Atherosclerosis
Volume 195, Issue 2 , Pages 225-235 , December 2007

Large variations in absolute wall shear stress levels within one species and between species

  • Caroline Cheng

      Affiliations

    • Department of Cardiology, Thoraxcenter, Erasmus MC, Rotterdam, The Netherlands
    • Authors have contributed equally to this manuscript.
    • Corresponding Author InformationCorresponding author at: Erasmus MC, Room Ee1073b, Dr. Molewaterplein 50, 3015 GE Rotterdam, The Netherlands. Tel.: +31 10 4089393; fax: +31 10 4089494.
  • ,
  • Frank Helderman

      Affiliations

    • Department of Cardiology, Thoraxcenter, Erasmus MC, Rotterdam, The Netherlands
    • Authors have contributed equally to this manuscript.
  • ,
  • Dennie Tempel

      Affiliations

    • Department of Cardiology, Thoraxcenter, Erasmus MC, Rotterdam, The Netherlands
  • ,
  • Dolf Segers

      Affiliations

    • Department of Cardiology, Thoraxcenter, Erasmus MC, Rotterdam, The Netherlands
  • ,
  • Beerend Hierck

      Affiliations

    • Department of Embryology and Anatomy, LUMC, Leiden, The Netherlands
  • ,
  • Rob Poelmann

      Affiliations

    • Department of Embryology and Anatomy, LUMC, Leiden, The Netherlands
  • ,
  • Arie van Tol

      Affiliations

    • Department of Cell Biology, Erasmus MC, Rotterdam, The Netherlands
  • ,
  • Dirk J. Duncker

      Affiliations

    • Department of Cardiology, Thoraxcenter, Erasmus MC, Rotterdam, The Netherlands
  • ,
  • Danielle Robbers-Visser

      Affiliations

    • Department of Pediatric Cardiology, Erasmus MC, Rotterdam, The Netherlands
  • ,
  • Nicolette T.C. Ursem

      Affiliations

    • Department of Obstetrics, Erasmus MC, Rotterdam, The Netherlands
  • ,
  • Rien van Haperen

      Affiliations

    • Department of Cell Biology, Erasmus MC, Rotterdam, The Netherlands
  • ,
  • Jolanda J. Wentzel

      Affiliations

    • Department of Cardiology, Thoraxcenter, Erasmus MC, Rotterdam, The Netherlands
  • ,
  • Frank Gijsen

      Affiliations

    • Department of Cardiology, Thoraxcenter, Erasmus MC, Rotterdam, The Netherlands
  • ,
  • Anton F.W. van der Steen

      Affiliations

    • Department of Cardiology, Thoraxcenter, Erasmus MC, Rotterdam, The Netherlands
  • ,
  • Rini de Crom

      Affiliations

    • Department of Cell Biology, Erasmus MC, Rotterdam, The Netherlands
    • Department of Vascular Surgery, Erasmus MC, Rotterdam, The Netherlands
  • ,
  • Rob Krams

      Affiliations

    • Department of Cardiology, Thoraxcenter, Erasmus MC, Rotterdam, The Netherlands
    • Department of Physiology, Medical Physics and Vascular Surgery, VUMC, Amsterdam, The Netherlands

Received 7 August 2006 ,Revised 25 October 2006 ,Accepted 15 November 2006.

