Generic placeholder image

Current Cardiology Reviews

Editor-in-Chief

ISSN (Print): 1573-403X
ISSN (Online): 1875-6557

Review Article

Biomechanical Forces and Atherosclerosis: From Mechanism to Diagnosis and Treatment

Author(s): Vadim V. Genkel*, Alla S. Kuznetcova and Igor I. Shaposhnik

Volume 16, Issue 3, 2020

Page: [187 - 197] Pages: 11

DOI: 10.2174/1573403X15666190730095153

Price: $65

Abstract

The article provides an overview of current views on the role of biomechanical forces in the pathogenesis of atherosclerosis. The importance of biomechanical forces in maintaining vascular homeostasis is considered. We provide descriptions of mechanosensing and mechanotransduction. The roles of wall shear stress and circumferential wall stress in the initiation, progression and destabilization of atherosclerotic plaque are described. The data on the possibilities of assessing biomechanical factors in clinical practice and the clinical significance of this approach are presented. The article concludes with a discussion on current therapeutic approaches based on the modulation of biomechanical forces.

Keywords: Atherosclerosis, wall shear stress, peripheral artery disease, circumferential wall stress, mechanosensing, plaque progression.

Graphical Abstract
[1]
Bäck M, Hansson GK. Anti-inflammatory therapies for atherosclerosis. Nat Rev Cardiol 2015; 12(4): 199-211.
[http://dx.doi.org/10.1038/nrcardio.2015.5] [PMID: 25666404]
[2]
Brown AJ, Teng Z, Evans PC, Gillard JH, Samady H, Bennett MR. Role of biomechanical forces in the natural history of coronary atherosclerosis. Nat Rev Cardiol 2016; 13(4): 210-20.
[http://dx.doi.org/10.1038/nrcardio.2015.203] [PMID: 26822720]
[3]
Kwak BR, Bäck M, Bochaton-Piallat ML, et al. et al. Biomechanical factors in atherosclerosis: Mechanisms and clinical implications. Eur Heart J 2014; 35(43): 3013-3020, 3020a-3020d..
[http://dx.doi.org/10.1093/eurheartj/ehu353] [PMID: 25230814]
[4]
Papaioannou TG, Stefanadis C. Vascular wall shear stress: Basic principles and methods. Hellenic J Cardiol 2005; 46(1): 9-15.
[PMID: 15807389]
[5]
Ricci S, Swillens A, Ramalli A, Segers P, Tortoli P. Wall shear rate measurement: Validation of a new method through multiphysics simulations. IEEE Trans Ultrason Ferroelectr Freq Control 2017; 64(1): 66-77.
[http://dx.doi.org/10.1109/TUFFC.2016.2608442] [PMID: 28092504]
[6]
Parker BA, Trehearn TL, Meendering JR. Pick your poiseuille: Normalizing the shear stimulus in studies of flow-mediated dilation. J Appl Physiol 2009; 107(4): 1357-9.
[7]
Reneman RS, Hoeks AP. Wall shear stress as measured in vivo: Consequences for the design of the arterial system. Med Biol Eng Comput 2008; 46(5): 499-507.
[http://dx.doi.org/10.1007/s11517-008-0330-2] [PMID: 18324431]
[8]
Martino F, Perestrelo AR, Vinarský V, Pagliari S, Forte G. Cellular mechanotransduction: From tension to function. Front Physiol 2018; 9: 824.
[http://dx.doi.org/10.3389/fphys.2018.00824] [PMID: 30026699]
[9]
Holle AW, Engler AJ. More than a feeling: Discovering, understanding, and influencing mechanosensing pathways. Curr Opin Biotechnol 2011; 22(5): 648-54.
[http://dx.doi.org/10.1016/j.copbio.2011.04.007] [PMID: 21536426]
[10]
Fedorchak GR, Kaminski A, Lammerding J. Cellular mechanosensing: Getting to the nucleus of it all. Prog Biophys Mol Biol 2014; 115(2-3): 76-92.
[http://dx.doi.org/10.1016/j.pbiomolbio.2014.06.009] [PMID: 25008017]
[11]
Fang Y, Wu D, Birukov KG. Mechanosensing and mechanoregulation of endothelial cell functions. Compr Physiol 2019; 9(2): 873-904.
[http://dx.doi.org/10.1002/cphy.c180020] [PMID: 30873580]
[12]
Liu YS, Lee OK. In search of the pivot point of mechanotransduction: Mechanosensing of stem cells. Cell Transplant 2014; 23(1): 1-11.
[http://dx.doi.org/10.3727/096368912X659925] [PMID: 24439034]
[13]
Chatterjee S. Endothelial mechanotransduction, redox signaling and the regulation of vascular inflammatory pathways. Front Physiol 2018; 9: 524.
[http://dx.doi.org/10.3389/fphys.2018.00524] [PMID: 29930512]
[14]
Abe J, Berk BC. Novel mechanisms of endothelial mechanotransduction. Arterioscler Thromb Vasc Biol 2014; 34(11): 2378-86.
[http://dx.doi.org/10.1161/ATVBAHA.114.303428] [PMID: 25301843]
[15]
Chistiakov DA, Orekhov AN, Bobryshev YV. Effects of shear stress on endothelial cells: Go with the flow. Acta Physiol (Oxf) 2017; 219(2): 382-408.
[http://dx.doi.org/10.1111/apha.12725] [PMID: 27246807]
[16]
Galie PA, Nguyen DH, Choi CK, Cohen DM, Janmey PA, Chen CS. Fluid shear stress threshold regulates angiogenic sprouting. Proc Natl Acad Sci USA 2014; 111(22): 7968-73.
[http://dx.doi.org/10.1073/pnas.1310842111] [PMID: 24843171]
[17]
Rodríguez I, González M. Physiological mechanisms of vascular response induced by shear stress and effect of exercise in systemic and placental circulation. Front Pharmacol 2014; 5: 209.
[http://dx.doi.org/10.3389/fphar.2014.00209] [PMID: 25278895]
[18]
Wragg JW, Durant S, McGettrick HM, Sample KM, Egginton S, Bicknell R. Shear stress regulated gene expression and angiogenesis in vascular endothelium. Microcirculation 2014; 21(4): 290-300.
[http://dx.doi.org/10.1111/micc.12119] [PMID: 24471792]
[19]
Ajami NE, Gupta S, Maurya MR, et al. Systems biology analysis of longitudinal functional response of endothelial cells to shear stress. Proc Natl Acad Sci USA 2017; 114(41): 10990-5.
[http://dx.doi.org/10.1073/pnas.1707517114] [PMID: 28973892]
[20]
Moskovtsev AA, Kolesov DV, Mylnikova AN, et al. et al. Endothelial shear stress responses: Mechanotransduction, cell stress and adaptation. PatologicheskayaFiziologiya i Eksperimental`naya terapiya Pathol Physiol Exp Ther Russ J 2017; 61(4): 112-25.
[21]
Kadam AA, Gersch RP, Rosengart TK, Frame MD. Inflammatory monocyte response due to altered wall shear stress in an isolated femoral artery model. J Biol Methods 2019; 6(1) e109
[http://dx.doi.org/10.14440/jbm.2019.274] [PMID: 31453258]
[22]
Mitchell MJ, Lin KS, King MR. Fluid shear stress increases neutrophil activation via platelet-activating factor. Biophys J 2014; 106(10): 2243-53.
[http://dx.doi.org/10.1016/j.bpj.2014.04.001] [PMID: 24853753]
[23]
Niethammer P. Neutrophil mechanotransduction: A GEF to sense fluid shear stress. J Cell Biol 2016; 215(1): 13-4.
[24]
Fine N, Dimitriou ID, Rullo J, et al. GEF-H1 is necessary for neutrophil shear stress-induced migration during inflammation. J Cell Biol 2016; 215(1): 107-19.
[25]
Qin WD, Mi SH, Li C, et al. Low shear stress induced HMGB1 translocation and release via PECAM-1/PARP-1 pathway to induce inflammation response. PLoS One 2015; 10(3) e0120586
[26]
Harrison DL, Fang Y, Huang J. T-Cell mechanobiology: Force sensation, potentiation, and translation. Front Phys 2019; 7: 45.
[http://dx.doi.org/10.3389/fphy.2019.00045] [PMID: 32601597]
[27]
Dominguez GA, Anderson NR, Hammer DA. The direction of migration of T-lymphocytes under flow depends upon which adhesion receptors are engaged. Integr Biol 2015; 7(3): 345-55.
[http://dx.doi.org/10.1039/C4IB00201F] [PMID: 25674729]
[28]
Jufri NF, Mohamedali A, Avolio A, Baker MS. Mechanical stretch: physiological and pathological implications for human vascular endothelial cells. Vasc Cell 2015; 7: 8.
[http://dx.doi.org/10.1186/s13221-015-0033-z] [PMID: 26388991]
[29]
Caro CG, Fitz-Gerald JM, Schroter RC. Arterial wall shear and distribution of early atheroma in man. Nature 1969; 223(5211): 1159-60.
[http://dx.doi.org/10.1038/2231159a0] [PMID: 5810692]
[30]
Li X, Yang Q, Wang Z, Wei D. Shear stress in atherosclerotic plaque determination. DNA Cell Biol 2014; 33(12): 830-8.
[http://dx.doi.org/10.1089/dna.2014.2480] [PMID: 25165867]
[31]
Harloff A, Markl M. In vivo wall shear stress patterns in carotid bifurcations assessed by 4D MRI. Perspec Med 2012; 1(1-12): 137- 8.
[32]
Otero-Cacho A, Aymerich M, Flores-Arias MT, et al. Determination of hemodynamic risk for vascular disease in planar artery bifurcations. Sci Rep 2018; 8(1): 2795.
[http://dx.doi.org/10.1038/s41598-018-21126-1] [PMID: 29434229]
[33]
Markl M, Wegent F, Zech T, et al. In vivo wall shear stress distribution in the carotid artery: Effect of bifurcation geometry, internal carotid artery stenosis, and recanalization therapy. Circ Cardiovasc Imaging 2010; 3(6): 647-55.
[http://dx.doi.org/10.1161/CIRCIMAGING.110.958504] [PMID: 20847189]
[34]
Dhawan SS, Avati Nanjundappa RP, Branch JR, et al. Shear stress and plaque development. Expert Rev Cardiovasc Ther 2010; 8(4): 545-56.
[http://dx.doi.org/10.1586/erc.10.28] [PMID: 20397828]
[35]
van der Giessen AG, Wentzel JJ, Meijboom WB, et al. Plaque and shear stress distribution in human coronary bifurcations: A multislice computed tomography study. EuroIntervention 2009; 4(5): 654-61.
[http://dx.doi.org/10.4244/EIJV4I5A109] [PMID: 19378688]
[36]
Kuhlmann MT, Cuhlmann S, Hoppe I, et al. Implantation of a carotid cuff for triggering shear-stress induced atherosclerosis in mice. J Vis Exp 2012; 13(59): 3308.
[http://dx.doi.org/10.3791/3308] [PMID: 22294044]
[37]
Carallo C, Tripolino C, De Franceschi MS, Irace C, Xu XY, Gnasso A. Carotid endothelial shear stress reduction with aging is associated with plaque development in twelve years. Atherosclerosis 2016; 251: 63-9.
[http://dx.doi.org/10.1016/j.atherosclerosis.2016.05.048] [PMID: 27266823]
[38]
Arzani A, Gambaruto AM, Chen G, Shadden SC. Wall shear stress exposure time: A Lagrangian measure of near-wall stagnation and concentration in cardiovascular flows. Biomech Model Mechanobiol 2017; 16(3): 787-803.
[http://dx.doi.org/10.1007/s10237-016-0853-7] [PMID: 27858174]
[39]
Vozzi F, Campolo J, Cozzi L, et al. Computing of low shear stress-driven endothelial gene network involved in early stages of atherosclerotic process. BioMed Res Int 2018; 2018 5359830
[http://dx.doi.org/10.1155/2018/5359830] [PMID: 30356351]
[40]
Mahmoud MM, Serbanovic-Canic J, Feng S, et al. Shear stress induces endothelial-to-mesenchymal transition via the transcription factor Snail. Sci Rep 2017; 7(1): 3375.
[http://dx.doi.org/10.1038/s41598-017-03532-z] [PMID: 28611395]
[41]
Chiu JJ, Usami S, Chien S. Vascular endothelial responses to altered shear stress: Pathologic implications for atherosclerosis. Ann Med 2009; 41(1): 19-28.
[http://dx.doi.org/10.1080/07853890802186921] [PMID: 18608132]
[42]
Simmons RD, Kumar S, Thabet SR, Sur S, Jo H. Omics-based approaches to understand mechanosensitive endothelial biology and atherosclerosis. Wiley Interdiscip Rev Syst Biol Med 2016; 8(5): 378-401.
[http://dx.doi.org/10.1002/wsbm.1344] [PMID: 27341633]
[43]
Baeyens N, Bandyopadhyay C, Coon BG, Yun S, Schwartz MA. Endothelial fluid shear stress sensing in vascular health and disease. J Clin Invest 2016; 126(3): 821-8.
