Hemodynamic Performance and Thrombogenic Properties of a Superhydrophobic Bileaflet Mechanical Heart Valve

In this study, we explore how blood-material interactions and hemodynamics are impacted by rendering a clinical quality 25 mm St. Jude Medical Bileaflet mechanical heart valve (BMHV) superhydrophobic (SH) with the aim of reducing thrombo-embolic complications associated with BMHVs. Basic cell adhesion is evaluated to assess blood-material interactions, while hemodynamic performance is analyzed with and without the SH coating. Results show that a SH coating with a receding contact angle (CA) of 160° strikingly eliminates platelet and leukocyte adhesion to the surface. Alternatively, many platelets attach to and activate on pyrolytic carbon (receding CA = 47), the base material for BMHVs. We further show that the performance index increases by 2.5% for coated valve relative to an uncoated valve, with a maximum possible improved performance of 5%. Both valves exhibit instantaneous shear stress below 10 N/m2 and Reynolds Shear Stress below 100 N/m2. Therefore, a SH BMHV has the potential to relax the requirement for antiplatelet and anticoagulant drug regimens typically required for patients receiving MHVs by minimizing blood-material interactions, while having a minimal impact on hemodynamics. We show for the first time that SH-coated surfaces may be a promising direction to minimize thrombotic complications in complex devices such as heart valves.

[1]  R. Sade,et al.  Cardiac valve replacement in children: comparison of tissue with mechanical prostheses. , 1979, The Journal of thoracic and cardiovascular surgery.

[2]  W S Pierce,et al.  A polyurethane trileaflet cardiac valve prosthesis: in vitro and in vivo studies. , 1982, Transactions - American Society for Artificial Internal Organs.

[3]  Khandakar Niaz Morshed,et al.  Theory to Predict Shear Stress on Cells in Turbulent Blood Flow , 2014, PloS one.

[4]  F. R. Rosendaal,et al.  Thromboembolic and Bleeding Complications in Patients With Mechanical Heart Valve Prostheses , 1994, Circulation.

[5]  Joseph D. Andrade,et al.  Blood compatibility of polyethylene oxide surfaces , 1995 .

[6]  C. Yakut,et al.  Biocompatibility of Heparin‐Coated Cardiopulmonary Bypass Circuits in Coronary Patients With Left Ventricular Dysfunction Is Superior to PMEA‐Coated Circuits , 2006, Journal of cardiac surgery.

[7]  J D Hellums,et al.  Aggregation and disaggregation kinetics of human blood platelets: Part II. Shear-induced platelet aggregation. , 1993, Biophysical journal.

[8]  N H Hwang,et al.  Human red blood cell hemolysis in a turbulent shear flow: contribution of Reynolds shear stresses. , 1984, Biorheology.

[9]  A. Tuteja,et al.  High-efficiency, ultrafast separation of emulsified oil–water mixtures , 2013 .

[10]  M. Yacoub,et al.  Surgical Treatment of Mitral Regurgitation Caused by Floppy Valves: Repair Versus Replacement , 1981, Circulation.

[11]  Hélène A. Simon,et al.  Vorticity dynamics of a bileaflet mechanical heart valve in an axisymmetric aorta , 2007 .

[12]  Melissa M. Reynolds,et al.  Anti-thrombogenic properties of a nitric oxide-releasing dextran derivative: evaluation of platelet activation and whole blood clotting kinetics. , 2013, RSC advances.

[13]  Andre Lamy,et al.  Antithrombotic management of patients with prosthetic heart valves: current evidence and future trends , 2009, The Lancet.

[14]  Chih-Ming Ho,et al.  Effective slip and friction reduction in nanograted superhydrophobic microchannels , 2006 .

[15]  Sean M. O'Brien,et al.  Isolated aortic valve replacement in North America comprising 108,687 patients in 10 years: changes in risks, valve types, and outcomes in the Society of Thoracic Surgeons National Database. , 2009, The Journal of thoracic and cardiovascular surgery.

[16]  J. Hirsh,et al.  Medical device‐induced thrombosis: what causes it and how can we prevent it? , 2015, Journal of thrombosis and haemostasis : JTH.

[17]  J.,et al.  Whitaker Lecture : Biorheology in Thrombosis Research , 2022 .

[18]  J. D. Hellums,et al.  1993 Whitaker lecture: Biorheology in thrombosis research , 1994, Annals of Biomedical Engineering.

[19]  D. Adams,et al.  Survival and long-term outcomes following bioprosthetic vs mechanical aortic valve replacement in patients aged 50 to 69 years. , 2014, JAMA.

[20]  Danny Bluestein,et al.  Fluid mechanics of arterial stenosis: Relationship to the development of mural thrombus , 1997, Annals of Biomedical Engineering.

[21]  D. Ku,et al.  Wall shear over high degree stenoses pertinent to atherothrombosis. , 2010, Journal of biomechanics.

[22]  S. S. Kim,et al.  Long-term results with St. Jude Medical and CarboMedics prosthetic heart valves. , 2001, The Journal of heart valve disease.

[23]  J. Rothstein Slip on Superhydrophobic Surfaces , 2010 .

[24]  B. Ho-Tin-Noé,et al.  Collagen Can Selectively Trigger a Platelet Secretory Phenotype via Glycoprotein VI , 2014, PloS one.

[25]  J. Reiber,et al.  Heparin-coated Wiktor stents in human coronary arteries (MENTOR trial). MENTOR Trial Investigators. , 2000, The American journal of cardiology.

[26]  D. Grainger,et al.  Adsorbed serum albumin is permissive to macrophage attachment to perfluorocarbon polymer surfaces in culture. , 2009, Journal of biomedical materials research. Part A.

[27]  N. Quinlan,et al.  Effect of Eddy Length Scale on Mechanical Loading of Blood Cells in Turbulent Flow , 2009, Annals of Biomedical Engineering.

[28]  Gerring El,et al.  Long term animal trials of the Oxford aortic/pulmonary valve prosthesis without anticoagulants. , 1974 .

[29]  M. Khorasani,et al.  In vitro blood compatibility of modified PDMS surfaces as superhydrophobic and superhydrophilic materials , 2004 .

[30]  Yasukiyo Ueda,et al.  The Lowest Surface Free Energy Based on −CF3 Alignment , 1999 .

[31]  F. Van de Werf,et al.  Experimental study of thrombogenicity and foreign body reaction induced by heparin-coated coronary stents. , 1997, Circulation.

[32]  E. Baudet,et al.  A 5 1/2 year experience with the St. Jude Medical cardiac valve prosthesis. Early and late results of 737 valve replacements in 671 patients. , 1985, The Journal of thoracic and cardiovascular surgery.

[33]  Marcio Forleo,et al.  Hemocompatibility and Hemodynamics of Novel Hyaluronan–Polyethylene Materials for Flexible Heart Valve Leaflets , 2014, Cardiovascular engineering and technology.

[34]  E. Chaikof,et al.  The effect of a recombinant elastin-mimetic coating of an ePTFE prosthesis on acute thrombogenicity in a baboon arteriovenous shunt. , 2007, Biomaterials.

[35]  A. Tuteja,et al.  Superomniphobic surfaces: Design and durability , 2013 .

[36]  T. Horbett,et al.  Proteins at Interfaces: An Overview , 1995 .

[37]  L Niu,et al.  Steady flow in an aneurysm model: correlation between fluid dynamics and blood platelet deposition. , 1996, Journal of biomechanical engineering.

[38]  Fotis Sotiropoulos,et al.  Fluid Mechanics of Heart Valves and Their Replacements , 2016 .

[39]  Blair Perot,et al.  Laminar drag reduction in microchannels using ultrahydrophobic surfaces , 2004 .

[40]  Andreas Franke,et al.  New flexible polymeric heart valve prostheses for the mitral and aortic positions. , 2004, The heart surgery forum.

[41]  Mark D. Huffman,et al.  AHA Statistical Update Heart Disease and Stroke Statistics — 2012 Update A Report From the American Heart Association WRITING GROUP MEMBERS , 2010 .

[42]  Alberto Redaelli,et al.  Platelet Activation Due to Hemodynamic Shear Stresses: Damage Accumulation Model and Comparison to In Vitro Measurements , 2008, ASAIO journal.

[43]  J Fisher,et al.  Hydrodynamic Function of a Biostable Polyurethane Flexible Heart Valve after Six Months in Sheep , 2001, The International journal of artificial organs.

[44]  Benjamin G. Keselowsky,et al.  Adsorption-Induced Conformational Changes in Fibronectin Due to Interactions with Well-Defined Surface Chemistries , 2003 .

[45]  F Clerc,et al.  Long-term results of valve replacement with the St. Jude Medical prosthesis. , 1995, The Journal of thoracic and cardiovascular surgery.

[46]  J D Hellums,et al.  Shear-induced platelet aggregation can be mediated by vWF released from platelets, as well as by exogenous large or unusually large vWF multimers, requires adenosine diphosphate, and is resistant to aspirin. , 1988, Blood.

[47]  A. Tuteja,et al.  Superoleophobic surfaces: design criteria and recent studies , 2013 .

[48]  Ajit P Yoganathan,et al.  Flow and thrombosis at orifices simulating mechanical heart valve leakage regions. , 2006, Journal of biomechanical engineering.

[49]  Ajit P Yoganathan,et al.  Fluid mechanics of heart valves. , 2004, Annual review of biomedical engineering.

[50]  Daniel C Leslie,et al.  A bioinspired omniphobic surface coating on medical devices prevents thrombosis and biofouling , 2014, Nature Biotechnology.

[51]  A. Yoganathan,et al.  Passive flow control of bileaflet mechanical heart valve leakage flow. , 2008, Journal of biomechanics.

[52]  M. Davies Pathology of ischaemic heart disease , 1987 .

[53]  M. Sarsam,et al.  The St. Jude Medical prosthesis. A thirteen-year experience. , 1994, The Journal of thoracic and cardiovascular surgery.

[54]  David Quéré,et al.  Non-sticking drops , 2005 .

[55]  P. Lu,et al.  A reevaluation and discussion on the threshold limit for hemolysis in a turbulent shear flow. , 2001, Journal of biomechanics.

[56]  L. Cohn,et al.  Mechanical versus bioprosthetic mitral valve replacement in patients <65 years old. , 2014, The Journal of thoracic and cardiovascular surgery.

[57]  H. Reul,et al.  Estimation of Shear Stress-related Blood Damage in Heart Valve Prostheses - in Vitro Comparison of 25 Aortic Valves , 1990, The International journal of artificial organs.

[58]  Marcio Forleo,et al.  Effect of Hypertension on the Closing Dynamics and Lagrangian Blood Damage Index Measure of the B-Datum Regurgitant Jet in a Bileaflet Mechanical Heart Valve , 2013, Annals of Biomedical Engineering.

[59]  Siddarth Srinivasan,et al.  Drag reduction for viscous laminar flow on spray-coated non-wetting surfaces , 2013 .

[60]  Richard A. Lange,et al.  Prosthetic heart valves. , 1996, The New England journal of medicine.

[61]  Larry V McIntire,et al.  Platelet Aggregation and Activation under Complex Patterns of Shear Stress , 2002, Thrombosis and Haemostasis.

[62]  R. Chow,et al.  On the ability of drops or bubbles to stick to non-horizontal surfaces of solids , 1983, Journal of Fluid Mechanics.

[63]  Iraj Mortazavi,et al.  Numerical modelling and passive flow control using porous media , 2008 .

[64]  C. Vosa,et al.  Aortic valve replacement: a prospective randomized evaluation of mechanical versus biological valves in patients ages 55 to 70 years. , 2009, Journal of the American College of Cardiology.

[65]  J. Blair Perot,et al.  Direct numerical simulations of turbulent flows over superhydrophobic surfaces , 2008, Journal of Fluid Mechanics.

[66]  D. Ku,et al.  Correlation of thrombosis growth rate to pathological wall shear rate during platelet accumulation , 2012, Biotechnology and bioengineering.

