The purpose of the present study was to investigate oxygen mass transfer in the human carotid bifurcation, focusing on the effects of the wall compliance and flow field on the temporal variation and spatial distribution of the oxygen wall flux. Details of unsteady convective-diffusive oxygen transport were examined numerically using a compliant model of the human carotid bifurcation and realistic blood flow waveforms. Results reveal that axial flow separation at the outer common-internal carotid wall can significantly alter the flow field, oxygen tension field, and oxygen wall flux distribution. At the outer wall of the sinus, the Sherwood number, Sh (non-dimensional oxygen wall flux), takes on significantly lower values than at other sites due to the attenuation of transport rates by convective flow away from wall. More specifically, the lowest value of Sh was Sh∼6 (in the sinus), which is much lower than the value of the non-dimensional oxygen consumption rate (Damkohler number, Da) in the reactive wall tissue (Da=29–39). At the inner wall of the sinus, Sh∼170 is far above the expected value of Da. This implies that flow separation on the outer wall of the sinus provides a very strong fluid mechanical barrier to oxygen transport; whereas at the inner wall of the sinus, the mechanism of transport is controlled by the wall consumption rate.
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REFERENCES
Adams, V., K. Lenk, A. Linke, D. Lenz, S. Erbs, M. Sandri, A. Tarnok, S. Gielen, F. Emmrich, G. Schuler, and R. Hambrecht. Increase of circulating endothelial progenitor cells in patients with coronary artery disease after exercise-induced ischemia. Arterioscler. Thromb. Vasc. Biol. 24(4):684–690, 2004.
al-Haboubi, H. A., and B. J. Ward. Microvascular permeability of the isolated rat heart to various solutes in well-oxygenated and hypoxic conditions. Int. J. Microcirc. Clin. Exp. 16:291–301, 1996.
Bella, J. N., M. J. Roman, R. Pini, J. E. Schwartz, T. G. Pickering, and R. B. Devereux. Assessment of arterial compliance by carotid midwall strain-stress relation in normotensive adults. Hypertension 33:787–792, 1999.
Bharadvaj, B. K., R. F. Mabon, and D. P. Giddens. Steady flow in a model of the human carotid bifurcation part I – flow visualization. J. Biomech. 15:349–362, 1982.
Botnar, R., G. Rappitsch, M. B. Scheidegger, D. Liepsch, K. Perktold, and P. Boesiger. Hemodynamics in the carotid artery bifurcation: a comparison between numerical simulations and in vitro MRI measurements. J. Biomech. 33:137–144, 2000.
Cebral, J. R., P. J. Yim, R. Lohner, O. Soto, and P. L. Choyke. Blood flow modeling in carotid arteries with computational fluid dynamics and MR imaging. Acad. Radiol. 9:1286–1299, 2002.
Crawford, D. W., and D. H. Blankenhorn. Arterial wall oxygenation, oxyradicals, and atherosclerosis. Atherosclerosis 89:97–108, 1991.
Fischer, S., D. Renz, W. Schaper, and G. F. Karliczek. Effect of barbiturates on hypoxic cultures of brain derived microvascular endothelial cells. Brain Res. 707:47–53, 1996.
He, X., and D. N. Ku. Pulsatile flow in the human left coronary artery bifurcation: average conditions. Trans. ASME J. Biomech. Eng. 118:74–82, 1996.
Holdworth, D. W., C. J. D. Norley, R. Frayne, D. A. Steinman, and B. K. Rutt. Characterization of common carotid artery blood-flow waveforms in normal human subjects. Physiol. Meas. 20:219–240, 1999.
Kaazempur-Mofrad, M. R., and C. R. Ethier. Mass transport in an anatomically realistic human right coronary artery. Ann. Biomed. Eng. 29(2):121–127, 2001.
Kobayashi, H., N. Takizawa, T. Negishi, and K. Tanishita. Intravascular inhomogeneous oxygen distribution in microvessels: Theory. Respir. Physiol. Neurobiol. 19; 133(3):271–275, 2002.
Krizbai, I. A., H. Bauer, N. Bresgen, P. M. Eckl, A. Farkas, E. Szatmari, A. Traweger, K. Wejksza, and H. C. Bauer. Effect of oxidative stress on the junctional proteins of cultured cerebral endothelial cells. Cell. Mol. Neurobiol. 25(1):129–139, 2005.
Ku, D. N., D. P. Giddens, C. K. Zarins, and S. Glagov. Pulsatile flow and atherosclerosis in the human carotid bifurcation. Positive correlation between plaque location and low oscillating shear stress. Arteriosclerosis 5:293–302, 1985.
