Cardiovascular Engineering and Technology

, Volume 8, Issue 3, pp 378–389 | Cite as

Pulsatile Flow Leads to Intimal Flap Motion and Flow Reversal in an In Vitro Model of Type B Aortic Dissection

  • Joav BirjiniukEmail author
  • Lucas H. Timmins
  • Mark Young
  • Bradley G. Leshnower
  • John N. Oshinski
  • David N. Ku
  • Ravi K. Veeraswamy


Understanding of the hemodynamics of Type B aortic dissection may improve outcomes by informing upon patient selection, device design, and deployment strategies. This project characterized changes to aortic hemodynamics as the result of dissection. We hypothesized that dissection would lead to elevated flow reversal and disrupted pulsatile flow patterns in the aorta that can be detected and quantified by non-invasive magnetic resonance imaging. Flexible, anatomic models of both normal aorta and dissected aorta, with a mobile intimal flap containing entry and exit tears, were perfused with a physiologic pulsatile waveform. Four-dimensional phase contrast magnetic resonance (4D PCMR) imaging was used to measure the hemodynamics. These images were processed to quantify pulsatile fluid velocities, flow rate, and flow reversal. Four-dimensional flow imaging in the dissected aorta revealed pockets of reverse flow and vortices primarily in the false lumen. The dissected aorta exhibited significantly greater flow reversal in the proximal-to-mid dissection as compared to normal (21.1 ± 3.8 vs. 1.98 ± 0.4%, p < 0.001). Pulsatility induced unsteady vortices and a pumping motion of the distal intimal flap corresponding to flow reversal. Summed true and false lumen flow rates in dissected models (4.0 ± 2.0 L/min) equaled normal flow rates (3.8 ± 0.1 L/min, p > 0.05), validated against external flow measurement. Pulsatile aortic hemodynamics in the presence of an anatomic, elastic dissection differed significantly from those of both steady flow through a dissection and pulsatile flow through a normal aorta. New hemodynamic features including flow reversal, large exit tear vortices, and pumping action of the mobile intimal flap, were observed. False lumen flow reversal would possess a time-averaged velocity close to stagnation, which may induce future thrombosis. Focal vortices may identify the location of tears that could be covered with a stent-graft. Future correlation of hemodynamics with outcomes may indicate which patients require earlier intervention.


4D PCMR Aortic dissection Flow model Hemodynamics Intimal flap motion 



We would like to acknowledge funding for this work from Medtronic, Inc.

Conflicts of Interest

Joav Birjiniuk has received a graduate research assistantship from Medtronic, Inc. Lucas Timmins declares that he has no conflict of interest. Mark Young is an employee of Medtronic, Inc. John Oshinski declares that he has no conflict of interest. David Ku declares that he has no conflict of interest. Ravi Veeraswamy has received consulting fees from Medtronic, Inc.

Ethical Approval

This article does not contain any studies with human participants or animals performed by any of the authors.


This study was funded by Medtronic, Inc. The following authors have received benefits for personal or professional use from a commercial party (Medtronic, Inc.) related directly to the subject matter of this manuscript: graduate research assistantship (J.B.), employment and salary (M.Y.), and consulting fees (R.K.V).

Supplementary material

13239_2017_312_MOESM1_ESM.tiff (440 kb)
Supplemental Figure 1 Pump driver voltage (top), central aortic pressure (middle), and model outlet flow rate (bottom) traces demonstrating physiologic pumping (TIFF 439 kb)
13239_2017_312_MOESM2_ESM.tiff (2 mb)
Supplemental Figure 2 Transverse motion of the intimal flap at different points in the cardiac cycle. Note accentuated motion of the intimal flap at the level of the exit tear (arrow) during fluid deceleration (TIFF 2093 kb)
13239_2017_312_MOESM3_ESM.tiff (5.8 mb)
Supplemental Figure 3 Pathline visualizations in both normal and dissected aortae. Physiological, helical flows can be noted throughout the aortic arch in both models, with significant skewing of velocity profile towards true lumen in the dissected case. Note filling of distal true lumen with cessation of flow partway down the false lumen (TIFF 5918 kb)
13239_2017_312_MOESM4_ESM.tiff (1.4 mb)
Supplemental Figure 4 Luminal flow rates in normal (black) and dissected (colored) aorta. Slice locations on right correspond to slices designated on left (asterisks indicate significant difference from the Normal aorta at all slices, p < 0.05) (TIFF 1392 kb)

Supplemental Video 1 Fluid flow reconstructed from PCMR data. Detail on right demonstrating diastolic vortex forming at exit tear (MP4 16570 kb)

Supplemental Video 2 Dye visualization of reversed false lumen flow and exit tear vortex formation in aortic dissection model (MOV 332517 kb)


  1. 1.
    Ahrens, J., B. Geveci, and C. Law. ParaView: an end-user tool for large data visualization. In: Visualization Handbook, edited by C. D. Hansen, and C. R. Johnson. Cambridge: Academic Press, 2005, pp. 717–731.CrossRefGoogle Scholar
  2. 2.
    Akutsu, K., J. Nejima, K. Kiuchi, K. Sasaki, M. Ochi, K. Tanaka, et al. Effects of the patent false lumen on the long-term outcome of type B acute aortic dissection. Eur. J. Cardiothorac. Surg. 26:359–366, 2004.CrossRefGoogle Scholar
  3. 3.
    Alimohammadi, M., J. M. Sherwood, M. Karimpour, O. Agu, S. Balabani, and V. Diaz-Zuccarini. Aortic dissection simulation models for clinical support: fluid–structure interaction vs. rigid wall models. Biomed. Eng. Online 14:1–16, 2015.CrossRefGoogle Scholar
  4. 4.
    Birjiniuk, J., J. M. Ruddy, E. Iffrig, T. S. Henry, B. G. Leshnower, J. N. Oshinski, et al. Development and testing of a silicone in vitro model of descending aortic dissection. J. Surg. Res. 198(2):502–507, 2015.CrossRefGoogle Scholar
  5. 5.
    Cecchi, E., C. Giglioli, S. Valente, C. Lazzeri, G. F. Gensini, R. Abbate, et al. Role of hemodynamic shear stress in cardiovascular disease. Atherosclerosis 214(2):249–256, 2011.CrossRefGoogle Scholar
  6. 6.
    “Characteristic Properties of Silicone Rubber Compounds.” Shin-Etsu Co.
  7. 7.
    Chatzizisis, Y. S., A. H. Coskun, M. Jonas, E. R. Edelman, C. L. Feldman, and P. H. Stone. Role of endothelial shear stress in the natural history of coronary atherosclerosis and vascular remodeling. J. Am. Coll. Cardiol. 49(25):2379–2393, 2007.CrossRefGoogle Scholar
  8. 8.
    Chen, D., M. Müller-Eschner, H. von Tengg-Kobligk, D. Barber, D. Böckler, R. Hose, et al. A patient-specific study of type-B aortic dissection: evaluation of true-false lumen blood exchange. Biomed. Eng. Online 12:1–16, 2013.CrossRefGoogle Scholar
  9. 9.
    Cheng, Z., N. B. Wood, R. G. J. Gibbs, and X. Y. Xu. Geometric and flow features of type B aortic dissection: initial findings and comparison of medically treated and stented cases. Ann. Biomed. Eng. 43(1):177–189, 2015.CrossRefGoogle Scholar
  10. 10.
    Chung, J. W., C. Elkins, T. Sakai, N. Kato, T. Vestring, C. P. Semba, et al. True-lumen collapse in aortic dissection: Part I. Evaluation of causative factors in phantoms with pulsatile flow. Radiology 214:87–98, 2000.CrossRefGoogle Scholar
  11. 11.
    Clough, R. E., M. Waltham, D. Giese, P. R. Taylor, and T. Schaeffter. A new imaging method for assessment of aortic dissection using four-dimensional phase contrast magnetic resonance imaging. J. Vasc. Surg. 55(4):914–923, 2012.CrossRefGoogle Scholar
  12. 12.
    Davies, P. F. Hemodynamic shear stress and the endothelium in cardiovascular pathophysiology. Nat. Clin. Pract. Cardiovasc. Med. 6(1):16–26, 2009.CrossRefGoogle Scholar
  13. 13.
    Eggebrecht, H., U. Herold, O. Kuhnt, A. Schmermund, T. Bartel, S. Martini, et al. Endovascular stent-graft treatment of aortic dissection: determinants of post-interventional outcome. Eur. Heart J. 26(5):489–497, 2005.CrossRefGoogle Scholar
  14. 14.
    François, C. J., M. Markl, M. L. Schiebler, E. Niespodzany, B. R. Landgraf, C. Schlensak, et al. Four-dimensional, flow-sensitive magnetic resonance imaging of blood flow patterns in thoracic aortic dissections. J. Thorac. Cardiovasc. Surg. 145(5):1359–1366, 2013.CrossRefGoogle Scholar
  15. 15.
    Haskett, D., et al. Microstructural and biomechanical alterations of the human aorta as a function of age and location. Biomech. Model. Mechanobiol. 9(6):725–736, 2010.CrossRefGoogle Scholar
  16. 16.
    Hwang, J., A. Saha, Y. C. Boo, G. P. Sorescu, J. S. McNally, S. M. Holland, et al. Oscillatory shear stress stimulates endothelial production of O2 from p47phox-dependent NAD(P)H oxidases, leading to monocyte adhesion. J. Biol. Chem. 278(47):47291–47298, 2003.CrossRefGoogle Scholar
  17. 17.
    Jackson, J. P. The growing complexity of platelet aggregation. Blood 109(12):5087–5095, 2007.CrossRefGoogle Scholar
  18. 18.
    Karmonik, C., S. Partovi, M. Müller-Eschner, J. Bismuth, M. G. Davies, D. J. Shah, et al. Longitudinal computational fluid dynamics study of aneurysmal dilatation in a chronic DeBakey type III aortic dissection. J. Vasc. Surg. 56(1):260–263.e1, 2012.CrossRefGoogle Scholar
  19. 19.
    Kilner, P. J., G. Z. Yang, R. H. Mohiaddin, D. N. Firmin, and D. B. Longmore. Helical and retrograde secondary flow patterns in the aortic arch studied by three-dimensional magnetic resonance velocity mapping. Circulation 88(5):2235–2247, 1993.CrossRefGoogle Scholar
  20. 20.
    Ku, D. N., D. P. Giddens, C. K. Zarins, and S. Glagov. Pulsatile flow and atherosclerosis in the human carotid bifurcation. Positive correlation between plaque location and low oscillating shear stress. Arterioscler. Thromb. Vasc. Biol. 5(3):293–302, 1985.Google Scholar
  21. 21.
    LeMaire, S. A., and L. Russell. Epidemiology of thoracic aortic dissection. Nat. Rev. Cardiol. 8(2):103–113, 2011.CrossRefGoogle Scholar
  22. 22.
    Lin, L. I. A concordance correlation coefficient to evaluate reproducibility. Biometrics 45(1):255–268, 1989.CrossRefGoogle Scholar
  23. 23.
    Markl, M., A. Frydrychowicz, S. Kozerke, M. Hope, and O. Wieben. 4D Flow MRI. J. Magn. Reson. Imaging 36:1015–1036, 2012.CrossRefGoogle Scholar
  24. 24.
    Mészáros, I., J. Mórocz, J. Szlávi, J. Schmidt, L. Tornóci, L. Nagy, et al. Epidemiology and clinicopathology of aortic dissection: a population-based longitudinal study over 27 years. Chest 117(5):1271–1278, 2000.CrossRefGoogle Scholar
  25. 25.
    Mohr-Kahaly, S., R. Erbel, H. Rennollet, N. Wittlich, M. Drexler, H. Oelert, et al. Ambulatory follow-up of aortic dissection by transesophageal two-dimensional and color-coded Doppler echocardiography. Circulation 80(1):24–33, 1989.CrossRefGoogle Scholar
  26. 26.
    Moore, J. E., C. Xu, S. Glagov, C. K. Zarins, and D. N. Ku. Fluid wall shear stress measurements in a model of the human abdominal aorta: oscillatory behavior and relationship to atherosclerosis. Atherosclerosis 110(2):225–240, 1994.CrossRefGoogle Scholar
  27. 27.
    Nienaber, C. A., and R. E. Clough. Management of acute aortic dissection. Lancet 385:800–811, 2015.CrossRefGoogle Scholar
  28. 28.
    Nienaber, C. A., S. Kische, H. Rousseau, H. Eggebrecht, T. C. Rehders, G. Kundt, et al. Endovascular repair of type B aortic dissection: long-term results of the randomized investigation of stent-grafts in aortic dissection trial. Circ. Cardiovasc. Interv. 6(4):407–416, 2013.CrossRefGoogle Scholar
  29. 29.
    Nienaber, C. A., H. Rousseau, H. Eggebrecht, S. Kische, R. Fattori, T. C. Rehders, et al. Randomized comparison of strategies for type B aortic dissection: the Investigation of STEnt grafts in Aortic Dissection (INSTEAD) trial. Circulation 120:2519–2528, 2009.CrossRefGoogle Scholar
  30. 30.
    Ranjan, V., Z. Xiao, and S. L. Diamond. Constitutive NOS expression in cultured endothelial cells is elevated by fluid shear stress. Am. J. Physiol. 269(2):H550–H555, 1995.Google Scholar
