Noninvasive evaluation of wall shear stress on retinal microcirculation in humans.

PURPOSE To evaluate wall shear stress (WSS) on retinal microcirculation noninvasively. METHODS Retinal vessel diameter (D) and mean centerline blood velocity (V(max, mean)) were measured in the retinal arterioles and venules at first- and second-order branches in 13 subjects using laser Doppler velocimetry (LDV). Retinal blood flow (RBF) and wall shear rate (WSR) were calculated using these two parameters. Blood viscosity at the calculated shear rate was also measured using a cone-plate viscometer. WSS was calculated as the product of the WSR and the blood viscosity. RESULTS In the first-order branches, the averaged D, V(max, mean), RBF, and WSR(mean) were 108 +/- 13 microm, 41 +/- 10 mm/s, 11 +/- 4 microL/min, and 1539 +/- 383 s(-1) in the arterioles and 147 +/- 13 microm, 23 +/- 3 mm/s, 12 +/- 4 microL/min, and 632 +/- 73 s(-1) in the venules, respectively. The apparent blood viscosities at the measured shear rates were 3.5 +/- 0.3 centipoise (cP) in the arterioles and 3.8 +/- 0.4 cP in the venules. Therefore, the averaged WSS was 54 +/- 13 dyne/cm2 in the arterioles and 24 +/- 4 dyne/cm2 in the venules. The WSS in the second-order arterioles was significantly lower than that in the first-order branches (P = 0.002), but the WSS in the first-order venules was similar to that in the second-order venules. CONCLUSIONS The authors demonstrated that the WSS in the retinal vessels could be evaluated noninvasively in humans using LDV and cone-plate viscometry. This system may be useful for further clinical investigation of the role of shear stress in the pathogenesis of various retinal disorders.

[1]  A. Koller,et al.  Exercise training augments flow-dependent dilation in rat skeletal muscle arterioles. Role of endothelial nitric oxide and prostaglandins. , 1995, Circulation research.

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

[3]  A. Gnasso,et al.  NIDDM is associated with lower wall shear stress of the common carotid artery. , 1999, Diabetes.

[4]  Angus M'Gillivray,et al.  The Ocular Circulation , 1904, Edinburgh Medical Journal.

[5]  R S Reneman,et al.  Noninvasive determination of shear-rate distribution across the arterial lumen. , 1995, Hypertension.

[6]  J. Tarbell,et al.  Effect of shear stress on the hydraulic conductivity of cultured bovine retinal microvascular endothelial cell monolayers , 2000, Current eye research.

[7]  R. Haynes.  Physical basis of the dependence of blood viscosity on tube radius. , 1960, The American journal of physiology.

[8]  H. Wayland.  Photosensor methods of flow measurement in the microcirculation. , 1973, Microvascular research.

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

[10]  A. Yoshida,et al.  Retinal blood flow changes in type I diabetes. A long-term follow-up study. , 1996, Investigative ophthalmology & visual science.

[11]  A. Gnasso,et al.  Association between wall shear stress and flow-mediated vasodilation in healthy men. , 2001, Atherosclerosis.

[12]  Robin Fåhræus,et al.  THE VISCOSITY OF THE BLOOD IN NARROW CAPILLARY TUBES , 1931 .

[13]  A. Simon,et al.  Abnormal wall shear conditions in the brachial artery of hypertensive patients. , 1990, Journal of Hypertension.

[14]  J. Weiter,et al.  Evaluation of micrometric and microdensitometric methods for measuring the width of retinal vessel images on fundus photographs , 2005, Graefe's Archive for Clinical and Experimental Ophthalmology.

[15]  G. Meininger,et al.  Arteriolar Dilation Produced by Venule Endothelium‐Derived Nitric Oxide , 1997, Microcirculation.

[16]  A. Yoshida,et al.  Relationship between the parameters of retinal circulation measured by laser Doppler velocimetry and a marker of early systemic atherosclerosis. , 2005, Investigative ophthalmology & visual science.

[17]  B L Petrig,et al.  Blood velocity and volumetric flow rate in human retinal vessels. , 1985, Investigative ophthalmology & visual science.

[18]  C. Pournaras,et al.  Decreased nitric oxide production accounts for secondary arteriolar constriction after retinal branch vein occlusion. , 1997, Investigative ophthalmology & visual science.

[19]  A. Yoshida,et al.  The effect of nitric oxide on retinal blood flow during hypoxia in cats. , 2002, Investigative ophthalmology & visual science.

[20]  I. Goldstein,et al.  Effect of nitric oxide synthase inhibition on blood flow after retinal ischemia in cats. , 1995, Investigative ophthalmology & visual science.

[21]  T. Togawa,et al.  Adaptive regulation of wall shear stress optimizing vascular tree function. , 1984, Bulletin of mathematical biology.

[22]  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.

[23]  A. Yoshida,et al.  Reproducibility and clinical application of a newly developed stabilized retinal laser Doppler instrument. , 2003, American journal of ophthalmology.

[24]  S. Alper,et al.  Hemodynamic shear stress and its role in atherosclerosis. , 1999, JAMA.

[25]  R. Pettigrew,et al.  Determination of wall shear stress in the aorta with the use of MR phase velocity mapping , 1995, Journal of magnetic resonance imaging : JMRI.

[26]  Shear-dependent release of venular nitric oxide: effect on arteriolar tone in rat striated muscle. , 1996, The American journal of physiology.

[27]  C E Riva,et al.  Laser Doppler measurements of blood velocity in human retinal vessels. , 1978, Journal of the Optical Society of America.

[28]  Tomoaki Eiju,et al.  Microscopic laser Doppler velocimeter for blood velocity measurement , 1993 .

[29]  C. D. Murray.  THE PHYSIOLOGICAL PRINCIPLE OF MINIMUM WORK , 1931, The Journal of general physiology.

[30]  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.

[31]  J. Michel,et al.  Arterial expansive remodeling induced by high flow rates. , 1997, The American journal of physiology.

[32]  M. Corretti,et al.  Endothelial reactivity and cardiac risk factors in older patients with peripheral arterial disease. , 1999, The American journal of cardiology.

[33]  L. Schmetterer,et al.  Velocity profile of red blood cells in human retinal vessels using confocal scanning laser Doppler velocimetry , 2003 .

[34]  E. Vicaut.  Microcirculation and arterial hypertension. , 1999, Drugs.

[35]  D. Glogar,et al.  Systemic endothelial dysfunction is related to the extent and severity of coronary artery disease. , 1997, Atherosclerosis.

[36]  R. Klein,et al.  Retinal microvascular abnormalities and incident stroke: the Atherosclerosis Risk in Communities Study , 2001, The Lancet.

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

[38]  C E Riva,et al.  Bidirectional LDV system for absolute measurement of blood speed in retinal vessels. , 1979, Applied optics.

[39]  G T Feke,et al.  Blood flow in the normal human retina. , 1989, Investigative ophthalmology & visual science.

[40]  P. Johnson,et al.  Attenuation of blood flow-induced dilation in arterioles after muscle contraction. , 1994, The American journal of physiology.

[41]  R. Klein,et al.  Cerebral white matter lesions, retinopathy, and incident clinical stroke. , 2002, JAMA.

[42]  M. J. Davis,et al.  Coronary venular responses to flow and pressure. , 1993, Circulation research.

[43]  R. Nerem.  Vascular fluid mechanics, the arterial wall, and atherosclerosis. , 1992, Journal of biomechanical engineering.

[44]  J. Faber,et al.  Interaction between microvascular alpha 1- and alpha 2-adrenoceptors and endothelium-derived relaxing factor. , 1992, Circulation research.

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

[46]  A. Gnasso,et al.  In vivo association between low wall shear stress and plaque in subjects with asymmetrical carotid atherosclerosis. , 1997, Stroke.

[47]  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.

[48]  Julian Moger,et al.  Measuring red blood cell flow dynamics in a glass capillary using Doppler optical coherence tomography and Doppler amplitude optical coherence tomography. , 2004, Journal of biomedical optics.

[49]  P. Boutouyrie,et al.  Remodeling of the radial artery in response to a chronic increase in shear stress. , 1996, Hypertension.