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.
Similar content being viewed by others
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
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Cornhill, J. F., E. E. Herderick, and H. C. Stary. Topography of human aortic sudanophilic lesions. Monogr. Atheroscler. 15:13–19, 1990.
Curci, J. A., and R. W. Thompson. Adaptive cellular immunity in aortic aneurysms: cause, consequence, or context? J. Clin. Invest. 114:168–171, 2004.
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.
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.
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.
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.
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.
Gillum, R. F. Epidemiology of aortic aneurysm in the United States. J. Clin. Epidemiol. 48:1289–1298, 1995.
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.
He, X., and D. N. Ku. Pulsatile flow in the human left coronary artery bifurcation: average conditions. J. Biomech. Eng. 118:74–82, 1996.
Holenstein, R., and D. N. Ku. Reverse flow in the major infrarenal vessels—a capacitive phenomenon. Biorheology 25:835–842, 1988.
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.
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.
Hughes, T. J. The Finite Element Method: Linear Static and Dynamic Finite Element Analysis. Mineola, NY: Dover Publications, 107 pp., 2000.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Nichols, W. W., and M. F. O’Rourke. Mcdonald’s Blood Flow in Arteries (4th ed.). New York: Oxford University Press, 179 pp., 1998.
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.
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.
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.
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.
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.
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.
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.
Santilli, J. D., and S. M. Santilli. Diagnosis and treatment of abdominal aortic aneurysms. Am. Fam. Physician 56:1081–1090, 1997.
Sergeev, S. I. Fluid oscillations in pipes at moderate Reynolds numbers. Fluid Dyn. 1:21–22, 1966.
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.
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.
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.
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.
Taylor, C. A., and M. T. Draney. Experimental and computational methods in cardiovascular fluid mechanics. Annu. Rev. Fluid Mech. 36:197–231, 2004.
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.
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.
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.
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.
van der Molen, A. J. Nephrogenic systemic fibrosis and the role of gadolinium contrast media. J. Med. Imaging Radiat. Oncol. 52:339–350, 2008.
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.
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).
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.
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.
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.
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.
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.
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).
Author information
Authors and Affiliations
Corresponding author
Additional information
Associate Editor Kenneth R. Lutchen oversaw the review of this article.
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10439-010-9949-x