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Annals of Biomedical Engineering

, Volume 45, Issue 5, pp 1305–1314 | Cite as

Aortic Regurgitation Generates a Kinematic Obstruction Which Hinders Left Ventricular Filling

  • Ikechukwu Okafor
  • Vrishank Raghav
  • Jose F. Condado
  • Prem A. Midha
  • Gautam Kumar
  • Ajit P. YoganathanEmail author
Article

Abstract

An incompetent aortic valve (AV) results in aortic regurgitation (AR), where retrograde flow of blood into the left ventricle (LV) is observed. In this work, we parametrically characterized the detailed changes in intra-ventricular flow during diastole as a result of AR in a physiological in vitro left-heart simulator (LHS). The loss of energy within the LV as the level of AR increased was also assessed. The validated LHS consisted of an optically-clear, flexible wall LV and a modular AV holder. Two-component, planar, digital particle image velocimetry was used to visualize and quantify intra-ventricular flow. A large coherent vortical structure which engulfed the whole LV was observed under control conditions. In the cases with AR, the regurgitant jet was observed to generate a “kinematic obstruction” between the mitral valve and the LV apex, preventing the trans-mitral jet from generating a coherent vortical structure. The regurgitant jet was also observed to impinge on the inferolateral wall of the LV. Energy dissipation rate (EDR) for no, trace, mild, and moderate AR were found to be 1.15, 2.26, 3.56, and 5.99 W/m3, respectively. This study has, for the first time, performed an in vitro characterization of intra-ventricular flow in the presence of AR. Mechanistically, the formation of a “kinematic obstruction” appears to be the cause of the increased EDR (a metric quantifiable in vivo) during AR. EDR increases non-linearly with AR fraction and could potentially be used as a metric to grade severity of AR and develop clinical interventional timing strategies for patients.

Keywords

Left ventricle filling Vortex flow Aortic regurgitation Energy dissipation Aortic valve 

Notes

Acknowledgments

We would like to thank VenAir (Terrassa-Barcelona, Spain) for casting the silicone LV, the machine shop personnel at the School of Chemical and Biomolecular Engineering at Georgia Tech for machining the LHS, and finally Procter & Gamble for providing the glycerin used in this work. Funding was provided by American Heart Association (Grant No. 16POST27520030).

Conflict of Interests

The authors have no conflicts of interests to disclose.

Supplementary material

Supplementary material 1 (MP4 5375 kb)

Supplementary material 2 (MP4 6207 kb)

10439_2017_1790_MOESM3_ESM.mp4 (3.2 mb)
Supplementary material 3 (MP4 3253 kb)

Supplementary material 4 (MP4 6196 kb)

10439_2017_1790_MOESM5_ESM.tif (1.2 mb)
Supplementary material 5 (TIFF 1230 kb) Supplementary Figure 1: Out of plane vorticity color map overlaid with streamlines for the plane 5 mm offset from the central LVOT plane of the mild AR case at T = (a) 0.05 s, start E-wave, (b) 0.15 s, peak E-wave, (c) 0.275 s, end E-wave, and (d) 0.5 s, peak A-wave

References

  1. 1.
    Augoustides, J. G. T., Y. Wolfe, E. K. Walsh, and W. Y. Szeto. Recent advances in aortic valve disease: highlights from a bicuspid aortic valve to transcatheter aortic valve replacement. J. Cardiothorac. Vasc. Anesth. 23:569–576, 2009.CrossRefPubMedGoogle Scholar
  2. 2.
    Austen, W. G., H. W. Bender, B. R. Wilcox, and A. G. Morrow. Experimental aortic regurgitation. J. Surg. Res. 3:466–470, 1963.CrossRefPubMedGoogle Scholar
  3. 3.
    Bekeredjian, R., and P. A. Grayburn. Valvular heart disease: aortic regurgitation. Circulation 112:125–134, 2005.CrossRefPubMedGoogle Scholar
  4. 4.
    Beroukhim, R. S., D. A. Graham, R. Margossian, D. W. Brown, T. Geva, and S. D. Colan. An echocardiographic model predicting severity of aortic regurgitation in congenital heart disease. Circ. Cardiovasc. Imaging 3:542–549, 2010.CrossRefPubMedGoogle Scholar
  5. 5.
    Bonow, R. O., B. A. Carabello, K. Chatterjee, A. C. de Leon, D. P. Faxon, M. D. Freed, W. H. Gaasch, B. W. Lytle, R. A. Nishimura, P. T. O’Gara, R. A. O’Rourke, C. M. Otto, P. M. Shah, J. S. Shanewise, S. C. Smith, A. K. Jacobs, C. D. Adams, J. L. Anderson, E. M. Antman, D. P. Faxon, V. Fuster, J. L. Halperin, L. F. Hiratzka, S. A. Hunt, B. W. Lytle, R. Nishimura, R. L. Page, and B. Riegel. ACC/AHA 2006 Guidelines for the management of patients with valvular heart disease. J. Am. Coll. Cardiol. 48:e1–e148, 2006.CrossRefPubMedGoogle Scholar
  6. 6.
    Calleja, A., P. Thavendiranathan, R. I. Ionasec, H. Houle, S. Liu, I. Voigt, C. Sai Sudhakar, J. Crestanello, T. Ryan, and M. A. Vannan. Automated quantitative 3-dimensional modeling of the aortic valve and root by 3-dimensional transesophageal echocardiography in normals, aortic regurgitation, and aortic stenosis: comparison to computed tomography in normals and clinical implications. Circ. Cardiovasc. Imaging 6:99–108, 2013.CrossRefPubMedGoogle Scholar
  7. 7.
    Carlsson, M., E. Heiberg, J. Toger, and H. Arheden. Quantification of left and right ventricular kinetic energy using four-dimensional intracardiac magnetic resonance imaging flow measurements. Am. J. Physiol. Heart Circ. Physiol. 302:H893–H900, 2012.CrossRefPubMedGoogle Scholar
  8. 8.
    Ewe, S. H., V. Delgado, R. van der Geest, J. J. M. Westenberg, M. L. A. Haeck, T. G. Witkowski, D. Auger, N. A. Marsan, E. R. Holman, A. de Roos, M. J. Schalij, J. J. Bax, A. Sieders, and H. J. Siebelink. Accuracy of three-dimensional versus two-dimensional echocardiography for quantification of aortic regurgitation and validation by three-dimensional three-directional velocity-encoded magnetic resonance imaging. Am. J. Cardiol. 112:560–566, 2013.CrossRefPubMedGoogle Scholar
  9. 9.
    Goldbarg, S. H., and J. L. Halperin. Aortic regurgitation: disease progression and management. Nat. Clin. Pract. Cardiovasc. Med. 5:269–279, 2008.CrossRefPubMedGoogle Scholar
  10. 10.
    Gotzmann, M., M. Lindstaedt, and A. Mügge. From pressure overload to volume overload: aortic regurgitation after transcatheter aortic valve implantation. Am. Heart J. 163:903–911, 2012.CrossRefPubMedGoogle Scholar
  11. 11.
    Grossman, W. Diastolic properties of the left ventricle. Ann. Intern. Med. 84:316, 1976.CrossRefPubMedGoogle Scholar
  12. 12.
    Leon, M. B., et al. Transcatheter or surgical aortic-valve replacement in intermediate-risk patients. N. Engl. J. Med. 374:1609–1609, 2016. doi: 10.1056/NEJMoa1514616.CrossRefPubMedGoogle Scholar
  13. 13.
    Lerakis, S., S. S. Hayek, and P. S. Douglas. Paravalvular aortic leak after transcatheter aortic valve replacement: current knowledge. Circulation 127:397–407, 2013.CrossRefPubMedGoogle Scholar
  14. 14.
    Nishimura, R. A., C. M. Otto, R. O. Bonow, B. A. Carabello, J. P. Erwin, R. A. Guyton, P. T. O’Gara, C. E. Ruiz, N. J. Skubas, P. Sorajja, T. M. Sundt, and J. D. Thomas. 2014 AHA/ACC guideline for the management of patients with valvular heart disease. J. Am. Coll. Cardiol. 63:e57–e185, 2014.CrossRefPubMedGoogle Scholar
  15. 15.
    Okafor, I., V. Raghav, P. Midha, G. Kumar, and A. Yoganathan. The hemodynamic effects of acute aortic regurgitation into a stiffened left ventricle resulting from chronic aortic stenosis. Am. J. Physiol. Hear. Circ. Physiol. 310:H1801–H1807, 2016.CrossRefGoogle Scholar
  16. 16.
    Okafor, I. U., A. Santhanakrishnan, B. D. Chaffins, L. Mirabella, J. N. Oshinski, and A. P. Yoganathan. Cardiovascular magnetic resonance compatible physical model of the left ventricle for multi-modality characterization of wall motion and hemodynamics. J. Cardiovasc. Magn. Reson. 17:51, 2015.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Okafor, I. U., A. Santhanakrishnan, V. S. Raghav, and A. P. Yoganathan. Role of mitral annulus diastolic geometry on intraventricular filling dynamics. J. Biomech. Eng. 137:121007, 2015.CrossRefPubMedGoogle Scholar
  18. 18.
    Pedrizzetti, G., and F. Domenichini. Left ventricular fluid mechanics: the long way from theoretical models to clinical applications. Ann. Biomed. Eng. 2014. doi: 10.1007/s10439-014-1101-x.PubMedGoogle Scholar
  19. 19.
    Pedrizzetti, G., and P. P. Sengupta. Vortex imaging: new information gain from tracking cardiac energy loss. Eur. Hear. J. Cardiovasc. Imaging 10–11, 2015. doi: 10.1093/ehjci/jev070
  20. 20.
    Pedrizzetti, G., A. R. Martiniello, V. Bianchi, A. D’Onofrio, P. Caso, and G. Tonti. Cardiac fluid dynamics anticipates heart adaptation. J. Biomech. 48:388–391, 2015.CrossRefPubMedGoogle Scholar
  21. 21.
    Pierrakos, O., and P. P. Vlachos. The effect of vortex formation on left ventricular filling and mitral valve efficiency. J. Biomech. Eng. 128:527–539, 2006.CrossRefPubMedGoogle Scholar
  22. 22.
    Raffel, M., C. E. Willert, S. T. Wereley, and J. Kompenhans. Particle Image Velocimetry. Berlin: Springer, 2007.Google Scholar
  23. 23.
    Saarenrinne, P., and M. Piirto. Turbulent kinetic energy dissipation rate estimation from PIV velocity vector fields. Exp. Fluids 2000. doi: 10.1007/s003480070032.Google Scholar
  24. 24.
    Sakhaeimanesh, A. A., and Y. S. Morsi. Analysis of regurgitation, mean systolic pressure drop and energy losses for two artificial aortic valves. J. Med. Eng. Technol. 23:63–68, 1999.CrossRefPubMedGoogle Scholar
  25. 25.
    Santhanakrishnan, A., I. Okafor, G. Kumar, and A. P. Yoganathan. Atrial systole enhances intraventricular filling flow propagation during increasing heart rate. J. Biomech. 1–6, 2016. doi: 10.1016/j.jbiomech.2016.01.026
  26. 26.
    Sharp, K. V., and R. J. Adrian. PIV Study of small-scale flow structure around a Rushton turbine. AIChE J. 47:766–778, 2001.CrossRefGoogle Scholar
  27. 27.
    Sinning, J.-M., M. Vasa-Nicotera, D. Chin, C. Hammerstingl, A. Ghanem, J. Bence, J. Kovac, E. Grube, G. Nickenig, and N. Werner. Evaluation and management of paravalvular aortic regurgitation after transcatheter aortic valve replacement. J. Am. Coll. Cardiol. 62:11–20, 2013.CrossRefPubMedGoogle Scholar
  28. 28.
    Stout, K. K., and E. D. Verrier. Acute valvular regurgitation. Circulation 119:3232–3241, 2009.CrossRefPubMedGoogle Scholar
  29. 29.
    Stugaard, M., H. Koriyama, K. Katsuki, K. Masuda, T. Asanuma, Y. Takeda, Y. Sakata, K. Itatani, and S. Nakatani. Energy loss in the left ventricle obtained by vector flow mapping as a new quantitative measure of severity of aortic regurgitation: a combined experimental and clinical study. Eur. Hear. J. Cardiovasc. Imaging 16:723–730, 2015.CrossRefGoogle Scholar
  30. 30.
    Uejima, T., A. Koike, H. Sawada, T. Aizawa, S. Ohtsuki, M. Tanaka, T. Furukawa, and A. G. Fraser. A new echocardiographic method for identifying vortex flow in the left ventricle: numerical validation. Ultrasound Med. Biol. 36:772–788, 2010.CrossRefPubMedGoogle Scholar
  31. 31.
    Uretsky, S., A. Supariwala, P. Nidadovolu, S. S. Khokhar, C. Comeau, O. Shubayev, F. Campanile, and S. D. Wolff. Quantification of left ventricular remodeling in response to isolated aortic or mitral regurgitation. J. Cardiovasc. Magn. Reson. 12:32, 2010.CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Welch, G. H., E. Braunwald, and S. J. Sarnoff. Hemodynamic effects of quantitatively varied experimental aortic regurgitation. Circ. Res. 5:546–551, 1957.CrossRefPubMedGoogle Scholar
  33. 33.
    Wittlinger, T., O. Dzemali, F. Bakhtiary, A. Moritz, and P. Kleine. Hemodynamic evaluation of aortic regurgitation by magnetic resonance imaging. Asian Cardiovasc. Thorac. Ann. 16:278–283, 2008.CrossRefPubMedGoogle Scholar

Copyright information

© Biomedical Engineering Society 2017

Authors and Affiliations

  • Ikechukwu Okafor
    • 1
    • 2
  • Vrishank Raghav
    • 3
    • 4
  • Jose F. Condado
    • 5
  • Prem A. Midha
    • 6
  • Gautam Kumar
    • 5
    • 7
  • Ajit P. Yoganathan
    • 1
    • 3
    Email author
  1. 1.School of Chemical and Biomolecular EngineeringGeorgia Institute of TechnologyAtlantaUSA
  2. 2.Exponent Failure Analysis AssociatesPhiladelphiaUSA
  3. 3.Wallace H. Coulter Department of Biomedical Engineering, Georgia Institute of Technology and Emory UniversityAtlantaUSA
  4. 4.Department of Aerospace EngineeringAuburn UniversityAuburnUSA
  5. 5.Division of CardiologyEmory University HospitalAtlantaUSA
  6. 6.Woodruff School of Mechanical Engineering, Georgia Institute of TechnologyAtlantaUSA
  7. 7.Atlanta Veterans Affairs Medical CenterDecaturUSA

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