC, Markl M, Rigsby C, Robinson JD. Thoracic aorta 3D hemodynamics in pediatric and young adult patients with bicuspid aortic valve. J Magn Reson Imaging. 2015;42:954–63.CrossRefPubMedPubMedCentral

24.

Bock J, Kreher B, Henning J, Markl M. Optimized pre-processing of time-resolved 2D and 3D phase contrast MRI data. Proceedings of the 15th Annual Meeting of ISMRM, Berlin, Germany. 2007:604. (Abstract 3138).

25.

Potters WV, van Ooij P, Marquering H, van Bavel E, Nederveen AJ. Volumetric arterial wall shear stress calculation based on cine phase contrast MRI. J Magn Reson Imaging. 2015;41:505–16.CrossRefPubMed

26.

van Ooij P, Powell AL, Potters WV, Carr JC, Markl M, Barker AA. Reproducibility and interobserver variability of systolic blood flow velocity and 3D wall shear stress derived from 4D flow MRI in the healthy aorta. J Magn Reson Imaging. 2016;43:236–48.CrossRefPubMed

27.

Faivre L, Masurel-Paulet A, Collod-Beroud G, Callewaert BL, Child AH, Stheneur C, Binquet C, Gautier E, Chevallier B, Huet F, et al. Clinical and molecular study of 320 children with Marfan syndrome and related type I fibrillinopathies in a series of 1009 probands with pathogenic FBN1 mutations. Pediatrics. 2009;123:391–8.CrossRefPubMed

28.

van Karnebeek CD, Naeff MS, Mulder BJ, Hennekam RC, Offringa M. Natural history of cardiovascular manifestations in Marfan syndrome. Arch Dis Child. 2001;84:129–37.CrossRefPubMedPubMedCentral

29.

Finkbohner R, Johnston D, Crawford ES, Coselli J, Milewicz DM. Marfan syndrome. Long-term survival and complications after aortic aneurysm repair. Circulation. 1995;91:728–33.CrossRefPubMed

30.

Fisher RG, Sanchez-Torres M, Whigham CJ, Thomas JW. "Lumps" and "bumps" that mimic acute aortic and brachiocephalic vessel injury. Radiographics. 1997;17:825–34.CrossRefPubMed

31.

Picher A, Cassar TE, Suttie J, Francis JM, Leeson P, Blair E, Wordsworth BP, Forfar JC, Myerson SG, Markl M, et al. Visualisation of aortic flow disturbance in Marfan syndrome by 4D phase-contrast CMR. J Cardiovasc Magn Reson. 2011;13 Suppl 1:201.CrossRef

32.

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

33.

Frydrychowicz A, Arnold R, Hirtler D, Schlensak C, Stalder AF, Hennig J, Langer M, Markl M. Multidirectional flow analysis by cardiovascular magnetic resonance in aneurysm development following repair of aortic coarctation. J Cardiovasc Magn Reson. 2008;10:30.CrossRefPubMedPubMedCentral

34.

Hope TA, Kvitting JP, Hope MD, Miller DC, Markl M, Herfkens RJ. Evaluation of Marfan patients status post valve-sparing aortic root replacement with 4D flow. Magn Reson Imaging. 2013;31:1479–84.CrossRefPubMed

35.

Burk J, Blanke P, Stankovic Z, Barker A, Russe M, Geiger J, Frydrychowicz A, Langer M, Markl M. Evaluation of 3D blood flow patterns and wall shear stress in the normal and dilated thoracic aorta using flow-sensitive 4D CMR. J Cardiovasc Magn Reson. 2012;14:84.CrossRefPubMedPubMedCentral

36.

Truong U, Fonseca B, Dunning J, Burgett S, Lanning C, Ivy DD, Shandas R, Hunter K, Barker AJ. Wall shear stress measured by phase contrast cardiovascular magnetic resonance in children and adolescents with pulmonary arterial hypertension. J Cardiovasc Magn Reson. 2013;15:81.CrossRefPubMedPubMedCentral

37.

van Ooij P, Garcia J, Potters WV, Malaisrie SC, Collins JD, Carr JC, Markl M, Barker AJ. Age-related changes in aortic 3D blood flow velocities and wall shear stress: Implications for the identification of altered hemodynamics in patients with aortic valve disease. J Magn Reson Imaging. 2016;43:1239–49.CrossRefPubMed

38.

Allen BD, Markl M, Barker AJ, van Ooij P, Carr JC, Malaisrie SC, McCarthy P, Bonow RO, Kansal P. Influence of beta-blocker therapy on aortic blood flow in patients with bicuspid aortic valve. Int J Cardiovasc Imaging. 2016;32:621–8.CrossRefPubMed

39.

Querzoli G, Fortini S, Espa S, Costantini M, Sorgini F. Fluid dynamics of aortic root dilation in Marfan syndrome. J Biomech. 2014;47:3120–8.CrossRefPubMed

Title: Altered aortic 3D hemodynamics and geometry in pediatric Marfan syndrome patients
Authors: Roel L. F. van der Palen
Alex J. Barker
Emilie Bollache
Julio Garcia
Michael J. Rose
Pim van Ooij
Luciana T. Young
Arno A. W. Roest
Michael Markl
Joshua D. Robinson
Cynthia K. Rigsby
Publication date: 01-12-2017
Publisher: BioMed Central
Published in: Journal of Cardiovascular Magnetic Resonance / Issue 1/2017
Electronic ISSN: 1532-429X
DOI: https://doi.org/10.1186/s12968-017-0345-7

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Altered aortic 3D hemodynamics and geometry in pediatric Marfan syndrome patients

Abstract

Background

Methods

Results

Conclusions

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 1/2017

The global cardiovascular magnetic resonance registry (GCMR) of the society for cardiovascular magnetic resonance (SCMR): its goals, rationale, data infrastructure, and current developments

Effects of caffeine on the detection of ischemia in patients undergoing adenosine stress cardiovascular magnetic resonance imaging

Nonenhanced MR angiography of the pulmonary arteries using single-shot radial quiescent-interval slice-selective (QISS): a technical feasibility study

Sources of variability in quantification of cardiovascular magnetic resonance infarct size - reproducibility among three core laboratories

CMR fluoroscopy right heart catheterization for cardiac output and pulmonary vascular resistance: results in 102 patients

Ambulatory systolic blood pressure and obesity are independently associated with left ventricular hypertrophic remodeling in children