[http://dx.doi.org/10.1172/JCI83083] [PMID: 26928035]
[44]
Hung OY, Brown AJ, Ahn SG, Veneziani A, Giddens DP, Samady H. Association of wall shear stress with coronary plaque progression and transformation. Interv Cardiol Clin 2015; 4(4): 491-502.
[http://dx.doi.org/10.1016/j.iccl.2015.06.009] [PMID: 28581935]
[45]
Stone PH, Coskun AU, Kinlay S, et al. Regions of low endothelial shear stress are the sites where coronary plaque progresses and vascular remodelling occurs in humans: An in vivo serial study. Eur Heart J 2007; 28(6): 705-10.
[http://dx.doi.org/10.1093/eurheartj/ehl575] [PMID: 17347172]
[46]
Stone PH, Saito S, Takahashi S, et al. PREDICTION Investigators. Prediction of progression of coronary artery disease and clinical outcomes using vascular profiling of endothelial shear stress and arterial plaque characteristics: The prediction study. Circulation 2012; 126(2): 172-81.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.112.096438] [PMID: 22723305]
[47]
Liu X, Wu G, Xu C, et al. Prediction of coronary plaque progression using biomechanical factors and vascular characteristics based on computed tomography angiography. Comput Assist Surg (Abingdon) 2017; 22(1): 286-94.
[http://dx.doi.org/10.1080/24699322.2017.1389407] [PMID: 29032716]
[48]
Parodi O, Exarchos TP, Marraccini P, et al. Patient-specific prediction of coronary plaque growth from CTA angiography: A multiscale model for plaque formation and progression. IEEE Trans Inf Technol Biomed 2012; 16(5): 952-65.
[http://dx.doi.org/10.1109/TITB.2012.2201732] [PMID: 22665513]
[49]
Samady H, Eshtehardi P, McDaniel MC, et al. Coronary artery wall shear stress is associated with progression and transformation of atherosclerotic plaque and arterial remodeling in patients with coronary artery disease. Circulation 2011; 124(7): 779-88.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.111.021824] [PMID: 21788584]
[50]
Shishikura D, Sidharta SL, Honda S, et al. The relationship between segmental wall shear stress and lipid core plaque derived from near-infrared spectroscopy. Atherosclerosis 2018; 275: 68-73.
[http://dx.doi.org/10.1016/j.atherosclerosis.2018.04.022] [PMID: 29864607]
[51]
Corban MT, Eshtehardi P, Suo J, et al. Combination of plaque burden, wall shear stress, and plaque phenotype has incremental value for prediction of coronary atherosclerotic plaque progression and vulnerability. Atherosclerosis 2014; 232(2): 271-6.
[http://dx.doi.org/10.1016/j.atherosclerosis.2013.11.049] [PMID: 24468138]
[52]
Murata N, Hiro T, Takayama T, et al. High shear stress on the coronary arterial wall is related to computed tomography-derived high-risk plaque: A three-dimensional computed tomography and color-coded tissue-characterizing intravascular ultrasonography study. Heart Vessels 2019; 34(9): 1429-39.
[http://dx.doi.org/10.1007/s00380-019-01389-y] [PMID: 30976923]
[53]
Boyle JJ, Weissberg PL, Bennett MR. Human macrophage-induced vascular smooth muscle cell apoptosis requires NO enhancement of Fas/Fas-L interactions. Arterioscler Thromb Vasc Biol 2002; 22(10): 1624-30.
[http://dx.doi.org/10.1161/01.ATV.0000033517.48444.1A] [PMID: 12377740]
[54]
Kok AM, Molony DS, Timmins LH, et al. The influence of multidirectional shear stress on plaque progression and composition changes in human coronary arteries. EuroIntervention 2019; 15(8): 692-9.
[http://dx.doi.org/10.4244/EIJ-D-18-00529]
[55]
Koskinas KC, Chatzizisis YS, Baker AB, Edelman ER, Stone PH, Feldman CL. The role of low endothelial shear stress in the conversion of atherosclerotic lesions from stable to unstable plaque. Curr Opin Cardiol 2009; 24(6): 580-90.
[http://dx.doi.org/10.1097/HCO.0b013e328331630b] [PMID: 19809311]
[56]
Costopoulos C, Timmins LH, Huang Y, et al. Impact of combined plaque structural stress and wall shear stress on coronary plaque progression, regression, and changes in composition. Eur Heart J 2019; 40(18): 1411-22.
