Abstract
Abdominal aortic aneurysm (AAA) is a vascular disease resulting in a permanent, localized enlargement of the abdominal aorta. We previously hypothesized that the progression of AAA may be slowed by altering the hemodynamics in the abdominal aorta through exercise [Dalman, R. L., M. M. Tedesco, J. Myers, and C. A. Taylor. Ann. N.Y. Acad. Sci. 1085:92–109, 2006]. To quantify the effect of exercise intensity on hemodynamic conditions in 10 AAA subjects at rest and during mild and moderate intensities of lower-limb exercise (defined as 33 ± 10% and 63 ± 18% increase above resting heart rate, respectively), we used magnetic resonance imaging and computational fluid dynamics techniques. Subject-specific models were constructed from magnetic resonance angiography data and physiologic boundary conditions were derived from measurements made during dynamic exercise. We measured the abdominal aortic blood flow at rest and during exercise, and quantified mean wall shear stress (MWSS), oscillatory shear index (OSI), and particle residence time (PRT). We observed that an increase in the level of activity correlated with an increase of MWSS and a decrease of OSI at three locations in the abdominal aorta, and these changes were most significant below the renal arteries. As the level of activity increased, PRT in the aneurysm was significantly decreased: 50% of particles were cleared out of AAAs within 1.36 ± 0.43, 0.34 ± 0.10, and 0.22 ± 0.06 s at rest, mild exercise, and moderate exercise levels, respectively. Most of the reduction of PRT occurred from rest to the mild exercise level, suggesting that mild exercise may be sufficient to reduce flow stasis in AAAs.
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Abbreviations
- AAA:
-
Abdominal aortic aneurysm
- CFD:
-
Computational fluid dynamics
- DBP:
-
Diastolic blood pressure
- IR:
-
Infrarenal
- MA:
-
Mid-aneurysm
- MRI:
-
Magnetic resonance imaging
- MWSS:
-
Mean wall shear stress
- OSI:
-
Oscillatory shear index
- PRI:
-
Particle residence index
- PRT:
-
Particle residence time
- RCR:
-
Resistance (proximal)–capacitance–resistance (distal)
- SC:
-
Supraceliac
- SBP:
-
Systolic blood pressure
- SRBF:
-
Splanchnic and renal blood flows
References
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.
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.
Cao, J., and S. E. Rittgers. Particle motion within in vitro models of stenosed internal carotid and left anterior descending coronary arteries. Ann. Biomed. Eng. 26:190–199, 1998.
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.
Dai, G., M. R. Kaazempur-Mofrad, S. Natarajan, Y. Zhang, S. Vaughn, B. R. Blackman, R. D. Kamm, G. Garcia-Cardena, and M. A. Gimbrone, Jr. Distinct endothelial phenotypes evoked by arterial waveforms derived from atherosclerosis-susceptible and -resistant regions of human vasculature. Proc. Natl. Acad. Sci. 101(41):14871–14876, 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.
De Meirelles, L. R., A. C. Mendes-Ribeiro, M. A. Mendes, M. N. da Silva, J. C. Ellory, G. E. Mann, and T. M. Brunini. Chronic exercise reduces platelet activation in hypertension: upregulation of the l-arginine-nitric oxide pathway. Scand. J. Med. Sci. Sports 19:67–74, 2009.
DeSouza, C. A., L. F. Shapiro, C. M. Clevenger, F. A. Dinenno, K. D. Monahan, H. Tanaka, and D. R. Seals. Regular aerobic exercise prevents and restores age-related declines in endothelium-dependent vasodilation in healthy men. Circulation 102:1351–1357, 2000.
Einav, S., and D. Bluestein. Dynamics of blood flow and platelet transport in pathological vessels. Ann. N.Y. Acad. Sci. 1015:351–366, 2004.
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 Circ. 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.
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., P. Gadhoke, R. Berguer, and J. L. Bull. Modeling pulsatile flow in aortic aneurysms: effect of nonnewtonian properties of blood. Biorheology 43:661–679, 2006.
Kim, H. J., C. A. Figueroa, T. J. Hughes, K. C. 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. Methods Appl. Mech. Eng. 198:3551–3566, 2009.
Laughlin, M. H. Cardiovascular response to exercise. Am. J. Physiol. 277:244–259, 1999.
Les, A. S., S. C. Shadden, C. A. Figueroa, J. M. Park, M. M. Tedesco, R. J. Herfkens, R. L. Dalman, and C. A. Taylor. 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.
Malek, A. M., S. L. Alper, and S. Izumo. Hemodynamic shear stress and its role in atherosclerosis. J. Am. Med. Assoc. 282:2035–2042, 1999.
Moore, J. E., Jr., 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, J. E., Jr., 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.
Myers, J. N., J. J. White, B. Narasimhan, and R. L. Dalman. Effects of exercise training in patients with abdominal aortic aneurysm: preliminary results from a randomaized trial. J. Cardiopulm. Rehabil. Prev. 30:374–383, 2010.
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.
Nelson, M. E., W. J. Rejeski, S. N. Blair, P. W. Duncan, J. O. Judge, A. C. King, C. A. Macera, and C. Castaneda-Seppa. Physical activity and public health in older adults. Recommendation from the American College of Sports and Medicine and the American Heart Association. Circulation 116:1094–1105, 2007.
Osada, T., T. Katsumura, T. Hamaoka, S. Inoue, K. Esaki, A. Sakamoto, N. Murase, J. Kajiyama, T. Shimomitsu, and H. Iwane. Reduced blood flow in abdominal viscera measured by Doppler ultrasound during one-legged knee extension. J. Appl. Physiol. 86:709–719, 1999.
Plehn, G., J. Vormbrock, T. Butz, M. Christ, H, Trappe, and A. Meissner. Different effect of exercise on left ventricular diastolic time and interventricular dyssnchrony in heart failure patients with and without left bundle branch block. Int. J. Med. Sci. 5:333–340, 2008.
Raines, J. K., M. Y. Jaffrin, and A. H. Shapiro. A computer simulation of arterial dynamics in the human leg. J. Biomech. 7:77–91, 1974.
Rowell, L. B. Human Cardiovascular Control. New York: Oxford University Press, 212 pp, 1993.
Rubler, S., V. J. Fisher, S. S. Schreiber, M. A. Rothschild, and A. S. Dobin. Left ventrivular ejection time during exercise testing with scintigraphy. Arch. Intern. Med. 144:1386–1391, 1984.
Sakalihasan, N., R. Limet, and O. D. Defawe. Abdominal aortic aneurysm. Lancet 365:1577–1589, 2005.
Spilker, R. L., and C. A. Taylor. Tuning multiscale hemodynamic simulations to match physiological measurements. Ann. Biomed. Eng. 38:2635–2648, 2010.
Suh, G., A. S. Les, A. S. Tenforde, S. C. Shadden, R. L. Spilker, J. J. Yeung, C. P. Cheng, R. J. Herfkens, R. L. Dalman, and C. A. Taylor. Quantification of particle residence time in abdominal aortic aneurysms using magnetic resonance imaging and computational fluid dynamics. Ann. Biomed. Eng. 29:864–883, 2011.
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 Circ. Physiol. 291:668–676, 2006.
Taylor, C. A., T. J. R. Hughes, and C. K. Zarins. Finite element modeling of blood flow in arteries. Comput. Methods Appl. Mech. Eng. 158:155–196, 1998.
Taylor, C. A., T. J. R. Hughes, and C. K. Zarins. Effect of exercise on hemodynamic conditions in the abdominal aorta. J. Vasc. Surg. 29:1077–1089, 1999.
Tenforde, A. S., C. P. Cheng, G. Suh, R. J. Herfkens, R. L. Dalman, and C. A. Taylor. Quantifying in vivo hemodynamic response to exercise in patients with intermittent claudication and abdominal aortic aneurysms using cine phase-contrast MRI. J. Magn. Reson. Imaging 31:425–429, 2010.
Vignon-Clementel, I. E., C. A. Figueroa, K. E. Jensen, and C. A. Taylor. Outflow boundary conditions for three-dimensional finite element modeling of blood flow and pressure in arteries. Comput. Methods Appl. Mech. Eng. 195:3776–3796, 2006.
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. Methods Fluids 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 in known. J. Physiol. 127:553–563, 1955.
Zarins, C. K., D. P. Giddens, B. K. Bharadvaj, V. S. Sottiurai, R. F. Mabon, and S. Glagov. Carotid bifurcation atherosclerosis. Quantitative correlation of plaque localization with flow velocity profiles and wall shear stress. Circ. Res. 53:502–514, 1983.
Acknowledgments
This research was supported by the National Institutes of Health (P50 HL083800, P41 RR09784), the Lucas Center for Magnetic Resonance Imaging, and the Veterans Affairs Palo Alto Health Care System (VAPAHCS) for the acquisition of experimental data, and NSF (CNS-0619926) for computer resources. Allen Chiou, Victoria Yeh, Yash Narang, and Bartlomiej R. Imielski provided assistance with imaging and modeling. Nan Xiao provided help with quantification of PRT data. We thank all research subjects for their participation.
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Associate Editor Kerry Hourigan oversaw the review of this article.
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Suh, GY., Les, A.S., Tenforde, A.S. et al. Hemodynamic Changes Quantified in Abdominal Aortic Aneurysms with Increasing Exercise Intensity Using MR Exercise Imaging and Image-Based Computational Fluid Dynamics. Ann Biomed Eng 39, 2186–2202 (2011). https://doi.org/10.1007/s10439-011-0313-6
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DOI: https://doi.org/10.1007/s10439-011-0313-6