  31. 31.
    Rudenick, P. A., B. H. Bijnens, D. García-Dorado, and A. Evangelista. An in vitro phantom study on the influence of tear size and configuration on the hemodynamics of the lumina in chronic type B aortic dissections. J. Vasc. Surg. 57(2):464–474, 2013.CrossRefGoogle Scholar
  32. 32.
    Rudenick, P. A., B. H. Bijnens, P. Segers, D. García-Dorado, and A. Evangelista. Assessment of wall elasticity variations on intraluminal haemodynamics in descending aortic dissections using a lumped-parameter model. PLoS ONE 10(4):e0124011, 2015.CrossRefGoogle Scholar
  33. 33.
    Ruggeri, Z. M. Platelet adhesion under flow. Microcirculation 16:58–83, 2009.CrossRefGoogle Scholar
  34. 34.
    Sorescu, G. P., M. Sykes, D. Weiss, M. O. Platt, A. Saha, J. Hwang, et al. Bone morphogenic protein 4 produced in endothelial cells by oscillatory shear stress stimulates an inflammatory response. J. Biol. Chem. 278(33):31128–31135, 2003.CrossRefGoogle Scholar
  35. 35.
    Sueyoshi, E., I. Sakamoto, K. Hayashi, T. Yamaguchi, and T. Imada. Growth rate of aortic diameter in patients with Type B aortic dissection during the chronic phase. Circulation 110(Supplemental II):II256–II261, 2004.Google Scholar
  36. 36.
    Tanaka, A., M. Sakakibara, H. Ishii, R. Hayashida, Y. Jinno, S. Okumura, et al. Influence of the false lumen status on clinical outcomes in patients with acute type B aortic dissection. J. Vasc. Surg. 59(2):321–326, 2014.CrossRefGoogle Scholar
  37. 37.
    Tsai, T. T., A. Evangelista, C. A. Nienaber, T. Myrmel, G. Meinhardt, J. V. Cooper, et al. Partial thrombosis of the false lumen in patients with acute type B aortic dissection. N. Engl. J. Med. 357(4):349–359, 2007.CrossRefGoogle Scholar
  38. 38.
    Tsai, T. T., M. S. Schlicht, K. Khanafer, J. L. Bull, D. T. Valassis, D. M. Williams, et al. Tear size and location impacts false lumen pressure in an ex vivo model of chronic type B aortic dissection. J. Vasc. Surg. 47(4):844–851, 2008.CrossRefGoogle Scholar
  39. 39.
    Tsai, T. T., S. Trimarchi, and C. A. Nienaber. Acute aortic dissection: perspectives from the International Registry of Acute Aortic Dissection (IRAD). Eur. J. Vasc. Endovasc. Surg. 37(2):149–159, 2009.CrossRefGoogle Scholar
  40. 40.
    Vorp, D. A., et al. Wall strength and stiffness of aneurysmal and nonaneurysmal abdominal aorta. Ann. N. Y. Acad. Sci. 800:274–276, 1996.CrossRefGoogle Scholar
  41. 41.
    Womersley, J. R. Method for the calculation of velocity, rate of flow and viscous drag in arteries when the pressure gradient is known. J. Physiol. 127:553–563, 1955.CrossRefGoogle Scholar

Copyright information

© Biomedical Engineering Society 2017

Authors and Affiliations

  1. 1.Wallace H. Coulter Department of Biomedical EngineeringGeorgia Institute of TechnologyAtlantaUSA
  2. 2.Department of BioengineeringUniversity of UtahSalt Lake CityUSA
  3. 3.Cardiac and Vascular GroupMedtronic, Inc.Santa RosaUSA
  4. 4.Division of Cardiothoracic Surgery, Joseph B. Whitehead Department of SurgeryEmory University School of MedicineAtlantaUSA
  5. 5.Department of Radiology and Imaging SciencesEmory University School of MedicineAtlantaUSA
  6. 6.George W. Woodruff School of Mechanical EngineeringGeorgia Institute of TechnologyAtlantaUSA
  7. 7.Division of Vascular Surgery, Joseph B. Whitehead Department of SurgeryEmory University School of MedicineAtlantaUSA
  8. 8.Division of Vascular Surgery, Department of SurgeryMedical University of South CarolinaCharlestonUSA
  9. 9.Emory University School of MedicineAtlantaUSA

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