[http://dx.doi.org/10.1093/eurheartj/ehz132] [PMID: 30907406]
[57]
Widlansky ME. Shear stress and flow-mediated dilation: All shear responses are not created equally. Am J Physiol Heart Circ Physiol 2009; 296(1): H31-2.
[http://dx.doi.org/10.1152/ajpheart.01187.2008] [PMID: 19028789]
[58]
Nishiyama SK, Walter Wray D, Berkstresser K, Ramaswamy M, Richardson RS. Limb-specific differences in flow-mediated dilation: The role of shear rate. J Appl Physiol 2007; 103(3): 843-51.
[http://dx.doi.org/10.1152/japplphysiol.00273.2007] [PMID: 17556495]
[59]
Zhang B, Ma Y, Ding F. Evaluation of spatial distribution and characterization of wall shear stress in carotid sinus based on two-dimensional color Doppler imaging. Biomed Eng Online 2018; 17(1): 141.
[http://dx.doi.org/10.1186/s12938-018-0589-y] [PMID: 30340641]
[60]
Gates PE, Gurung A, Mazzaro L, et al. Measurement of wall shear stress exerted by flowing blood in the human carotid artery: Ultrasound doppler velocimetry and echo particle image velocimetry. Ultrasound Med Biol 2018; 44(7): 1392-401.
[http://dx.doi.org/10.1016/j.ultrasmedbio.2018.02.013] [PMID: 29678322]
[61]
Peng SL, Shih CT, Huang CW, Chiu SC, Shen WC. Optimized analysis of blood flow and wall shear stress in the common carotid artery of rat model by phase-contrast MRI. Sci Rep 2017; 7(1): 5253.
[http://dx.doi.org/10.1038/s41598-017-05606-4] [PMID: 28701695]
[62]
Pantos I, Patatoukas G, Efstathopoulos EP, Katritsis D. In vivo wall shear stress measurements using phase-contrast MRI. Expert Rev Cardiovasc Ther 2007; 5(5): 927-38.
[http://dx.doi.org/10.1586/14779072.5.5.927] [PMID: 17867922]
[63]
Ha H, Kim GB, Kweon J, et al. Hemodynamic measurement using four-dimensional phase-contrast MRI: Quantification of hemodynamic parameters and clinical applications. Korean J Radiol 2016; 17(4): 445-62.
[http://dx.doi.org/10.3348/kjr.2016.17.4.445] [PMID: 27390537]
[64]
van der Giessen AG, Schaap M, Gijsen FJ, et al. 3D fusion of intravascular ultrasound and coronary computed tomography for in-vivo wall shear stress analysis: A feasibility study. Int J Cardiovasc Imaging 2010; 26(7): 781-96.
[http://dx.doi.org/10.1007/s10554-009-9546-y] [PMID: 19946749]
[65]
Itatani K, Miyazaki S, Furusawa T, et al. New imaging tools in cardiovascular medicine: Computational fluid dynamics and 4D flow MRI. Gen Thorac Cardiovasc Surg 2017; 65(11): 611-21.
[http://dx.doi.org/10.1007/s11748-017-0834-5] [PMID: 28929446]
[66]
Steinman DA. Image-based computational fluid dynamics: A new paradigm for monitoring hemodynamics and atherosclerosis. Curr Drug Targets Cardiovasc Haematol Disord 2004; 4(2): 183-97.
[http://dx.doi.org/10.2174/1568006043336302] [PMID: 15180490]
[67]
Xing R, Moerman AM, Ridwan Y, et al. Temporal and spatial changes in wall shear stress during atherosclerotic plaque progression in mice. R Soc Open Sci 2018; 5(3) 171447
[http://dx.doi.org/10.1098/rsos.171447] [PMID: 29657758]
[68]
Zhang B, Gu J, Qian M, Niu L, Zhou H, Ghista D. Correlation between quantitative analysis of wall shear stress and intima-media thickness in atherosclerosis development in carotid arteries. Biomed Eng Online 2017; 16(1): 137.