References 

  1. Hogers B, DeRuiter MC, Gittenberger-de Groot AC, Poelmann RE. Unilateral vitelline vein ligation alters intracardiac blood flow patterns and morphogenesis in the chick embryo. Circ Res. 1997;80:473–481
  2. Hove JR, Koster RW, Forouhar AS, Acevedo-Bolton G, Fraser SE, Gharib M. Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis. Nature. 2003;421:172–177
  3. Gimbrone MA, Topper JN, Nagel T, Anderson KR, Garcia-Cardena G. Endothelial dysfunction, hemodynamic forces, and atherogenesis. Ann N Y Acad Sci. 2000;902:230–239[discussion 239–240]
  4. Cheng C, Tempel D, van Haperen R, et al. Atherosclerotic lesion size and vulnerability are determined by patterns of fluid shear stress. Circulation. 2006;113:2744–2753
  5. Malek AM, Alper SL, Izumo S. Hemodynamic shear stress and its role in atherosclerosis. JAMA. 1999;282:2035–2042
  6. LaBarbera M. Principles of design of fluid transport systems in zoology. Science. 1990;249:992–1000
  7. Girerd X, London G, Boutouyrie P, Mourad JJ, Safar M, Laurent S. Remodeling of the radial artery in response to a chronic increase in shear stress. Hypertension. 1996;27:799–803
  8. Kamiya A, Bukhari R, Togawa T. Adaptive regulation of wall shear stress optimizing vascular tree function. Bull Math Biol. 1984;46:127–137
  9. Rossitti S, Lofgren J. Vascular dimensions of the cerebral arteries follow the principle of minimum work. Stroke. 1993;24:371–377
  10. Gnasso A, Carallo C, Irace C, et al. Association between wall shear stress and flow-mediated vasodilation in healthy men. Atherosclerosis. 2001;156:171–176
  11. Jiang Y, Kohara K, Hiwada K. Low wall shear stress contributes to atherosclerosis of the carotid artery in hypertensive patients. Hypertens Res. 1999;22:203–207
  12. Joannides R, Bizet-Nafeh C, Costentin A, et al. Chronic ACE inhibition enhances the endothelial control of arterial mechanics and flow-dependent vasodilatation in heart failure. Hypertension. 2001;38:1446–1450
  13. Taber LA, Ng S, Quesnel AM, Whatman J, Carmen CJ. Investigating Murray's law in the chick embryo. J Biomech. 2001;34:121–124
  14. Taber LA. An optimization principle for vascular radius including the effects of smooth muscle tone. Biophys J. 1998;74:109–114
  15. Murray C. The physiological principle of minimum work. I. The vascular system and the cost of blood volume. Proc. Natl Acad Sci USA. 1926;12:207–214
  16. Murray C. The physiological principle of minimum work applied to the angle of the branching of arteries. J Gen Physiol. 1926;9:835–841
  17. Zamir M. Shear forces and blood vessel radii in the cardiovascular system. J Gen Physiol. 1977;69:449–461
  18. Gnasso A, Carallo C, Irace C, et al. Association between intima-media thickness and wall shear stress in common carotid arteries in healthy male subjects. Circulation. 1996;94:3257–3262
  19. Cheng CP, Herfkens RJ, Taylor CA. Abdominal aortic hemodynamic conditions in healthy subjects aged 50–70 at rest and during lower limb exercise: in vivo quantification using MRI. Atherosclerosis. 2003;168:323–331
  20. Kornet L, Hoeks AP, Lambregts J, Reneman RS. Mean wall shear stress in the femoral arterial bifurcation is low and independent of age at rest. J Vasc Res. 2000;37:112–122
  21. Wu SP, Ringgaard S, Oyre S, et al. Wall shear rates differ between the normal carotid, femoral, and brachial arteries: an in vivo MRI study. J Magn Reson Imaging. 2004;19:188–193
  22. Kamiya A, Togawa T. Adaptive regulation of wall shear stress to flow change in the canine carotid artery. Am J Physiol. 1980;239:H14–H21
  23. Marano G, Palazzesi S, Vergari A, Ferrari AU. Protection by shear stress from collar-induced intimal thickening: role of nitric oxide. Arterioscler Thromb Vasc Biol. 1999;19:2609–2614
  24. Ross G, White FN, Brown AW, Kolin A. Regional blood flow in the rat. J Appl Physiol. 1966;21:1273–1275
  25. Li YH, Reddy AK, Taffet GE, et al. Doppler evaluation of peripheral vascular adaptations to transverse aortic banding in mice. Ultrasound Med Biol. 2003;29:1281–1289
  26. Dammers R, Stifft F, Tordoir JH, et al. Shear stress depends on vascular territory: comparison between common carotid and brachial artery. J Appl Physiol. 2003;94:485–489
  27. Oyre S, Ringgaard S, Kozerke S, 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. J Am Coll Cardiol. 1998;32:128–134
  28. Samijo SK, Willigers JM, Barkhuysen R, et al. Wall shear stress in the human common carotid artery as function of age and gender. Cardiovasc Res. 1998;39:515–522
  29. Samijo SK, Barkhuysen R, Willigers JM, et al. Wall shear stress assessment in the common carotid artery of end-stage renal failure patients. Nephron. 2002;92:557–563
  30. Oshinski JN, Ku DN, Mukundan S, Loth F, Pettigrew RI. Determination of wall shear stress in the aorta with the use of MR phase velocity mapping. J Magn Reson Imaging. 1995;5:640–647
  31. Oyre S, Pedersen EM, Ringgaard S, Boesiger P, Paaske WP. In vivo wall shear stress measured by magnetic resonance velocity mapping in the normal human abdominal aorta. Eur J Vasc Endovasc Surg. 1997;13:263–271
  32. Pedersen EM, Oyre S, Agerbaek M, et al. Distribution of early atherosclerotic lesions in the human abdominal aorta correlates with wall shear stresses measured in vivo. Eur J Vasc Endovasc Surg. 1999;18:328–333
  33. Tang BT. Abdominal aortic hemodynamics in young healthy adults at rest and during lower limp exercise: quantification using image-based computer modelling, in review.
  34. Gaenzer H, Neumayr G, Marschang P, et al. Flow-mediated vasodilation of the femoral and brachial artery induced by exercise in healthy nonsmoking and smoking men. J Am Coll Cardiol. 2001;38:1313–1319
  35. Silber HA, Ouyang P, Bluemke DA, et al. Why is flow-mediated dilation dependent on arterial size? Assessment of the shear stimulus using phase-contrast magnetic resonance imaging. Am J Physiol Heart Circ Physiol. 2005;288:H822–H828
  36. Mitchell GF, Parise H, Vita JA, et al. Local shear stress and brachial artery flow-mediated dilation: the Framingham Heart Study. Hypertension. 2004;44:134–139
  37. Matsuda K, Teragawa H, Fukuda Y, et al. Response of the left anterior descending coronary artery to acetylcholine in patients with chest pain and angiographically normal coronary arteries. Am J Cardiol. 2003;92:1394–1398
  38. Fukuda Y, Teragawa H, Matsuda K, Yamagata T, Matsuura H, Chayama K. Tetrahydrobiopterin restores endothelial function of coronary arteries in patients with hypercholesterolaemia. Heart. 2002;87:264–269
  39. Eleuteri E, Scapellato F, Temporelli PL, Giannuzzi P. Evaluation of the left anterior descending coronary artery flow velocity by transthoracic echo-Doppler without contrast enhancement. Ital Heart J. 2002;3:520–524
  40. Liepsch D. An introduction to biofluid mechanics–basic models and applications. J Biomech. 2002;35:415–435
  41. Dammers R, Tordoir JH, Hameleers JM, Kitslaar PJ, Hoeks AP. Brachial artery shear stress is independent of gender or age and does not modify vessel wall mechanical properties. Ultrasound Med Biol. 2002;28:1015–1022
  42. Long Q, Xu XY, Ariff B, Thom SA, Hughes AD, Stanton AV. Reconstruction of blood flow patterns in a human carotid bifurcation: a combined CFD and MRI study. J Magn Reson Imaging. 2000;11:299–311
  43. Struijk PC, Stewart PA, Fernando KL, et al. Wall shear stress and related hemodynamic parameters in the fetal descending aorta derived from color Doppler velocity profiles. Ultrasound Med Biol. 2005;31:1441–1450
  44. Bots ML, Grobbee DE, Hofman A, Witteman JC. Common carotid intima-media thickness and risk of acute myocardial infarction: the role of lumen diameter. Stroke. 2005;36:762–767
  45. Pohl U, Holtz J, Busse R, Bassenge E. Crucial role of endothelium in the vasodilator response to increased flow in vivo. Hypertension. 1986;8:37–44
  46. Serhatlioglu S, Kiris A, Kocakoc E, Canpolat I, Bozgeyik Z, Han MC. Evaluation of the effects of sildenafil citrate (Viagra) on canine renal artery, carotid and aortic blood flow with the aid of color Doppler sonography. Urol Int. 2003;71:103–107
  47. Lie M, Sejersted OM, Kiil F. Local regulation of vascular cross section during changes in femoral arterial blood flow in dogs. Circ Res. 1970;27:727–737
  48. Lee K, Choi M, Yoon J, Jung J. Spectral waveform analysis of major arteries in conscious dogs by Doppler ultrasonography. Vet Radiol Ultrasound. 2004;45:166–171
  49. Sumitra M, Manikandan P, Rao KV, Nayeem M, Manohar BM, Puvanakrishnan R. Cardiorespiratory effects of diazepam-ketamine, xylazine-ketamine and thiopentone anesthesia in male Wistar rats—a comparative analysis. Life Sci. 2004;75:1887–1896
  50. Janssen BJ, De Celle T, Debets JJ, Brouns AE, Callahan MF, Smith TL. Effects of anesthetics on systemic hemodynamics in mice. Am J Physiol Heart Circ Physiol. 2004;287:H1618–H1624
  51. Uylings HB. Optimization of diameters and bifurcation angles in lung and vascular tree structures. Bull Math Biol. 1977;39:509–520
  52. Gafiychuk VV, Lubashevsky IA. On the principles of the vascular network branching. J Theor Biol. 2001;212:1–9
  53. Zamir M, Sinclair P, Wonnacott TH. Relation between diameter and flow in major branches of the arch of the aorta. J Biomech. 1992;25:1303–1310
  54. Karau KL, Krenz GS, Dawson CA. Branching exponent heterogeneity and wall shear stress distribution in vascular trees. Am J Physiol Heart Circ Physiol. 2001;280:H1256–H1263
  55. Morris TE, Mattox PA, Shipley GD, Wagner CR, Hosenpud JD. The pattern of cytokine messenger RNA expression in human aortic endothelial cells is different from that of human umbilical vein endothelial cells. Transpl Immunol. 1993;1:137–142
  56. Chen BP, Li YS, Zhao Y, et al. DNA microarray analysis of gene expression in endothelial cells in response to 24-h shear stress. Physiol Genomics. 2001;7:55–63
  57. Garcia-Cardena G, Comander J, Anderson KR, Blackman BR, Gimbrone MA. Biomechanical activation of vascular endothelium as a determinant of its functional phenotype. Proc Natl Acad Sci USA. 2001;98:4478–4485
  58. Mochizuki S, Vink H, Hiramatsu O, et al. Role of hyaluronic acid glycosaminoglycans in shear-induced endothelium-derived nitric oxide release. Am J Physiol Heart Circ Physiol. 2003;285:H722–H726
  59. Gouverneur M, Spaan JA, Pannekoek H, Fontijn RD, Vink H. Fluid shear stress stimulates incorporation of hyaluronan into endothelial cell glycocalyx. Am J Physiol Heart Circ Physiol. 2006;290:H458–H462
  60. Tzima E, Irani-Tehrani M, Kiosses WB, et al. A mechanosensory complex that mediates the endothelial cell response to fluid shear stress. Nature. 2005;437:426–431
  61. Cheng C, van Haperen R, de Waard M, et al. Shear stress affects the intracellular distribution of eNOS: direct demonstration by a novel in vivo technique. Blood. 2005;106:3691–3698
  62. Illi B, Nanni S, Scopece A, et al. Shear stress-mediated chromatin remodeling provides molecular basis for flow-dependent regulation of gene expression. Circ Res. 2003;93:155–161
  63. Illi B, Scopece A, Nanni S, et al. Epigenetic histone modification and cardiovascular lineage programming in mouse embryonic stem cells exposed to laminar shear stress. Circ Res. 2005;96:501–508
  64. Zderic V, Keshavarzi A, Noble ML, et al. Hemorrhage control in arteries using high-intensity focused ultrasound: a survival study. Ultrasonics. 2006;44:46–53
  65. Tronc F, Wassef M, Esposito B, et al. Role of NO in flow-induced remodeling of the rabbit common carotid artery. Arterioscler Thromb Vasc Biol. 1996;16:1256–1262
  66. Walpola PL, Gotlieb AI, Langille BL. Monocyte adhesion and changes in endothelial cell number, morphology, and F-actin distribution elicited by low shear stress in vivo. Am J Pathol. 1993;142:1392–1400
  67. Langille BL, Bendeck MP, Keeley FW. Adaptations of carotid arteries of young and mature rabbits to reduced carotid blood flow. Am J Physiol. 1989;256:H931–H939
  68. Sho E, Nanjo H, Sho M, et al. Arterial enlargement, tortuosity, and intimal thickening in response to sequential exposure to high and low wall shear stress. J Vasc Surg. 2004;39:601–612
  69. Masuda H, Zhuang YJ, Singh TM, et al. Adaptive remodeling of internal elastic lamina and endothelial lining during flow-induced arterial enlargement. Arterioscler Thromb Vasc Biol. 1999;19:2298–2307
  70. Lu X, Zhao JB, Wang GR, Gregersen H, Kassab GS. Remodeling of the zero-stress state of femoral arteries in response to flow overload. Am J Physiol Heart Circ Physiol. 2001;280:H1547–H1559
  71. Ibrahim J, Miyashiro JK, Berk BC. Shear stress is differentially regulated among inbred rat strains. Circ Res. 2003;92:1001–1009
  72. Miyashiro JK, Poppa V, Berk BC. Flow-induced vascular remodeling in the rat carotid artery diminishes with age. Circ Res. 1997;81:311–319
  73. Tohda K, Masuda H, Kawamura K, Shozawa T. Difference in dilatation between endothelium-preserved and -desquamated segments in the flow-loaded rat common carotid artery. Arterioscler Thromb. 1992;12:519–528
  74. Hartley CJ, Reddy AK, Madala S, et al. Hemodynamic changes in apolipoprotein E-knockout mice. Am J Physiol Heart Circ Physiol. 2000;279:H2326–H2334
  75. Korshunov VA, Berk BC. Flow-induced vascular remodeling in the mouse: a model for carotid intima-media thickening. Arterioscler Thromb Vasc Biol. 2003;23:2185–2191
  76. Castier Y, Brandes RP, Leseche G, Tedgui A, Lehoux S. p47phox-dependent NADPH oxidase regulates flow-induced vascular remodeling. Circ Res. 2005;97:533–540
  77. Rudic RD, Bucci M, Fulton D, Segal SS, Sessa WC. Temporal events underlying arterial remodeling after chronic flow reduction in mice: correlation of structural changes with a deficit in basal nitric oxide synthesis. Circ Res. 2000;86:1160–1166
  78. Sullivan CJ, Hoying JB. Flow-dependent remodeling in the carotid artery of fibroblast growth factor-2 knockout mice. Arterioscler Thromb Vasc Biol. 2002;22:1100–1105
  79. Schiffers PM, Henrion D, Boulanger CM, et al. Altered flow-induced arterial remodeling in vimentin-deficient mice. Arterioscler Thromb Vasc Biol. 2000;20:611–616

PII: S0021-9150(06)00695-2

doi: 10.1016/j.atherosclerosis.2006.11.019

Atherosclerosis
Volume 195, Issue 2 , Pages 225-235 , December 2007