[67]  A. Cassie,et al.  Wettability of porous surfaces , 1944 .

[68]  J. Rothstein,et al.  Direct velocity measurements of the flow past drag-reducing ultrahydrophobic surfaces , 2005 .

[69]  A. Leitão,et al.  Hemocompatibility study of a bacterial cellulose/polyvinyl alcohol nanocomposite. , 2013, Colloids and surfaces. B, Biointerfaces.

[70]  K. Popat,et al.  Hemocompatibility of titania nanotube arrays. , 2010, Journal of biomedical materials research. Part A.

[71]  V. Falk,et al.  Retrospective analysis of outcome data with regards to the use of Phisio®-, Bioline®- or Softline®-coated cardiopulmonary bypass circuits in cardiac surgery , 2012, Perfusion.

[72]  B J Bellhouse,et al.  Long term animal trials of the Oxford aortic/pulmonary valve prosthesis without anticoagulants. , 1974, Transactions - American Society for Artificial Internal Organs.

[73]  Thomas Young,et al.  An Essay on the Cohesion of Fluids , 1800 .

[74]  N. Quinlan,et al.  High-Resolution Measurement of the Unsteady Velocity Field to Evaluate Blood Damage Induced by a Mechanical Heart Valve , 2011, Annals of Biomedical Engineering.

[75]  R. N. Wenzel RESISTANCE OF SOLID SURFACES TO WETTING BY WATER , 1936 .

[76]  J. H. Lee,et al.  Immobilization of proteins on poly(methyl methacrylate) films. , 1993, Biomaterials.

[77]  P. Constantinides,et al.  Plaque fissures in human coronary thrombosis , 1966 .

[78]  Jonathan P. Rothstein,et al.  Drag reduction in turbulent flows over superhydrophobic surfaces , 2009 .

[79]  Chang-Jin C J Kim,et al.  Maximizing the giant liquid slip on superhydrophobic microstructures by nanostructuring their sidewalls. , 2009, Langmuir : the ACS journal of surfaces and colloids.

[80]  D. Ku,et al.  Platelet transport rates and binding kinetics at high shear over a thrombus. , 2013, Biophysical journal.

[81]  Fotis Sotiropoulos,et al.  Characterization of Hemodynamic Forces Induced by Mechanical Heart Valves: Reynolds vs. Viscous Stresses , 2008, Annals of Biomedical Engineering.

[82]  David Farrar,et al.  Interpretation of protein adsorption: surface-induced conformational changes. , 2005, Journal of the American Chemical Society.

[83]  W Rutsch,et al.  Heparin-coated Palmaz-Schatz stents in human coronary arteries. Early outcome of the Benestent-II Pilot Study. , 1996, Circulation.

[84]  J. Marchal,et al.  Caractérisation de réactions primaires de dégradation oxydante au cours de l'autoxydation des poly(oxyéthylène)s à 25°C: Étude en solution aqueuse avec amorçage par radiolyse du solvant, 8. Étude cinétique en fonction du ph compris entre 1 et 13† , 1976 .

[85]  D. Mozaffarian,et al.  Executive Summary: Heart Disease and Stroke Statistics—2015 Update A Report From the American Heart Association , 2011, Circulation.

[86]  G. Shepherd,et al.  Adverse Drug Reaction Deaths Reported in United States Vital Statistics, 1999-2006 , 2012, The Annals of pharmacotherapy.

[87]  Sean M. O'Brien,et al.  Trends in mitral valve surgery in the United States: results from the Society of Thoracic Surgeons Adult Cardiac Surgery Database. , 2009, The Annals of thoracic surgery.

[88]  A. Seifalian,et al.  Is there an alternative to systemic anticoagulation, as related to interventional biomedical devices? , 2006, Expert review of medical devices.

[89]  J. Lin,et al.  Turbulent flow separation control through passive techniques , 1989 .

[90]  Qiang Fu,et al.  No platelet can adhere--largely improved blood compatibility on nanostructured superhydrophobic surfaces. , 2005, Small.