[http://dx.doi.org/10.1186/s12938-017-0425-9] [PMID: 29208019]
[69]
Genkel VV, Salashenko AO, Shamaeva TN, Sumerkina VA, Shaposhnik II. Association between carotid wall shear rate and arterial stiffness in patients with hypertension and atherosclerosis of peripheral arteries. Int J Vasc Med 2018; 2018 6486234
[http://dx.doi.org/10.1155/2018/6486234] [PMID: 30155305]
[70]
Cho KI, Kim BH, Kim HS, Heo JH. Low carotid artery wall shear stress is associated with significant coronary artery disease in patients with chest pain. J Atheroscler Thromb 2016; 23(3): 297-308.
[http://dx.doi.org/10.5551/jat.31377] [PMID: 26477886]
[71]
Ng J, Bourantas CV, Torii R, et al. Local hemodynamic forces after stenting: Implications on restenosis and thrombosis. Arterioscler Thromb Vasc Biol 2017; 37(12): 2231-42.
[http://dx.doi.org/10.1161/ATVBAHA.117.309728] [PMID: 29122816]
[72]
Papafaklis MI, Bourantas CV, Theodorakis PE, et al. The effect of shear stress on neointimal response following sirolimus- and paclitaxel-eluting stent implantation compared with bare-metal stents in humans. JACC Cardiovasc Interv 2010; 3(11): 1181-9.
[http://dx.doi.org/10.1016/j.jcin.2010.08.018] [PMID: 21087755]
[73]
Torii R, Stettler R, Räber L, et al. Implications of the local hemodynamic forces on the formation and destabilization of neoatherosclerotic lesions. Int J Cardiol 2018; 272: 7-12.
[http://dx.doi.org/10.1016/j.ijcard.2018.06.065] [PMID: 30293579]
[74]
Tenekecioglu E, Torii R, Katagiri Y, et al. Post-implantation shear stress assessment: An emerging tool for differentiation of bioresorbable scaffolds. Int J Cardiovasc Imaging 2019; 35(3): 409-18.
[http://dx.doi.org/10.1007/s10554-018-1481-3] [PMID: 30426299]
[75]
Guo Y, Wei F, Wang J, et al. Carotid artery wall shear stress is independently correlated with renal function in the elderly. Oncotarget 2018; 9(4): 5251-62.
[http://dx.doi.org/10.18632/oncotarget.23825] [PMID: 29435176]
[76]
Liu Z, Zhao Y, Wang X, et al. Low carotid artery wall shear stress is independently associated with brain white-matter hyperintensities and cognitive impairment in older patients. Atherosclerosis 2016; 247: 78-86.
[http://dx.doi.org/10.1016/j.atherosclerosis.2016.02.003] [PMID: 26868512]
[77]
Zhang H, Liu H, Dong Y, et al. Low carotid wall shear stress independently accelerates the progression of cognitive impairment and white matter lesions in the elderly. Oncotarget 2017; 9(13): 11402-13.
[http://dx.doi.org/10.18632/oncotarget.23191] [PMID: 29541422]
[78]
Valen-Sendstad K, Bergersen AW, Shimogonya Y, et al. Real-world variability in the prediction of intracranial aneurysm wall shear stress: The 2015 international aneurysm CFD Challenge. Cardiovasc Eng Technol 2018; 9(4): 544-64.
[http://dx.doi.org/10.1007/s13239-018-00374-2] [PMID: 30203115]
[79]
Grewal N, Gittenberger-de Groot AC. Wall shear stress directional abnormalities in BAV aortas: Toward a new hemodynamic predictor of aortopathy? Front Physiol 2019; 10(10): 225.
[http://dx.doi.org/10.3389/fphys.2019.00225] [PMID: 30941050]
[80]
Chen HY, Hermiller J, Sinha AK, Sturek M, Zhu L, Kassab GS. Effects of stent sizing on endothelial and vessel wall stress: Potential mechanisms for in-stent restenosis. J Appl Physiol 2009; 106(5): 1686-91.
[http://dx.doi.org/10.1152/japplphysiol.91519.2008] [PMID: 19299567]
[81]
Wentzel JJ, Gijsen FJH, Schuurbiers JCH, van der Steen AFW, Serruys PW. The influence of shear stress on in-stent restenosis and thrombosis. EuroIntervention 2008; 4(Suppl. C): C27-32.
[PMID: 19202688]
[82]
Koskinas KC, Chatzizisis YS, Antoniadis AP, Giannoglou GD. Role of endothelial shear stress in stent restenosis and thrombosis: Pathophysiologic mechanisms and implications for clinical translation. J Am Coll Cardiol 2012; 59(15): 1337-49.
