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Quantification of Hemodynamics in Abdominal Aortic Aneurysms During Rest and Exercise Using Magnetic Resonance Imaging and Computational Fluid Dynamics

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Abstract

Abdominal aortic aneurysms (AAAs) affect 5–7% of older Americans. We hypothesize that exercise may slow AAA growth by decreasing inflammatory burden, peripheral resistance, and adverse hemodynamic conditions such as low, oscillatory shear stress. In this study, we use magnetic resonance imaging and computational fluid dynamics to describe hemodynamics in eight AAAs during rest and exercise using patient-specific geometric models, flow waveforms, and pressures as well as appropriately resolved finite-element meshes. We report mean wall shear stress (MWSS) and oscillatory shear index (OSI) at four aortic locations (supraceliac, infrarenal, mid-aneurysm, and suprabifurcation) and turbulent kinetic energy over the entire computational domain on meshes containing more than an order of magnitude more elements than previously reported results (mean: 9.0-million elements; SD: 2.3 M; range: 5.7–12.0 M). MWSS was lowest in the aneurysm during rest 2.5 dyn/cm2 (SD: 2.1; range: 0.9–6.5), and MWSS increased and OSI decreased at all four locations during exercise. Mild turbulence existed at rest, while moderate aneurysmal turbulence was present during exercise. During both rest and exercise, aortic turbulence was virtually zero superior to the AAA for seven out of eight patients. We postulate that the increased MWSS, decreased OSI, and moderate turbulence present during exercise may attenuate AAA growth.

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Abbreviations

AAA:

Abdominal aortic aneurysm

DBP:

Diastolic blood pressure

IR:

Infrarenal

Mid-An:

Mid-aneurysm

MRI:

Magnetic resonance imaging

MWSS:

Mean wall shear stress

OSI:

Oscillatory shear index

SB:

Suprabifurcation

SBP:

Systolic blood pressure

SC:

Supraceliac

TKE:

Turbulent kinetic energy

References

  1. Allardice, J. T., G. J. Allwright, J. M. Wafula, and A. P. Wyatt. High prevalence of abdominal aortic aneurysm in men with peripheral vascular disease: screening by ultrasonography. Brit. J. Surg. 75:240–242, 1988.

    Article  CAS  PubMed  Google Scholar 

  2. Asbury, C. L., J. W. Ruberti, E. I. Bluth, and R. A. Peattie. Experimental investigation of steady flow in rigid models of abdominal aortic aneurysms. Ann. Biomed. Eng. 23:29–39, 1995.

    Article  CAS  PubMed  Google Scholar 

  3. Bax, L., C. J. Bakker, W. M. Klein, N. Blanken, J. J. Beutler, and W. P. Mali. Renal blood flow measurements with use of phase-contrast magnetic resonance imaging: normal values and reproducibility. J. Vasc. Interv. Radiol. 16:807–814, 2005.

    PubMed  Google Scholar 

  4. Berguer, R., J. L. Bull, and K. Khanafer. Refinements in mathematical models to predict aneurysm growth and rupture. Ann. N.Y. Acad. Sci. 1085:110–116, 2006.

    Article  PubMed  Google Scholar 

  5. 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. Biomech. Eng. 118:280–286, 1996.

    Article  CAS  PubMed  Google Scholar 

  6. Bluth, E. I., S. M. Murphey, L. H. Hollier, and M. A. Sullivan. Color flow doppler in the evaluation of aortic aneurysms. Int. Angiol. 9:8–10, 1990.

    CAS  PubMed  Google Scholar 

  7. Boussel, L., V. Rayz, C. McCulloch, A. Martin, G. Acevedo-Bolton, M. Lawton, R. Higashida, W. S. Smith, W. L. Young, and D. Saloner. Aneurysm growth occurs at region of low wall shear stress: patient-specific correlation of hemodynamics and growth in a longitudinal study. Stroke 39:2997–3002, 2008.

    Article  PubMed  Google Scholar 

  8. Brady, A. R., S. G. Thompson, F. G. Fowkes, R. M. Greenhalgh, and J. T. Powell. Abdominal aortic aneurysm expansion: risk factors and time intervals for surveillance. Circulation 110:16–21, 2004.

    Article  PubMed  Google Scholar 

  9. Brewster, D. C., J. L. Cronenwett, J. W. Hallett, Jr., K. W. Johnston, W. C. Krupski, and J. S. Matsumura. Guidelines for the treatment of abdominal aortic aneurysms. Report of a subcommittee of the joint council of the american association for vascular surgery and society for vascular surgery. J. Vasc. Surg. 37:1106–1117, 2003.

    Article  PubMed  Google Scholar 

  10. Cheng, C. P., R. J. Herfkens, and C. A. Taylor. Abdominal aortic hemodynamic conditions in healthy subjects aged 50–70 at rest and during lower limb exercise: in vivo quantification using mri. Atherosclerosis 168:323–331, 2003.

    Article  CAS  PubMed  Google Scholar 

  11. Cornhill, J. F., E. E. Herderick, and H. C. Stary. Topography of human aortic sudanophilic lesions. Monogr. Atheroscler. 15:13–19, 1990.

    CAS  PubMed  Google Scholar 

  12. Curci, J. A., and R. W. Thompson. Adaptive cellular immunity in aortic aneurysms: cause, consequence, or context? J. Clin. Invest. 114:168–171, 2004.

    CAS  PubMed  Google Scholar 

  13. Dalman, R. L., M. M. Tedesco, J. Myers, and C. A. Taylor. AAA disease: mechanism, stratification, and treatment. Ann. N.Y. Acad. Sci. 1085:92–109, 2006.

    Article  PubMed  Google Scholar 

  14. Draney, M. T., M. T. Alley, B. T. Tang, N. M. Wilson, R. J. Herfkens, and C. A. Taylor. Importance of 3d nonlinear gradient corrections for quantitative analysis of 3d mr angiographic data. In: International Society for Magnetic Resonance in Medicine, Honolulu, HI, 2002.

  15. Egelhoff, C. J., R. S. Budwig, D. F. Elger, T. A. Khraishi, and K. H. Johansen. Model studies of the flow in abdominal aortic aneurysms during resting and exercise conditions. J. Biomech. 32:1319–1329, 1999.

    Article  CAS  PubMed  Google Scholar 

  16. Finol, E. A., K. Keyhani, and C. H. Amon. The effect of asymmetry in abdominal aortic aneurysms under physiologically realistic pulsatile flow conditions. J. Biomech. Eng. 125:207–217, 2003.

    Article  CAS  PubMed  Google Scholar 

  17. Fleming, C., E. P. Whitlock, T. L. Beil, and F. A. Lederle. Screening for abdominal aortic aneurysm: a best-evidence systematic review for the us preventive services task force. Ann. Intern. Med. 142:203–211, 2005.

    PubMed  Google Scholar 

  18. Gillum, R. F. Epidemiology of aortic aneurysm in the United States. J. Clin. Epidemiol. 48:1289–1298, 1995.

    Article  CAS  PubMed  Google Scholar 

  19. Hance, K. A., M. Tataria, S. J. Ziporin, J. K. Lee, and R. W. Thompson. Monocyte chemotactic activity in human abdominal aortic aneurysms: role of elastin degradation peptides and the 67-kd cell surface elastin receptor. J. Vasc. Surg. 35:254–261, 2002.

    Article  PubMed  Google Scholar 

  20. He, X., and D. N. Ku. Pulsatile flow in the human left coronary artery bifurcation: average conditions. J. Biomech. Eng. 118:74–82, 1996.

    Article  CAS  PubMed  Google Scholar 

  21. Holenstein, R., and D. N. Ku. Reverse flow in the major infrarenal vessels—a capacitive phenomenon. Biorheology 25:835–842, 1988.

    CAS  PubMed  Google Scholar 

  22. Hope, S. A., D. B. Tay, I. T. Meredith, and J. D. Cameron. Waveform dispersion, not reflection, may be the major determinant of aortic pressure wave morphology. Am. J. Physiol. Heart Circul. Physiol. 289:H2497–H2502, 2005.

    Article  CAS  Google Scholar 

  23. Hoshina, K., E. Sho, M. Sho, T. K. Nakahashi, and R. L. Dalman. Wall shear stress and strain modulate experimental aneurysm cellularity. J. Vasc. Surg. 37:1067–1074, 2003.

    PubMed  Google Scholar 

  24. Hughes, T. J. The Finite Element Method: Linear Static and Dynamic Finite Element Analysis. Mineola, NY: Dover Publications, 107 pp., 2000.

  25. Humphrey, J. D., and C. A. Taylor. Intracranial and abdominal aortic aneurysms: similarities, differences, and need for a new class of computational models. Annu. Rev. Biomed. Eng. 10:221–246, 2008.

    Article  CAS  PubMed  Google Scholar 

  26. Khanafer, K. M., J. L. Bull, G. R. Upchurch, Jr., and R. Berguer. Turbulence significantly increases pressure and fluid shear stress in an aortic aneurysm model under resting and exercise flow conditions. Ann. Vasc. Surg. 21:67–74, 2007.

    Article  PubMed  Google Scholar 

  27. Khanafer, K. M., P. Gadhoke, R. Berguer, and J. L. Bull. Modeling pulsatile flow in aortic aneurysms: effect of non-newtonian properties of blood. Biorheology 43:661–679, 2006.

    PubMed  Google Scholar 

  28. Kim, H. J., C. A. Figueroa, T. J. R. Hughes, K. E. Jansen, and C. A. Taylor. Augmented lagrangian method for constraining the shape of velocity profiles at outlet boundaries for three-dimensional finite element simulations of blood flow. Comput. Meth. Appl. Mech. Eng. 198:3551–3566, 2009.

    Article  Google Scholar 

  29. Koch, A. E., S. L. Kunkel, W. H. Pearce, M. R. Shah, D. Parikh, H. L. Evanoff, G. K. Haines, M. D. Burdick, and R. M. Strieter. Enhanced production of the chemotactic cytokines interleukin-8 and monocyte chemoattractant protein-1 in human abdominal aortic aneurysms. Am. J. Pathol. 142:1423–1431, 1993.

    CAS  PubMed  Google Scholar 

  30. Laskey, W. K., H. G. Parker, V. A. Ferrari, W. G. Kussmaul, and A. Noordergraaf. Estimation of total systemic arterial compliance in humans. J. Appl. Physiol. 69:112–119, 1990.

    CAS  PubMed  Google Scholar 

  31. Lederle, F. A., G. R. Johnson, S. E. Wilson, E. P. Chute, R. J. Hye, M. S. Makaroun, G. W. Barone, D. Bandyk, G. L. Moneta, and R. G. Makhoul. The aneurysm detection and management study screening program: validation cohort and final results. Aneurysm detection and management veterans affairs cooperative study investigators. Arch. Intern. Med. 160:1425–1430, 2000.

    Article  CAS  PubMed  Google Scholar 

  32. Long, A., L. Rouet, F. Vitry, J. N. Albertini, C. Marcus, and C. Clement. Compliance of abdominal aortic aneurysms before and after stenting with tissue Doppler imaging: evolution during follow-up and correlation with aneurysm diameter. Ann. Vasc. Surg. 23:49–59, 2009.

    Article  PubMed  Google Scholar 

  33. Miller, Jr., F. J., W. J. Sharp, X. Fang, L. W. Oberley, T. D. Oberley, and N. L. Weintraub. Oxidative stress in human abdominal aortic aneurysms: a potential mediator of aneurysmal remodeling. Arterioscler. Thromb. Vasc. Biol. 22:560–565, 2002.

    Article  CAS  PubMed  Google Scholar 

  34. Montain, S. J., S. M. Jilka, A. A. Ehsani, and J. M. Hagberg. Altered hemodynamics during exercise in older essential hypertensive subjects. Hypertension 12:479–484, 1988.

    CAS  PubMed  Google Scholar 

  35. Moore, Jr., J. E., and D. N. Ku. Pulsatile velocity measurements in a model of the human abdominal aorta under resting conditions. J. Biomech. Eng. 116:337–346, 1994.

    Article  PubMed  Google Scholar 

  36. Moore, Jr., 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 110:225–240, 1994.

    Article  CAS  PubMed  Google Scholar 

  37. Muller, J., O. Sahni, X. Li, K. E. Jansen, M. S. Shephard, and C. A. Taylor. Anisotropic adaptive finite element method for modelling blood flow. Comput. Meth. Biomech. Biomed. Eng. 8:295–305, 2005.

    CAS  Google Scholar 

  38. Myers, J., M. Prakash, V. Froelicher, D. Do, S. Partington, and J. E. Atwood. Exercise capacity and mortality among men referred for exercise testing. N. Engl. J. Med. 346:793–801, 2002.

    Article  PubMed  Google Scholar 

  39. Nakahashi, T. K., K. Hoshina, P. S. Tsao, E. Sho, M. Sho, J. K. Karwowski, C. Yeh, R. B. Yang, J. N. Topper, and R. L. Dalman. Flow loading induces macrophage antioxidative gene expression in experimental aneurysms. Arterioscler. Thromb. Vasc. Biol. 22:2017–2022, 2002.

    Article  CAS  PubMed  Google Scholar 

  40. Newman, K. M., J. Jean-Claude, H. Li, W. G. Ramey, and M. D. Tilson. Cytokines that activate proteolysis are increased in abdominal aortic aneurysms. Circulation 90:II224–II227, 1994.

    CAS  PubMed  Google Scholar 

  41. Nichols, W. W., and M. F. O’Rourke. Mcdonald’s Blood Flow in Arteries (4th ed.). New York: Oxford University Press, 179 pp., 1998.

  42. Peattie, R. A., T. J. Riehle, and E. I. Bluth. Pulsatile flow in fusiform models of abdominal aortic aneurysms: flow fields, velocity patterns and flow-induced wall stresses. J. Biomech. Eng. 126:438–446, 2004.

    Article  PubMed  Google Scholar 

  43. Perktold, K., R. O. Peter, M. Resch, and G. Langs. Pulsatile non-newtonian blood flow in three-dimensional carotid bifurcation models: a numerical study of flow phenomena under different bifurcation angles. J. Biomed. Eng. 13:507–515, 1991.

    Article  CAS  PubMed  Google Scholar 

  44. Perktold, K., and G. Rappitsch. Computer simulation of local blood flow and vessel mechanics in a compliant carotid artery bifurcation model. J. Biomech. 28:845–856, 1995.

    Article  CAS  PubMed  Google Scholar 

  45. Rayz, V. L., L. Boussel, M. T. Lawton, G. Acevedo-Bolton, L. Ge, W. L. Young, R. T. Higashida, and D. Saloner. Numerical modeling of the flow in intracranial aneurysms: prediction of regions prone to thrombus formation. Ann. Biomed. Eng. 36:1793–1804, 2008.

    Article  CAS  PubMed  Google Scholar 

  46. Sallam, A. M., and N. H. C. Hwang. Human red blood-cell hemolysis in a turbulent shear-flow—contribution of Reynolds shear stresses. Biorheology 21:783–797, 1984.

    CAS  PubMed  Google Scholar 

  47. Salsac, A. V., S. R. Sparks, J. M. Chomaz, and J. C. Lasheras. Evolution of the wall shear stresses during the progressive enlargement of symmetric abdominal aortic aneurysms. J. Fluid Mech. 560:19–51, 2006.

    Article  Google Scholar 

  48. Salsac, A. V., S. R. Sparks, and J. C. Lasheras. Hemodynamic changes occurring during the progressive enlargement of abdominal aortic aneurysms. Ann. Vasc. Surg. 18:14–21, 2004.

    Article  PubMed  Google Scholar 

  49. Santilli, J. D., and S. M. Santilli. Diagnosis and treatment of abdominal aortic aneurysms. Am. Fam. Physician 56:1081–1090, 1997.

    CAS  PubMed  Google Scholar 

  50. Sergeev, S. I. Fluid oscillations in pipes at moderate Reynolds numbers. Fluid Dyn. 1:21–22, 1966.

    Google Scholar 

  51. Steele, B. N., M. S. Olufsen, and C. A. Taylor. Fractal network model for simulating abdominal and lower extremity blood flow during resting and exercise conditions. Comput. Meth. Biomech. Biomed. Eng. 10:39–51, 2007.

    Article  Google Scholar 

  52. Stergiopulos, N., P. Segers, and N. Westerhof. Use of pulse pressure method for estimating total arterial compliance in vivo. Am. J. Physiol. Heart Circul. Physiol. 276:H424–H428, 1999.

    CAS  Google Scholar 

  53. Tang, B. T., C. P. Cheng, M. T. Draney, N. M. Wilson, P. S. Tsao, R. J. Herfkens, and C. A. Taylor. Abdominal aortic hemodynamics in young healthy adults at rest and during lower limb exercise: quantification using image-based computer modeling. Am. J. Physiol. Heart Circul. Physiol. 291:H668–H676, 2006.

    Article  CAS  Google Scholar 

  54. Taylor, C. A., C. P. Cheng, L. A. Espinosa, B. T. Tang, D. Parker, and R. J. Herfkens. In vivo quantification of blood flow and wall shear stress in the human abdominal aorta during lower limb exercise. Ann. Biomed. Eng. 30:402–408, 2002.

    Article  PubMed  Google Scholar 

  55. Taylor, C. A., and M. T. Draney. Experimental and computational methods in cardiovascular fluid mechanics. Annu. Rev. Fluid Mech. 36:197–231, 2004.