Lauwerier, H. A. The use of confluent hypergeometric functions in mathematical physics and solution of an eigenvalue problem. Appl. Sci. Res. Sect. A. 2:184–204, 1950.
Lèvêque, M. A. Les lois de la transmission de chaleur par convection. Annales des Mines Memoires Series 12. 13:201–299, 305–362, 381–415, 1928.
Ma, P. P., X. M. Li, and D. N. Ku. Convective mass transfer at the carotid bifurcation. J. Biomech. 30:565–571, 1997.
Maeda, N., Y. Sawayama, M. Tatsukawa, K. Okada, N. Furusyo, M. Shigematsu, S. Kashiwagi, and J. Hayashi. Carotid artery lesions and atherosclerotic risk factors in Japanese hemodynamics patients. Atherosclerosis 169:183–192, 2003.
Matsushita, H., R. Morishita, T. Nata, M. Aoki, H. Nakagami, Y. Taniyama, K. Yamamoto, J. Higaki, Y. Kaneda, and T. Ogihara. Hypoxia-induced endothelial apoptosis through nuclear factor-κB (NF-κB) mediated bcl-2 suppression: in vitro evidence of the importance of NF-κB in endothelial cell regulation. Circ. Res. 86:974–981, 2000.
Milner, J. S., J. A. Moore, B. K. Rutt, and D. A. Steinman. Hemodynamics of human carotid artery bifurcations: computational studies with models reconstructed from magnetic resonance imaging of normal subjects. J. Vasc. Surg. 27:143–156, 1998.
Moore, J. A., and C. R. Ethier. Oxygen mass transfer calculations in large arteries. Trans. ASME J. Biomech. Eng. 119:469–475, 1997.
Papathanasopoulou, P., S. Zhao, U. Koehler, M. B. Robertson, Q. Long, P. Hoskins, X. Y. Xu, and I. Marshall. MRI measurement of time-resolved wall shear stress vectors in a carotid bifurcation model, and comparison with CFD predictions. J. Magn. Reson. Imaging 17:153–162, 2003.
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.
Qiu, Y., and J. M. Tarbell. Numerical simulation of oxygen mass transfer in a compliant curved tube model of a coronary artery. Ann. Biomed. Eng. 28(1):26–38, 2000.
Ramnarine, K. V., T. Hartshorne, Y. Sensier, M. Naylor, J. Walker, A. R. Naylor, R. B. Panerai, and D. H. Evans. Tissue Doppler imaging of carotid plaque wall motion: a pilot study. Cardiovascular Ultrasound 1:1–15, 2003.
Salzer, R. S., M. J. Thubrikar, and R. T. Eppink. Pressure-induced mechanical stress in the carotid artery bifurcation: a possible correlation to atherosclerosis. J. Biomech. 28:1333–1340, 1995.
Santilli, S. M., R. B. Stevens, J. G. Anderson, W. D. Payne, and M. D. F. Caldwell. Transarterial wall oxygen gradients at the dog carotid bifurcation. Am. J. Physiol. Heart Circ. Physiol. 268: H155–H161, 1995.
Schlichting, H. Boundary Layer Theory. New York, NY, USA: McGraw-Hill, pp. 436–439, 1979.
Schulz, U. G. R., and P. M. Rothwell. Major variation in carotid bifurcation anatomy – a possible risk factor for plaque development. Stroke 32:2522–2529, 2001.
Secomb, T. W. Flow in a channel with pulsating walls. J. Fluid Mech. 88(2):273–288, 1978.
Sellars, J. R., M. Tribus, and J. S. Klein. Heat transfer to laminar flow in a round tube or flat conduit – the graetz problem extended. Trans. ASME 78, 441–448, 1956.
Selzer, R. H., W. J. Mack, P. L. Lee, H. Kwong-Fu, and H. N. Hodis. Improved common carotid elasticity and intima-media thickness measurements from computer analysis of sequential ultrasound frames. Athrosclerosis 154:185–193, 2001.
Sitzer, M., D. Puac, A. Buehler, D. A. Steckel, S. von Kegler, H. S. Markus, and H. Steinmetz. Internal carotid artery angle of origin: a novel risk factor for early carotid atherosclerosis. Stroke 34:950–955, 2003.
Stadler, R. W., J. A. Taylor, and R. S. Lees. Comparison of B-mode, M-mode and Echo-tracking methods for measurement of the arterial distension waveform. Ultrasound Med. Biol. 23:879–887, 1997.
Steinman, D. A., J. B. Thomas, H. M. Ladak, J. S. Milner, B. K. Rutt, and J. D. Spence. Reconstruction of carotid bifurcation hemodynamics and wall thickness using computational fluid dynamics and MRI. Magnet. Reson. Med. 47:149–159, 2002.
Sun, Y., C. H. Lin, C. J. Lu, P. K. Yip, and R. C. Chen. Carotid atherosclerosis, intima media thickness and risk factors – an analysis of 1781 asymptomatic subjects in Taiwan. Atherosclerosis 164:89–94, 2002.
Tada, S., and J. M. Tarbell. A computational study of flow in a compliant carotid bifurcation – stress phase angle correlation with shear stress. Ann. Biomed. Eng. 33:1202–1212, 2005.
Tarbell, J. M. Mass transport in arteries and the localization of atherosclerosis. Annu. Rev. Biomed. Eng. 5:79–118, 2003.
Tuder, R. M., B. E. Flook, and N. F. Voelkel. Increased gene expression for VEGF and the VEGF receptors KDR/Flk and Flt in lungs exposed to acute or to chronic hypoxia. J. Clin. Invest. 95:1798–1807, 1995.
Urbina, E. M., S. R. Srinivasan, R. Tang, M. G. Bond, L. Kieltyka, and G. S. Berenson. Impact of multiple coronary risk factors on the intima-media thickness of different segments of carotid artery in healthy young adults (The Bogalusa Heart Study). Am. J. Cardiol. 90:953–958, 2002.
Vadapalli, A., R. N. Pittman, and A. S. Popel. Estimating oxygen transport resistance of the microvascular wall. Am. J. Physiol. Heart Circ. Physiol. 279:H657–H671, 2000.
Whiteley, J. P., D. J. Gavaghan, and C. E. W. Hahn. Mathematical modeling of oxygen transport to tissue. J. Math. Biol. 44:503–522, 2002.
Younis, H. F., M. R. Kaazempur-Mofrad, C. Chung, R. C. Chan, and R. D. Kamm. Computational analysis of the effects of exercise on hemodynamics in the carotid bifurcation. Ann. Biomed. Eng. 13:995–1006, 2003.
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.
Zhao, S. Z., B. Ariff, Q. Long, A. D. Hughes, S. A. Thom, A. V. Stanton, and X. Y. Xu. Inter-individual variations in wall shear stress and mechanical stress distributions at the carotid artery bifurcation of healthy humans. J. Biomech. 35:1367–1377, 2002.
Zhao, S. Z., X. Y. Xu, A. D. Hughes, S. A. Thom, A. V. Stanton, B. Ariff, and Q. Long. Blood flow and vessel mechanics in a physiologically realistic model of a human carotid arterial bifurcation. J. Biomech. 33:975–984, 2000.
Zulliger, M. A., N. T. M. R. Kwak, T. Tsapikouni, and N. Stergiopulos. Effects of longitudinal stretch on VSM tone and distensibility of muscular conduit arteries. Am. J. Physiol. Heart Circ. Physiol. 283:H2599–H2605, 2002.
ACKNOWLEDGMENTS
This work was supported by NIH NHLBI HL35549 to JMT. Numerical simulations were carried out on a parallel supercomputing machine the Silicon Graphics Origin-2000, at the National Center for Supercomputing Applications (NCSA, Champaign, IL).
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APPENDIX
APPENDIX
The equations governing the fluid motion are the momentum equations and the equation of continuity:
where u j is the velocity component in the x j direction, comma j (, j) denotes the partial derivative of a function with respect to the independent variable x j . Any terms in which the same index appears twice stands for the sum of all terms obtained by giving this index its complete range of values (j=1, 2, 3). In addition, ρ is the fluid density, σ ij is the stress, f i is the body force at time t per unit mass, and \(\bar u\) is the mesh velocity at time t. The equations governing the structural domain are the momentum equations, the equilibrium conditions and the constitutive equations, respectively:
where a i represents the acceleration of a material point (where displacement is defined as \(d_i = x_i - x_i^0\), and \(x_i^0\) is the stress-free position) at time t, n j is the outward pointing normal vector on the structural boundary at time t, s t i is the surface traction vector at time t, D ijkl is the material elasticity tensor, and ɛ ij is the infinitesimal strain tensor.
The grid system is adjusted to accommodate the deformation of the structural body to avoid distortion due to significant deformation of the computational domain.
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Tada, S., Tarbell, J.M. Oxygen Mass Transport in a Compliant Carotid Bifurcation Model. Ann Biomed Eng 34, 1389–1399 (2006). https://doi.org/10.1007/s10439-006-9155-z
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DOI: https://doi.org/10.1007/s10439-006-9155-z