[83]
Chesnutt JK, Han HC. Computational simulation of platelet interactions in the initiation of stent thrombosis due to stent malapposition. Phys Biol 2016; 13(1) 016001
[http://dx.doi.org/10.1088/1478-3975/13/1/016001] [PMID: 26790093]
[84]
Kokkalis E, Aristokleous N, Houston JG. Haemodynamics and flow modification stents for peripheral arterial disease: A review. Ann Biomed Eng 2016; 44(2): 466-76.
[http://dx.doi.org/10.1007/s10439-015-1483-4] [PMID: 26467554]
[85]
Stonebridge PA, Vermassen F, Dick J, Belch JJF, Houston G. Spiral laminar flow prosthetic bypass graft: Medium-term results from a first-in-man structured registry study. Ann Vasc Surg 2012; 26(8): 1093-9.
[http://dx.doi.org/10.1016/j.avsg.2012.02.001] [PMID: 22682930]
[86]
Caro CG, Cheshire NJ, Watkins N. Preliminary comparative study of small amplitude helical and conventional ePTFE arteriovenous shunts in pigs. J R Soc Interface 2005; 2(3): 261-6.
[http://dx.doi.org/10.1098/rsif.2005.0044] [PMID: 16849184]
[87]
Huijbregts HJ, Blankestijn PJ, Caro CG, et al. A helical PTFE arteriovenous access graft to swirl flow across the distal anastomosis: Results of a preliminary clinical study. Eur J Vasc Endovasc Surg 2007; 33(4): 472-5.
[http://dx.doi.org/10.1016/j.ejvs.2006.10.028] [PMID: 17161962]
[88]
Zeller T, Gaines PA, Ansel GM, Caro CG. Helical centerline stent improves patency: Two-year results from the randomized mimics trial. Circ Cardiovasc Interv 2016; 9(6) 002930
[http://dx.doi.org/10.1161/CIRCINTERVENTIONS.115.002930] [PMID: 27208046]
[89]
Ruiz-Soler A, Kabinejadian F, Slevin MA, Bartolo PJ, Keshmiri A. Optimisation of a novel spiral-inducing bypass graft using computational fluid dynamics. Sci Rep 2017; 7(1): 1865.
[http://dx.doi.org/10.1038/s41598-017-01930-x] [PMID: 28500311]
[90]
Sullivan TM, Zeller T, Nakamura M, Caro CG, Lichtenberg M. Swirling flow and wall shear: Evaluating the biomimics 3d helical centerline stent for the femoropopliteal segment. Int J Vasc Med 2018; 2018 9795174
[http://dx.doi.org/10.1155/2018/9795174] [PMID: 29682350]
[91]
Kabinejadian F, McElroy M, Ruiz-Soler A, et al. Numerical assessment of novel helical/spiral grafts with improved hemodynamics for distal graft anastomoses. PLoS One 2016; 11(11) e0165892
[http://dx.doi.org/10.1371/journal.pone.0165892] [PMID: 27861485]
[92]
Bondke Persson A, Buschmann EE, Lindhorst R, et al. Therapeutic arteriogenesis in peripheral arterial disease: Combining intervention and passive training. Vasa 2011; 40(3): 177-87.
[http://dx.doi.org/10.1024/0301-1526/a000092] [PMID: 21638246]
[93]
Padilla J, Simmons GH, Bender SB, Arce-Esquivel AA, Whyte JJ, Laughlin MH. Vascular effects of exercise: Endothelial adaptations beyond active muscle beds. Physiology (Bethesda) 2011; 26(3): 132-45.
[http://dx.doi.org/10.1152/physiol.00052.2010] [PMID: 21670160]
[94]
Picard F, Panagiotidou P, Wolf-Pütz A, et al. Individual shear rate therapy (ISRT)-further development of external counterpulsation for decreasing blood pressure in patients with symptomatic coronary artery disease (CAD). Hypertens Res 2020; 43(3): 186-96.
[http://dx.doi.org/10.1038/s41440-019-0380-x] [PMID: 31866668]
[95]
Qin X, Deng Y, Wu D, Yu L, Huang R. Does Enhanced External Counterpulsation (EECP) Significantly affect myocardial perfusion?: A systematic review meta-analysis. PLoS One 2016; 11(4) e0151822
[96]
Bonetti PO, Holmes DR Jr, Lerman A, Barsness GW. Enhanced external counterpulsation for ischemic heart disease: What’s behind the curtain? J Am Coll Cardiol 2003; 41(11): 1918-25.
