Mechanical circulatory support is associated with loss of platelet receptors glycoprotein Ibα and glycoprotein VI

Journal of Thrombosis and Haemostasis

Volumn 14, Issue 11, 2016, Pages 2253-2260

  Lukito, P ^a   Wong, A ^a   Jing, J ^b   Arthur, J F ^b   Marasco, S F ^a   Murphy, D A ^a   Bergin, P J ^a   Shaw, J A ^a   Collecutt, M ^a   Andrews, R K ^b   Gardiner, E E ^c   Davis, A K ^a  

^a ALFRED HOSPITAL   (Australia)

^b MONASH UNIVERSITY   (Australia)

^c Australian National University   (Australia)

Author keywords

extracorporeal membrane oxygenation; heart assist devices; platelet glycoprotein Ib; platelet glycoprotein VI; von Willebrand disease

Indexed keywords

ACETYLSALICYLIC ACID; DIPYRIDAMOLE; GLYCOPROTEIN IB ALPHA; GLYCOPROTEIN VI; THROMBOCYTE RECEPTOR; VON WILLEBRAND FACTOR; WARFARIN; FIBRINOGEN RECEPTOR; GLYCOCALICIN; HEPARIN; PLATELET MEMBRANE GLYCOPROTEIN VI; THROMBIN RECEPTOR;

ADULT; AGED; AORTA STENOSIS; ARTICLE; BLOOD CLOTTING; CLINICAL ARTICLE; CONGESTIVE CARDIOMYOPATHY; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; EXTRACORPOREAL OXYGENATION; FEMALE; FLOW CYTOMETRY; HEART LEFT VENTRICLE EJECTION FRACTION; HUMAN; IMMUNOASSAY; INFORMED CONSENT; INTERNATIONAL NORMALIZED RATIO; ISCHEMIC CARDIOMYOPATHY; MALE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN DEPLETION; RISK ASSESSMENT; SHEAR STRESS; THROMBOCYTE COUNT; THROMBOCYTE DYSFUNCTION; THROMBOCYTE RICH PLASMA; VON WILLEBRAND DISEASE; ADOLESCENT; AORTIC VALVE STENOSIS; BLEEDING; CHEMISTRY; COHORT ANALYSIS; COMPLICATION; CYTOLOGY; HEART ASSIST DEVICE; HEART FAILURE; MECHANICAL STRESS; METABOLISM; MIDDLE AGED; PATHOPHYSIOLOGY; THROMBOCYTE; THROMBOCYTE ACTIVATION; THROMBOSIS; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; AORTIC VALVE STENOSIS; BLOOD PLATELETS; COHORT STUDIES; EXTRACORPOREAL MEMBRANE OXYGENATION; FEMALE; HEART FAILURE; HEART-ASSIST DEVICES; HEMORRHAGE; HEPARIN; HUMANS; MALE; MIDDLE AGED; PLATELET ACTIVATION; PLATELET GLYCOPROTEIN GPIB-IX COMPLEX; PLATELET MEMBRANE GLYCOPROTEINS; STRESS, MECHANICAL; THROMBOSIS; VON WILLEBRAND FACTOR; WARFARIN; YOUNG ADULT;

EID: 84992445359     PISSN: 15387933     EISSN: 15387836     Source Type: Journal    
DOI: 10.1111/jth.13497     Document Type: Article

References (38)

1. Suarez J, Patel CB, Felker GM, Becker R, Hernandez AF, Rogers JG. Mechanisms of bleeding and approach to patients with axial-flow left ventricular assist devices. Circ Heart Fail 2011; 4: 779–84.
2. Miller LW, Pagani FD, Russell SD, John R, Boyle AJ, Aaronson KD, Conte JV, Naka Y, Mancini D, Delgado RM, MacGillivray TE, Farrar DJ, Frazier OH. Use of a continuous-flow device in patients awaiting heart transplantation. N Engl J Med 2007; 357: 885–96.
3. Slaughter MS, Rogers JG, Milano CA, Russell SD, Conte JV, Feldman D, Sun B, Tatooles AJ, Delgado RM 3rd, Long JW, Wozniak TC, Ghumman W, Farrar DJ, Frazier OH. Advanced heart failure treated with continuous-flow left ventricular assist device. N Engl J Med 2009; 361: 2241–51.
4. Meyer AL, Malehsa D, Bara C, Budde U, Slaughter MS, Haverich A, Strueber M. Acquired von Willebrand syndrome in patients with an axial flow left ventricular assist device. Circ Heart Fail 2010; 3: 675–81.
5. Meyer AL, