Wall shear rates in human and mouse arteries: Standardization of hemodynamics for in vitro blood flow assays: Communication from the ISTH SSC subcommittee on biorheology.


Journal

Journal of thrombosis and haemostasis : JTH
ISSN: 1538-7836
Titre abrégé: J Thromb Haemost
Pays: England
ID NLM: 101170508

Informations de publication

Date de publication:
02 2021
Historique:
revised: 04 11 2020
received: 16 09 2020
accepted: 05 11 2020
entrez: 16 8 2021
pubmed: 17 8 2021
medline: 25 2 2023
Statut: ppublish

Résumé

Hemodynamics play a central role in hemostasis and thrombosis by affecting all aspects linked to platelet functions and coagulation. In vitro flow devices are extensively used in basic research, pharmacological studies, antiplatelet agent screening, and development of diagnostic tools. Because hemodynamic conditions vary tremendously throughout the vascular tree and among different (patho)physiological processes, it is important to use flow conditions based on relevant biorheological reference ranges. Surprisingly, it is particularly difficult to find a concise overview of relevant hemodynamic parameters in various human and mouse vessels. To our knowledge, this is the first time an inventory of flow conditions in healthy, non-diseased, human and mouse vessels has been created. The objective of providing such a repertoire is to aid researchers in the field of hemostasis and thrombosis in choosing rheological conditions relevant in in vitro flow experiments and to promote harmonization of flow-based assays to facilitate comparative evaluations between studies. With reference to the human, we discuss relevant similarities and discrepancies in wall shear rates in the mouse, which are typically one order of magnitude greater in agreement with allometric scaling laws between species. Importantly, we bring the attention of the researchers to the fact that the relevant range of average wall shear rates in human arteries where clinically relevant arterial thrombosis occurs may fall as low as 100 to 200 s

Identifiants

pubmed: 34396692
doi: 10.1111/jth.15174
pii: S1538-7836(22)00658-4
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

588-595

Informations de copyright

© 2020 International Society on Thrombosis and Haemostasis.

Références

Nesbitt WS, Mangin P, Salem HH, Jackson SP. The impact of blood rheology on the molecular and cellular events underlying arterial thrombosis. J Mol Med (Berl). 2006;84(12):989‐995.
Rana K, Neeves KB. Blood flow and mass transfer regulation of coagulation. Blood Rev. 2016;30(5):357‐368.
Mangin PH, Gardiner EE, Nesbitt WS, et al. In vitro flow based systems to study platelet function and thrombus formation: Recommendations for standardization: Communication from the SSC on Biorheology of the ISTH. J Thromb Haemost. 2020;18(3):748‐752.
Baaten C, Meacham S, de Witt SM, et al. A synthesis approach of mouse studies to identify genes and proteins in arterial thrombosis and bleeding. Blood. 2018;132(24):e35‐e46.
McCarty OJ, Ku D, Sugimoto M, et al. Dimensional analysis and scaling relevant to flow models of thrombus formation: communication from the SSC of the ISTH. J Thromb Haemost. 2016;14(3):619‐622.
Gijsen FJ, Allanic E, van de Vosse FN, Janssen JD. The influence of the non‐Newtonian properties of blood on the flow in large arteries: unsteady flow in a 90 degrees curved tube. J Biomech. 1999;32(7):705‐713.
De Wilde D, Trachet B, Debusschere N, et al. Assessment of shear stress related parameters in the carotid bifurcation using mouse‐specific FSI simulations. J Biomech. 2016;49(11):2135‐2142.
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.
Weinberg PD, Ethier CR. Twenty‐fold difference in hemodynamic wall shear stress between murine and human aortas. J Biomech. 2007;40(7):1594‐1598.
Greve JM, Les AS, Tang BT, et al. Allometric scaling of wall shear stress from mice to humans: quantification using cine phase‐contrast MRI and computational fluid dynamics. Am J Physiol Heart Circ Physiol. 2006;291(4):H1700‐H1708.
Seymour RS, Hu Q, Snelling EP, White CR. Interspecific scaling of blood flow rates and arterial sizes in mammals. J Exp Biol. 2019;222(7):jeb199554.
Vogel J, Kiessling I, Heinicke K, et al. Transgenic mice overexpressing erythropoietin adapt to excessive erythrocytosis by regulating blood viscosity. Blood. 2003;102(6):2278‐2284.
Doriot PA, Dorsaz PA, Dorsaz L, De Benedetti E, Chatelain P, Delafontaine P. In‐vivo measurements of wall shear stress in human coronary arteries. Coron Artery Dis. 2000;11(6):495‐502.
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(4):H1618‐H1624.
Sashindranath M, Sturgeon SA, French S, et al. The mode of anesthesia influences outcome in mouse models of arterial thrombosis. Res Pract Thromb Haemost. 2019;3(2):197‐206.
Reneman RS, Arts T, Hoeks AP. Wall shear stress–an important determinant of endothelial cell function and structure–in the arterial system in vivo. Discrepancies with theory. J Vasc Res. 2006;43(3):251‐269.
Cheng C, Helderman F, Tempel D, et al. Large variations in absolute wall shear stress levels within one species and between species. Atherosclerosis. 2007;195(2):225‐235.
Barr JD, Chauhan AK, Schaeffer GV, Hansen JK, Motto DG. Red blood cells mediate the onset of thrombosis in the ferric chloride murine model. Blood. 2013;121(18):3733‐3741.
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.
Takumi T, Yang EH, Mathew V, et al. Coronary endothelial dysfunction is associated with a reduction in coronary artery compliance and an increase in wall shear stress. Heart. 2010;96(10):773‐778.
Douglas PS, Fiolkoski J, Berko B, Reichek N. Echocardiographic visualization of coronary artery anatomy in the adult. J Am Coll Cardiol. 1988;11(3):565‐571.
Marcus JT, Smeenk HG, Kuijer JP, Van der Geest RJ, Heethaar RM, Van Rossum AC. Flow profiles in the left anterior descending and the right coronary artery assessed by MR velocity quantification: effects of through‐plane and in‐plane motion of the heart. J Comput Assist Tomogr. 1999;23(4):567‐576.
Wikstrom J, Gronros J, Bergstrom G, Gan LM. Functional and morphologic imaging of coronary atherosclerosis in living mice using high‐resolution color Doppler echocardiography and ultrasound biomicroscopy. J Am Coll Cardiol. 2005;46(4):720‐727.
Feng Y, Wang X, Fan T, et al. Bifurcation asymmetry of small coronary arteries in juvenile and adult mice. Front Physiol. 2018;9:519.
Nonne C, Lenain N, Hechler B, et al. Importance of platelet phospholipase Cgamma2 signaling in arterial thrombosis as a function of lesion severity. Arterioscler Thromb Vasc Biol. 2005;25(6):1293‐1298.
Barral M, El Sanharawi I, Eveno C, et al. Post‐operative wall shear stress in the superior mesenteric artery: biomarker of long term outcome in patients with residual disease after incomplete cytoreductive surgery for pseudomyxoma peritonei. Eur J Surg Oncol. 2019;45(9):1727‐1733.
Chauhan AK, Motto DG, Lamb CB, et al. Systemic antithrombotic effects of ADAMTS13. J Exp Med. 2006;203(3):767‐776.
Ni H, Yuen PS, Papalia JM, et al. Plasma fibronectin promotes thrombus growth and stability in injured arterioles. Proc Natl Acad Sci USA. 2003;100(5):2415‐2419.
Falati S, Gross P, Merrill‐Skoloff G, Furie BC, Furie B. Real‐time in vivo imaging of platelets, tissue factor and fibrin during arterial thrombus formation in the mouse. Nat Med. 2002;8(10):1175‐1181.
Kunkel EJ, Jung U, Ley K. TNF‐alpha induces selectin‐mediated leukocyte rolling in mouse cremaster muscle arterioles. Am J Physiol. 1997;272(3 Pt 2):H1391‐H1400.
Gross PL, Furie BC, Merrill‐Skoloff G, Chou J, Furie B. Leukocyte‐versus microparticle‐mediated tissue factor transfer during arteriolar thrombus development. J Leukoc Biol. 2005;78(6):1318‐1326.
Andrews RK, Gardiner EE. Monitoring the pulse of thrombus formation: Comment on "Modeling thrombosis in silico: Frontiers, challenges, unresolved problems and milestones" by A.V. Belyaev et al. Phys Life Rev. 2018;26–27:113‐115.
Sakariassen KS, Bolhuis PA, Sixma JJ. Platelet adherence to subendothelium of human arteries in pulsatile and steady flow. Thromb Res. 1980;19(4‐5):547‐559.
van Breugel HH, Sixma JJ, Heethaar RM. Effects of flow pulsatility on platelet adhesion to subendothelium. Arteriosclerosis. 1988;8(3):332‐335.
Zhao XM, Wu YP, Cai HX, et al. The influence of the pulsatility of the blood flow on the extent of platelet adhesion. Thromb Res. 2008;121(6):821‐825.
Glagov S, Zarins C, Giddens DP, Ku DN. Hemodynamics and atherosclerosis. Insights and perspectives gained from studies of human arteries. Arch Pathol Lab Med. 1988;112(10):1018‐1031.
Bark DL Jr, Ku DN. Wall shear over high degree stenoses pertinent to atherothrombosis. J Biomech. 2010;43(15):2970‐2977.
Hoeks AP, Reesink KD, Hermeling E, Reneman RS. Local blood pressure rather than shear stress should be blamed for plaque rupture. J Am Coll Cardiol. 2008;52(13):1107‐1108. author reply 8–9.
Nesbitt WS, Westein E, Tovar‐Lopez FJ, et al. A shear gradient‐dependent platelet aggregation mechanism drives thrombus formation. Nat Med. 2009;15(6):665‐673.
Receveur N, Nechipurenko D, Knapp Y, et al. Shear rate gradients promote a bi‐phasic thrombus formation on weak adhesive proteins, such as fibrinogen in a VWF‐dependent manner. Haematologica. 2020;105(10):2471‐2483.
Westein E, van der Meer AD, Kuijpers MJ, Frimat JP, van den Berg A, Heemskerk JW. Atherosclerotic geometries exacerbate pathological thrombus formation poststenosis in a von Willebrand factor‐dependent manner. Proc Natl Acad Sci USA. 2013;110(4):1357‐1362.
Arabi M, Vellody R, Cho K. Acute renal artery occlusion with prolonged renal ischemia: a case of successful treatment with stent placement and catheter‐directed thrombolysis. J Clin Imaging Sci. 2011;1:11.
Zhu S, Chen J, Diamond SL. Establishing the transient mass balance of thrombosis: from tissue factor to thrombin to fibrin under venous flow. Arterioscler Thromb Vasc Biol. 2018;38(7):1528‐1536.
Pasquet M, Aladjidi N, Guiton C, et al. Romiplostim in children with chronic immune thrombocytopenia (ITP): the French experience. Br J Haematol. 2014;164(2):266‐271.
van Bochove GS, Straathof R, Krams R, Nicolay K, Strijkers GJ. MRI‐determined carotid artery flow velocities and wall shear stress in a mouse model of vulnerable and stable atherosclerotic plaque. MAGMA. 2010;23(2):77‐84.

Auteurs

Mikhail A Panteleev (MA)

Center for Theoretical Problems of Physicochemical Pharmacology, Moscow, Russia.
National Medical Research Center of Pediatric Hematology, Oncology and Immunology named after Dmitry Rogachev, Moscow, Russia.

Netanel Korin (N)

Department of Biomedical Engineering Technion, Israel Institute of Technology Haifa, Haifa, Israel.

Koen D Reesink (KD)

Department of Biomedical Engineering, Maastricht University Medical Centre, Maastricht, the Netherlands.

David L Bark (DL)

Department of Mechanical Engineering, Colorado State University, Fort Collins, CO, USA.

Judith M E M Cosemans (JMEM)

Department of Biochemistry, Cardiovascular Research Institute Maastricht (CARIM), Maastricht University, Maastricht, the Netherlands.

Elizabeth E Gardiner (EE)

The John Curtin School of Medical Research, ACRF Department of Cancer Biology and Therapeutics, The Australian National University, Canberra, ACT, Australia.

Pierre H Mangin (PH)

INSERM, EFS Grand-Est, BPPS UMR-S1255, FMTS, Université de Strasbourg, Strasbourg, France.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH