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Annals of Biomedical Engineering

, Volume 38, Issue 2, pp 380–390 | Cite as

Hemodynamics of the Normal Aorta Compared to Fusiform and Saccular Abdominal Aortic Aneurysms with Emphasis on a Potential Thrombus Formation Mechanism

  • Jacopo Biasetti
  • T. Christian GasserEmail author
  • Martin Auer
  • Ulf Hedin
  • Fausto Labruto
Article

Abstract

Abdominal Aortic Aneurysms (AAAs), i.e., focal enlargements of the aorta in the abdomen are frequently observed in the elderly population and their rupture is highly mortal. An intra-luminal thrombus is found in nearly all aneurysms of clinically relevant size and multiply affects the underlying wall. However, from a biomechanical perspective thrombus development and its relation to aneurysm rupture is still not clearly understood. In order to explore the impact of blood flow on thrombus development, normal aortas (n = 4), fusiform AAAs (n = 3), and saccular AAAs (n = 2) were compared on the basis of unsteady Computational Fluid Dynamics simulations. To this end patient-specific luminal geometries were segmented from Computerized Tomography Angiography data and five full heart cycles using physiologically realistic boundary conditions were analyzed. Simulations were carried out with computational grids of about half a million finite volume elements and the Carreau–Yasuda model captured the non-Newtonian behavior of blood. In contrast to the normal aorta the flow in aneurysm was highly disturbed and, particularly right after the neck, flow separation involving regions of high streaming velocities and high shear stresses were observed. Naturally, at the expanded sites of the aneurysm average flow velocity and wall shear stress were much lower compared to normal aortas. These findings suggest platelets activation right after the neck, i.e., within zones of pronounced recirculation, and platelet adhesion, i.e., thrombus formation, downstream. This mechanism is supported by recirculation zones promoting the advection of activated platelets to the wall.

Keywords

Intra-luminal thrombus Aortic aneurysm Computational Fluid Dynamics Saccular Fusiform Aorta 

Notes

Acknowledgments

We’d like to thank Dr. Piergiorgio Spazzini (INRiM, Italy) for all the helpful discussions about solving procedure and data analysis. This work has been supported by the Young Faculty Grant No. 2006-7568 provided by the Swedish Research Council, VINNOVA and the Swedish Foundation for Strategic Research, and the EC Seventh Framework Programme, Fighting Aneurysmal Disease (FAD-200647) which is gratefully acknowledged.

References

  1. 1.
    Auer, M., and T. C. Gasser. Reconstruction and finite element mesh generation of abdominal aortic aneurysms from computerized tomography angiography data with minimal user interaction. IEEE T. Med. Imaging 2009 (submitted).Google Scholar
  2. 2.
    Bird, R. B., R. C. Armstrong, and O. Hassager. Dynamics of Polymeric Liquids, Vol. 1. Fluid Mechanics. New York: Wiley, 1987.Google Scholar
  3. 3.
    Bluestein, D., L. Niu, R. T. Schoephoerster, and M. K. Dewanjee. Steady flow in an aneurysm model: correlation between fluid dynamics and blood platelet deposition. J. Biomed. Eng. 118:280–286, 1996.Google Scholar
  4. 4.
    Bluestein, D., L. Niu, R. Schoephoerster, and M. K. Dewanjee. Fluid mechanics of arterial stenosis: relationship to the development of mural thrombus. Ann. Biomed. Eng. 25:344–356, 1997.CrossRefPubMedGoogle Scholar
  5. 5.
    Carmo, M., L. Colombo, A. Bruno, F. R. Corsi, L. Roncoroni, M. S. Cuttin, F. Radice, E. Mussini, and P. G. Settembrini. Alteration of elastin, collagen and their cross-links in abdominal aortic aneurysms. Eur. J. Vasc. Endovasc. Surg. 23:543–549, 2002.CrossRefPubMedGoogle Scholar
  6. 6.
    Chen, J., X. Lu, and W. Wang. Non-newtonian effects of blood flow on hemodynamics in distal vascular graft anastomoses. J. Biomech. 39:1983–1995, 2006.CrossRefGoogle Scholar
  7. 7.
    Choke, E., G. Cockerill, W. R. Wilson, S. Sayed, J. Dawson, I. Loftus, and M. M. Thompson. A review of biological factors implicated in abdominal aortic aneurysm rupture. Eur. J. Vasc. Endovasc. Surg. 30:227–244, 2005.CrossRefGoogle Scholar
  8. 8.
    di Martino, E. S., S. Mantero, F. Inzoli, G. Melissano, D. Astore, R. Chiesa, and R. Fumero. Biomechanics of abdominal aortic aneurysm in the presence of endoluminal thrombus: experimental characterization and structural static computational analysis. Eur. J. Vasc. Endovasc. Surg. 15:290–299, 1998.CrossRefGoogle Scholar
  9. 9.
    Fillinger, M. F., M. L. Raghavanand, S. P. Marra, J.-L. Cronenwett, and F. E. Kennedy. In vivo analysis of mechanical wall stress and abdominal aortic aneurysm rupture risk. J. Vasc. Surg. 36:589–597, 2002.CrossRefPubMedGoogle Scholar
  10. 10.
    Fleming, C., E. P. Whitlock, T. Beil, and F. A. Lederle. Review: screening for abdominal aortic aneurysm: a best-evidence systematic review for the U.S. preventive services task force. Ann. Intern. Med. 142:203–211, 2005.Google Scholar
  11. 11.
    Gasser, T. C., G. Görgülü, M. Folkesson, and J. Swedenborg. Failure properties of intraluminal thrombus in abdominal aortic aneurysm under static and pulsating mechanical loads. J. Vasc. Surg. 48:179–188, 2008.CrossRefGoogle Scholar
  12. 12.
    Gasser, T. C., P. Gudmundson, and G. Dohr. Failure mechanisms of ventricular tissue due to deep penetration. J. Biomech. 42:626–633, 2009.CrossRefGoogle Scholar
  13. 13.
    Gijsen, F. J. H., E. Allanic, F. N. van de Vosse, and J. D. Janssen. The influence of the non-Newtonian properties of blood on the flow in large arteries: unsteady flow in a 90° curved tube. J. Biomech. 32:705–713, 1999.CrossRefGoogle Scholar
  14. 14.
    Hans, S. S., O. Jareunpoon, M. Balasubramaniam, and G. B. Zelenock. Size and location of thrombus in intact and ruptured abdominal aortic aneurysms. J. Vasc. Surg. 41:584–588, 2005.CrossRefGoogle Scholar
  15. 15.
    Hellums, J. D. 1993 Whitaker lecture: biorheology in thrombosis research. Ann. Biomed. Eng. 22:445–455, 1994.CrossRefGoogle Scholar
  16. 16.
    Heng, M. S., M. J. Fagan, J. W. Collier, G. Desai, P. T. McCollum, and I. C. Chetter. Peak wall stress measurement in elective and acute abdominal aortic aneurysms. J. Vasc. Surg. 47:17–22, 2008.CrossRefGoogle Scholar
  17. 17.
    Humphrey, J. D., and C. A. Taylor. Intracranial and abdominal aortic aneurysms: similarities, differences, and need for a new class of computational models. Ann. Biomed. Eng. 10:221–246, 2008.CrossRefGoogle Scholar
  18. 18.
    Inzoli, F., F. Boschetti, M. Zappa, T. Longo, and R. Fumero. Biomechanical factors in abdominal aortic aneurysm rupture. Eur. J. Vasc. Surg. 7:667–674, 1993.CrossRefGoogle Scholar
  19. 19.
    Kazi, M., J. Thyberg, P. Religa, J. Roy, P. Eriksson, U. Hedin, and J. Swedenborg. Influence of intraluminal thrombus on structural and cellular composition of abdominal aortic aneurysm wall. J. Vasc. Surg. 38:1283–1292, 2003.CrossRefGoogle Scholar
  20. 20.
    Kazi, M., C. Zhu, J. Roy, G. Paulsson-Berne, A. Hamsten, J. Swedenborg, U. Hedin, and P. Eriksson. Difference in matrix-degrading protease expression and activity between thrombus-free and thrombus-covered wall of abdominal aortic aneurysm. Arterioscler. Thromb. Vasc. Biol. 25:1341–1346, 2005.CrossRefPubMedGoogle Scholar
  21. 21.
    Länne, T., B. Sonesson, D. Bergqvist, H. Bengtsson, and D. Gustafsson. Diameter and compliance in the male human abdominal aorta: influence of age and aortic aneurysm. Eur. J. Vasc. Surg. 6:178–184, 1992.CrossRefGoogle Scholar
  22. 22.
    Leung, J. H., A. R. Wright, N. Cheshire, J. Crane, S. A. Thom, A. D. Hughes, and Y. Xu. Fluid structure interaction of patient specific abdominal aortic aneurysms: a comparison with solid stress models. Biomed. Eng. Online 5–33, 2006.Google Scholar
  23. 23.
    Li, Z., and C. Kleinstreuer. Computational analysis of type II endoleaks in a stented abdominal aortic aneurysm model. J. Biomech. 2005.Google Scholar
  24. 24.
    Li, Z., and C. Kleinstreuer. A comparison between different asymmetric abdominal aortic aneurysm morphologies employing computational fluid-structure interaction analysis. Eur. J. Mech. B/Fluids 26:615–631, 2007.CrossRefGoogle Scholar
  25. 25.
    Li, Z.-Y., J. U-King-Im, T. Y. Tang, E. Soh, T. C. See, and J. H. Gillard. Impact of calcification and intraluminal thrombus on the computed wall stresses of abdominal aortic aneurysm. J. Vasc. Surg. 47:928–935, 2008.CrossRefPubMedGoogle Scholar
  26. 26.
    Long, A., L. Rouet, A. Bissery, P. Rossignol, D. Mouradian, and M. Sapoval. Compliance of abdominal aortic aneurysms: evaluation of tissue doppler imaging. Ultrasound Med. Biol. 30:1099–1108, 2004.CrossRefPubMedGoogle Scholar
  27. 27.
    Macedo, T. A., A. W. Stanson, G. S. Oderich, C. M. Johnson, J. M. Panneton, and M. L. Tie. Infected aortic aneurysms: imaging findings. Radiology 231:250–257, 2004.CrossRefPubMedGoogle Scholar
  28. 28.
    Malvern, L. E. Introduction to the Mechanics of a Continuous Medium. Englewood Cliffs, NJ: Prentice-Hall, 1969.Google Scholar
  29. 29.
    Mills, C., I. Gabe, J. Gault, D. Mason, J. Ross, E. Braunwald, et al. Pressure-flow relationships and vascular impedance in man. Cardiovasc. Res. 4:405–417, 1970.CrossRefPubMedGoogle Scholar
  30. 30.
    Mower, W. R., W. J. Quiñones, and S. S. Gambhir. Effect of intraluminal thrombus on abdominal aortic aneurysm wall stress. J. Vasc. Surg. 33:602–608, 1997.CrossRefGoogle Scholar
  31. 31.
    Prakash, S., and C. R. Ethier. Requirements for mesh resolution in 3D computational hemodynamics. J. Biomech. Eng. 123:134–144, 2001.CrossRefGoogle Scholar
  32. 32.
    Raz, S., S. Einav, Y. Alemu, and D. Bluestein. DPIV prediction of flow induced platelet activation—comparison to numerical predictions. Ann. Biomed. Eng. 35:493–504, 2007.CrossRefGoogle Scholar
  33. 33.
    Richardson, P. D. Biomechanics of plaque rupture: progress, problems, and new frontiers. Ann. Biomed. Eng. 30:524–536, 2002.CrossRefGoogle Scholar
  34. 34.
    Rissland, P., Y. Alemu, S. Einav, J. Ricotta, and D. Bluestein. Abdominal aortic aneurysm risk of rupture: patient-specific FSI simulations using anisotropic model. J. Biomech. Eng. 131, 2009 (online).Google Scholar
  35. 35.
    Sack, J.-R., and J. Urrutia, editors. Handbook of Computational Geometry. Amsterdam: Elsevier, 2000.Google Scholar
  36. 36.
    Scotti, C. M., and E. A. Finol. Compliant biomechanics of abdominal aortic aneurysms: a fluid-structure interaction study. Comput. Struct. 85:1097–1113, 2007.CrossRefGoogle Scholar
  37. 37.
    Steinman, D. A., D. A. Vorp, and C. R. Ethier. Computational modeling of arterial biomechanics: insights into pathogenesis and treatment of vascular disease. J. Vasc. Res. 37:1118–1128, 2003.Google Scholar
  38. 38.
    Stenbaek, J., B. Kalin, and J. Swedenborg. Growth of thrombus may be a better predictor of rupture than diameter in patients with abdominal aortic aneurysms. Eur. J. Vasc. Endovasc. Surg. 20:466–499, 2000.CrossRefGoogle Scholar
  39. 39.
    Swedenborg, J., and P. Eriksson. The intraluminal thrombus as a source of proteolytic activity. Ann. N.Y. Acad. Sci. 1085:133–138, 2006.CrossRefGoogle Scholar
  40. 40.
    Taylor, R. L. FEAP—A Finite Element Analysis Program, Version 7.4 User Manual. Berkeley, California: University of California at Berkeley, 2002.Google Scholar
  41. 41.
    Upchurch Jr., G. R., and T. A. Schaub. Abdominal aortic aneurysm. Am. Fam. Physician 73:1198–1204, 2006.Google Scholar
  42. 42.
    van Dam, E. A., S. D. Dams, G. W. M. Peters, M. C. M. Rutten, G. W. H. Schurink, J. Buth, and F. N. van de Vosse. Non-linear viscoelastic behavior of abdominal aortic aneurysm thrombus. Biomech. Model. Mechanobiol. 7:127–137, 2007.PubMedGoogle Scholar
  43. 43.
    Vande Geest, J. P., M. S. Sacks, and D. A. Vorp. A planar biaxial constitutive relation for the luminal layer of intra-luminal thrombus in abdominal aortic aneurysms. J. Biomech. 39:2347–2354, 2006.CrossRefGoogle Scholar
  44. 44.
    Venkatasubramaniam, A. K., M. J. Fagan, T. Mehta, K. J. Mylankal, B. Ray, G. Kuhan, I. C. Chetter, and P. T. McCollum. A comparative study of aortic wall stress using finite element analysis for ruptured and non-ruptured abdominal aortic aneurysms. Eur. J. Vasc. Surg. 28:168–176, 2004.Google Scholar
  45. 45.
    Vorp, D. A., P. C. Lee, D. H. Wang, M. S. Makaroun, E. M. Nemoto, S. Ogawa, and M. W. Webster. Association of intraluminal thrombus in abdominal aortic aneurysm with local hypoxia and wall weakening. J. Vasc. Surg. 34:291–299, 2001.CrossRefGoogle Scholar
  46. 46.
    Vorp, D. A., W. A. Mandarino, M. W. Webster, and J. Gorcsan. Potential influence of intraluminal thrombus on abdominal aortic aneurysm as assessed by a new non-invasive method. Cardiovasc. Surg. 4:732–739, 1996.CrossRefPubMedGoogle Scholar
  47. 47.
    Wang, D. H., M. S. Makaroun, M. W. Webster, and D. A. Vorp. Mechanical properties and microstructure of intraluminal thrombus from abdominal aortic aneurysm. J. Biomech. Eng. 123:536–539, 2001.CrossRefPubMedGoogle Scholar
  48. 48.
    Wang, D. H., M. S. Makaroun, M. W. Webster, and D. A. Vorp. Effect of intraluminal thrombus on wall stress in patient-specific models of abdominal aortic aneurysm. J. Vasc. Surg. 36:598–604, 2002.CrossRefGoogle Scholar
  49. 49.
    Wolters, B. J. B. M., M. C. M. Rutten, G. W. H. Schurink, U. Kose, J. de Hart, and F. N. van de Vosse. A patient-specific computational model of fluid-structure interaction in abdominal aortic aneurysms. Med. Eng. Phys. 27:871–883, 2005.CrossRefGoogle Scholar
  50. 50.
    Wootton, D. M., and D. N. Ku. Fluid mechanics of vascular systems, diseases, and thrombosis. Ann. Rev. Biomed. Eng. 1:299–329, 1999.CrossRefGoogle Scholar
  51. 51.
    Xu, C., D. L. Pham, and J. L. Prince. Image segmentation using deformable models. In: Handbook of Medical Imaging. Volume 2. Medical Image Processing and Analysis, edited by M. Sonka and J. M. Fitzpatrick. Bellingham: Spie press, 2000, pp. 129–174.Google Scholar

Copyright information

© Biomedical Engineering Society 2009

Authors and Affiliations

  • Jacopo Biasetti
    • 1
  • T. Christian Gasser
    • 1
    Email author
  • Martin Auer
    • 2
  • Ulf Hedin
    • 3
  • Fausto Labruto
    • 4
  1. 1.Department of Solid MechanicsRoyal Institute of Technology (KTH)StockholmSweden
  2. 2.VASCOPS GmbHGrazAustria
  3. 3.Department of Molecular Medicine and SurgeryKarolinska University HospitalStockholmSweden
  4. 4.Department of RadiologyKarolinska University HospitalStockholmSweden

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