[97]
Wu G, Du Z, Hu C, et al. Angiogenic effects of long-term enhanced external counterpulsation in a dog model of myocardial infarction. Am J Physiol Heart Circ Physiol 2006; 290(1): H248-54.
[http://dx.doi.org/10.1152/ajpheart.01225.2004] [PMID: 16113071]
[98]
Wu GF, Du ZM, Hu CH, et al. Microvessel angiogenesis: A possible cardioprotective mechanism of external counterpulsation for canine myocardial infarction. Chin Med J (Engl) 2005; 118(14): 1182-9.
[99]
Eslamian F, Aslanabadi N, Mahmoudian B, Shakouri SK. Therapeutic effects of enhanced external counterpulsation on clinical sumptoms, echocardiographic measurements, perfusion scan parameters and exercise tolerance test in coronary artery disease patients with refractory angina. Int J Med Sci Public Health 2013; 2: 187-95.
[http://dx.doi.org/10.5455/ijmsph.2013.2.179-187]
[100]
Brix M, Buschmann EE, Zietzer A, et al. Long-term individual shear rate therapy counterpulsation enhances plasma nitrite release in patients with PAD. Vasa 2017; 46(1): 37-45.
[http://dx.doi.org/10.1024/0301-1526/a000600] [PMID: 27960614]
[101]
Buschmann EE, Brix M, Li L, et al. Adaptation of external counterpulsation based on individual shear rate therapy improves endothelial function and claudication distance in peripheral artery disease. Vasa 2016; 45(4): 317-24.
[http://dx.doi.org/10.1024/0301-1526/a000544] [PMID: 27428501]
[102]
Zietzer A, Buschmann EE, Janke D, et al. Acute physical exercise and long-term individual shear rate therapy increase telomerase activity in human peripheral blood mononuclear cells. Acta Physiol (Oxf) 2017; 220(2): 251-62.
[http://dx.doi.org/10.1111/apha.12820] [PMID: 27770498]
[103]
Picard F, Panagiotidou P, Wolf-Pütz A, et al. Usefulness of individual shear rate therapy, new treatment option for patients with symptomatic coronary artery disease. Am J Cardiol 2018; 121(4): 416-22.
[http://dx.doi.org/10.1016/j.amjcard.2017.11.004] [PMID: 29274808]
[104]
Peters SA, Woodward M, Rumley A, Tunstall-Pedoe HD, Lowe GD. Plasma and blood viscosity in the prediction of cardiovascular disease and mortality in the Scottish Heart Health Extended Cohort Study. Eur J Prev Cardiol 2017; 24(2): 161-7.
[http://dx.doi.org/10.1177/2047487316672004] [PMID: 27798361]
[105]
Salazar Vázquez BY, Martini J, Chávez Negrete A, et al. Cardiovascular benefits in moderate increases of blood and plasma viscosity surpass those associated with lowering viscosity: Experimental and clinical evidence. Clin Hemorheol Microcirc 2010; 44(2): 75-85.
[http://dx.doi.org/10.3233/CH-2010-1261] [PMID: 20203362]
[106]
Irace C, Casciaro F, Scavelli FB, et al. Empagliflozin influences blood viscosity and wall shear stress in subjects with type 2 diabetes mellitus compared with incretin-based therapy. Cardiovasc Diabetol 2018; 17(1): 52.
[http://dx.doi.org/10.1186/s12933-018-0695-y] [PMID: 29631585]
[107]
Niu N, Xu S, Xu Y, Little PJ, Jin ZG. Targeting mechanosensitive transcription factors in atherosclerosis. Trends Pharmacol Sci 2019; 40(4): 253-66.
[http://dx.doi.org/10.1016/j.tips.2019.02.004] [PMID: 30826122]
[108]
Parmar KM, Nambudiri V, Dai G, Larman HB, Gimbrone MA Jr, García-Cardeña G. Statins exert endothelial atheroprotective effects via the KLF2 transcription factor. J Biol Chem 2005; 280(29): 26714-9.
[http://dx.doi.org/10.1074/jbc.C500144200] [PMID: 15878865]
[109]
Zakkar M, Van der Heiden K, Luong A, et al. Activation of Nrf2 in endothelial cells protects arteries from exhibiting a proinflammatory state. Arterioscler Thromb Vasc Biol 2009; 29(11): 1851-7.
[http://dx.doi.org/10.1161/ATVBAHA.109.193375] [PMID: 19729611]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy