Wall shear stress as measured in vivo: consequences for the design of the arterial system

Based upon theory, wall shear stress (WSS), an important determinant of endothelial function and gene expression, has been assumed to be constant along the arterial tree and the same in a particular artery across species. In vivo measurements of WSS, however, have shown that these assumptions are far from valid. In this survey we will discuss the assessment of WSS in the arterial system in vivo and present the results obtained in large arteries and arterioles. In vivo WSS can be estimated from wall shear rate, as derived from non-invasively recorded velocity profiles, and whole blood viscosity in large arteries and plasma viscosity in arterioles, avoiding theoretical assumptions. In large arteries velocity profiles can be recorded by means of a specially designed ultrasound system and in arterioles via optical techniques using fluorescent flow velocity tracers. It is shown that in humans mean WSS is substantially higher in the carotid artery (1.1–1.3 Pa) than in the brachial (0.4–0.5 Pa) and femoral (0.3–0.5 Pa) arteries. Also in animals mean WSS varies substantially along the arterial tree. Mean WSS in arterioles varies between about 1.0 and 5.0 Pa in the various studies and is dependent on the site of measurement in these vessels. Across species mean WSS in a particular artery decreases linearly with body mass, e.g., in the infra-renal aorta from 8.8 Pa in mice to 0.5 Pa in humans. The observation that mean WSS is far from constant along the arterial tree implies that Murray’s cube law on flow-diameter relations cannot be applied to the whole arterial system. Because blood flow velocity is not constant along the arterial tree either, a square law also does not hold. The exponent in the power law likely varies along the arterial system, probably from 2 in large arteries near the heart to 3 in arterioles. The in vivo findings also imply that in in vitro studies no average shear stress value can be taken to study effects on endothelial cells derived from different vascular areas or from the same artery in different species. The cells have to be studied under the shear stress conditions they are exposed to in real life.

[1]  M Zamir,et al.  Shear forces and blood vessel radii in the cardiovascular system , 1977, The Journal of general physiology.

[2]  Theo Arts,et al.  Wall Shear Stress – an Important Determinant of Endothelial Cell Function and Structure – in the Arterial System in vivo , 2006, Journal of Vascular Research.

[3]  R S Reneman,et al.  Differences in near-wall shear rate in the carotid artery within subjects are associated with different intima-media thicknesses. , 1998, Arteriosclerosis, thrombosis, and vascular biology.

[4]  Avrum I. Gotlieb,et al.  Molecular Basis of Cardiovascular Disease , 2009 .

[5]  R. Krams,et al.  Large variations in absolute wall shear stress levels within one species and between species. , 2007, Atherosclerosis.

[6]  D. Slaaf,et al.  Orientation and diameter distribution of rabbit blood platelets flowing in small arterioles. , 1984, Biorheology.

[7]  T. Kenner,et al.  Flow and stress characteristics in rigid walled and compliant carotid artery bifurcation models , 2006, Medical and Biological Engineering and Computing.

[8]  R S Reneman,et al.  Control of arterial branching morphogenesis in embryogenesis: go with the flow. , 2005, Cardiovascular research.

[9]  T Togawa,et al.  Adaptive regulation of wall shear stress to flow change in the canine carotid artery. , 1980, The American journal of physiology.

[10]  A. Hoeks,et al.  Brachial artery shear stress is independent of gender or age and does not modify vessel wall mechanical properties. , 2002, Ultrasound in medicine & biology.

[11]  R S Reneman,et al.  The effect of echo suppression on the mean velocity estimation range of the RF cross-correlation model estimator. , 1995, Ultrasound in medicine & biology.

[12]  P. Sipkema,et al.  Differential structural adaptation to haemodynamics along single rat cremaster arterioles , 2003, The Journal of physiology.

[13]  R. Busse,et al.  Pulsatile Stretch and Shear Stress: Physical Stimuli Determining the Production of Endothelium-Derived Relaxing Factors , 1998, Journal of Vascular Research.

[14]  P. Serruys,et al.  Extension of Increased Atherosclerotic Wall Thickness Into High Shear Stress Regions Is Associated With Loss of Compensatory Remodeling , 2003, Circulation.

[15]  H N Mayrovitz,et al.  Microvascular blood flow: evidence indicating a cubic dependence on arteriolar diameter. , 1983, The American journal of physiology.

[16]  P. Davies,et al.  Mechanical stress mechanisms and the cell. An endothelial paradigm. , 1993, Circulation research.

[17]  J. Spaan,et al.  Shear stress is not sufficient to control growth of vascular networks: a model study. , 1996, The American journal of physiology.

[18]  Arnold P G Hoeks,et al.  Shear stress depends on vascular territory: comparison between common carotid and brachial artery. , 2003, Journal of applied physiology.

[19]  A. M. Melkumyants,et al.  Control of Arterial Lumen By Shear Stress on Endothelium , 1995 .

[20]  P Boesiger,et al.  In vivo wall shear stress measured by magnetic resonance velocity mapping in the normal human abdominal aorta. , 1997, European journal of vascular and endovascular surgery : the official journal of the European Society for Vascular Surgery.

[21]  T F Sherman,et al.  On connecting large vessels to small. The meaning of Murray's law , 1981, The Journal of general physiology.

[22]  Jerry Westerweel,et al.  In vivo micro particle image velocimetry measurements of blood-plasma in the embryonic avian heart. , 2006, Journal of biomechanics.

[23]  R S Reneman,et al.  A noninvasive method to estimate wall shear rate using ultrasound. , 1995, Ultrasound in medicine & biology.

[24]  Gabor Kaley,et al.  Shear Stress Dependent Regulation of Vascular Resistance in Health and Disease: Role of Endothelium , 1996 .

[25]  R S Reneman,et al.  Wall shear stress in the human common carotid artery as function of age and gender. , 1998, Cardiovascular research.

[26]  B. L. Langille,et al.  Shear Stress Regulates Forward and Reverse Planar Cell Polarity of Vascular Endothelium In Vivo and In Vitro , 2006, Circulation research.

[27]  R. Furchgott Role of endothelium in responses of vascular smooth muscle. , 1983, Circulation research.

[28]  S. A. Balashov,et al.  Effect of blood viscocity on arterial flow induced dilator response. , 1990, Cardiovascular research.

[29]  A. Koller,et al.  Development of nitric oxide and prostaglandin mediation of shear stress-induced arteriolar dilation with aging and hypertension. , 1999, Hypertension.

[30]  Y. Fung,et al.  The pattern of coronary arteriolar bifurcations and the uniform shear hypothesis , 2006, Annals of Biomedical Engineering.

[31]  S. Rodbard Vascular caliber. , 1975, Cardiology.

[32]  P. Doriot,et al.  In‐vivo measurements of wall shear stress in human coronary arteries , 2000, Coronary artery disease.

[33]  D. Bluemke,et al.  Why is flow-mediated dilation dependent on arterial size? Assessment of the shear stimulus using phase-contrast magnetic resonance imaging. , 2004, American journal of physiology. Heart and circulatory physiology.

[34]  D. Slaaf,et al.  Endogenous nitric oxide protects against thromboembolism in venules but not in arterioles. , 1998, Arteriosclerosis, thrombosis, and vascular biology.

[35]  Charles A. Taylor,et al.  Allometric scaling of wall shear stress from mice to humans: quantification using cine phase-contrast MRI and computational fluid dynamics. , 2006, American journal of physiology. Heart and circulatory physiology.

[36]  M. Gimbrone,et al.  Blood flow and vascular gene expression: fluid shear stress as a modulator of endothelial phenotype. , 1999, Molecular medicine today.

[37]  D. Stepp,et al.  Regulation of shear stress in the canine coronary microcirculation. , 1999, Circulation.

[38]  R S Reneman,et al.  Wall shear rate in arterioles in vivo: least estimates from platelet velocity profiles. , 1988, The American journal of physiology.

[39]  A. Gnasso,et al.  Association between intima-media thickness and wall shear stress in common carotid arteries in healthy male subjects. , 1996, Circulation.

[40]  A. Pries,et al.  Resistance to blood flow in microvessels in vivo. , 1994, Circulation research.

[41]  M. Rondaij,et al.  KLF2 provokes a gene expression pattern that establishes functional quiescent differentiation of the endothelium. , 2006, Blood.

[42]  Theo Arts,et al.  Wall shear stress--an important determinant of endothelial cell function and structure--in the arterial system in vivo. Discrepancies with theory. , 2006, Journal of vascular research.

[43]  R S Reneman,et al.  Propagation velocity and reflection of pressure waves in the canine coronary artery. , 1979, The American journal of physiology.

[44]  H. H. Lipowsky,et al.  The Distribution of Blood Rheological Parameters in the Microvasculature of Cat Mesentery , 1978, Circulation research.

[45]  R Busse,et al.  Crucial role of endothelium in the vasodilator response to increased flow in vivo. , 1986, Hypertension.

[46]  Dick W. Slaaf,et al.  Concentration and Velocity Profiles of Blood Cells in the Microcirculation , 1992 .

[47]  Craig J. Hartley,et al.  Doppler evaluation of peripheral vascular adaptations to transverse aortic banding in mice. , 2003 .

[48]  P J Brands,et al.  Assessment of the spatial homogeneity of artery dimension parameters with high frame rate 2-D B-mode. , 2001, Ultrasound in medicine & biology.

[49]  Arnold P G Hoeks,et al.  Assessment of spatial inhomogeneities in intima media thickness along an arterial segment using its dynamic behavior. , 2003, American journal of physiology. Heart and circulatory physiology.

[50]  Yuzhi Zhang,et al.  Integration of flow-dependent endothelial phenotypes by Kruppel-like factor 2. , 2005, The Journal of clinical investigation.

[51]  S. Oyre,et al.  Accurate noninvasive quantitation of blood flow, cross-sectional lumen vessel area and wall shear stress by three-dimensional paraboloid modeling of magnetic resonance imaging velocity data. , 1998, Journal of the American College of Cardiology.

[52]  T. Wonnacott,et al.  Relation between diameter and flow in major branches of the arch of the aorta. , 1992, Journal of biomechanics.

[53]  R S Reneman,et al.  Velocity Profiles of Blood Platelets and Red Blood Cells Flowing in Arterioles of the Rabbit Mesentery , 1986, Circulation research.

[54]  A. Pries,et al.  Design principles of vascular beds. , 1995, Circulation research.

[55]  C D Murray,et al.  The Physiological Principle of Minimum Work: I. The Vascular System and the Cost of Blood Volume. , 1926, Proceedings of the National Academy of Sciences of the United States of America.

[56]  R. Gramiak,et al.  Cardiovascular Applications of Ultrasound , 1975 .

[57]  R. Mohiaddin,et al.  Applications of phase-contrast flow and velocity imaging in cardiovascular MRI , 2005, European Radiology.

[58]  N. Hwang,et al.  Advances in Cardiovascular Engineering , 1992, NATO ASI Series.

[59]  M. Frojmovic,et al.  Geometry of normal mammalian platelets by quantitative microscopic studies. , 1976, Biophysical journal.

[60]  R. Reneman,et al.  Mean Wall Shear Stress in the Femoral Arterial Bifurcation Is Low and Independent of Age at Rest , 2000, Journal of Vascular Research.

[61]  A. Pries,et al.  Corrections and Retraction , 2004 .

[62]  M. Labarbera Principles of design of fluid transport systems in zoology. , 1990, Science.

[63]  A. Pries,et al.  Control of blood vessel structure: insights from theoretical models. , 2005, American journal of physiology. Heart and circulatory physiology.

[64]  D. N. Walder,et al.  The effect of increased fibrinogen content on the viscosity of blood. , 1969, Clinical science.

[65]  R S Reneman,et al.  In the femoral artery bifurcation, differences in mean wall shear stress within subjects are associated with different intima-media thicknesses. , 1999, Arteriosclerosis, thrombosis, and vascular biology.