    Article  Google Scholar 

  56. Taylor, C. A., T. J. R. Hughes, and C. K. Zarins. Finite element modeling of three-dimensional pulsatile flow in the abdominal aorta: relevance to atherosclerosis. Ann. Biomed. Eng. 26:975–987, 1998.

    Article  CAS  PubMed  Google Scholar 

  57. Taylor, C. A., and D. A. Steinman. Image-based modeling of blood flow and vessel wall dynamics: applications, methods and future directions. Ann. Biomed. Eng., 2010. doi:10.1007/s10439-010-9901-0.

  58. Taylor, T. W., and T. Yamaguchi. Three-dimensional simulation of blood flow in an abdominal aortic aneurysm—steady and unsteady flow cases. J. Biomech. Eng. 116:89–97, 1994.

    Article  CAS  PubMed  Google Scholar 

  59. Thompson, R. W., D. R. Holmes, R. A. Mertens, S. Liao, M. D. Botney, R. P. Mecham, H. G. Welgus, and W. C. Parks. Production and localization of 92-kilodalton gelatinase in abdominal aortic aneurysms. An elastolytic metalloproteinase expressed by aneurysm-infiltrating macrophages. J. Clin. Invest. 96:318–326, 1995.

    Article  CAS  PubMed  Google Scholar 

  60. van der Molen, A. J. Nephrogenic systemic fibrosis and the role of gadolinium contrast media. J. Med. Imaging Radiat. Oncol. 52:339–350, 2008.

    Article  PubMed  Google Scholar 

  61. Vignon-Clementel, I. E., C. A. Figueroa, K. C. Jansen, and C. A. Taylor. Outflow boundary conditions for three-dimensional finite element modeling of blood flow and pressure in arteries. Comput. Meth. Appl. Mech. Eng. 195:3776–3796, 2006.

    Google Scholar 

  62. Vignon-Clementel, I. E., C. A. Figueroa, K. E. Jensen, and C. A. Taylor. Outflow boundary conditions for three-dimensional simulations of non-periodic blood flow and pressure fields in deformable arteries. Comput. Meth. Biomech. Biomed. Eng., 2009 (in press).

  63. Vollmar, J. F., E. Paes, P. Pauschinger, E. Henze, and A. Friesch. Aortic aneurysms as late sequelae of above-knee amputation. Lancet 2:834–835, 1989.

    Article  CAS  PubMed  Google Scholar 

  64. Whiting, C. H., and K. C. Jansen. A stabilized finite element method for the incompressible Navier–Stokes equations using a hierarchical basis. Int. J. Numer. Meth. Fluid 35:93–116, 2001.

    Article  CAS  Google Scholar 

  65. Wilson, N., K. Wang, R. W. Dutton, and C. A. Taylor. A software framework for creating patient specific geometric models from medical imaging data for simulation based medical planning of vascular surgery. Lect. Notes Comput. Sci. 2208:449–456, 2001.

    Article  Google Scholar 

  66. 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.

    CAS  PubMed  Google Scholar 

  67. Yeung, J. J., H. J. Kim, T. A. Abbruzzese, I. E. Vignon-Clementel, M. T. Draney-Blomme, K. K. Yeung, I. Perkash, R. J. Herfkens, C. A. Taylor, and R. L. Dalman. Aortoiliac hemodynamic and morphologic adaptation to chronic spinal cord injury. J. Vasc. Surg. 44:1254–1265, 2006.

    Article  PubMed  Google Scholar 

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Acknowledgments

The authors would like to thank Victoria Yeh and Allen Chiou for their assistance in constructing the computer models, Mary McElrath and Julie White for their assistance with patient recruitment, and Sandra Rodriguez, Romi Samra, Anne Sawyer, Dr. Janice Yeung, Dr. Geoffrey Schultz, and Dr. Byard Edwards and all staff at the Lucas Center at Stanford University for assistance with imaging. This study was supported by the National Institutes of Health (Grants P50 HL083800, 2RO1 HL064338, P41 RR09784, and U54 GM072970) and the National Science Foundation (0205741, and CNS-0619926 for computer resources).

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Correspondence to Charles A. Taylor.

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Associate Editor Kenneth R. Lutchen oversaw the review of this article.

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Les, A.S., Shadden, S.C., Figueroa, C.A. et al. Quantification of Hemodynamics in Abdominal Aortic Aneurysms During Rest and Exercise Using Magnetic Resonance Imaging and Computational Fluid Dynamics. Ann Biomed Eng 38, 1288–1313 (2010). https://doi.org/10.1007/s10439-010-9949-x

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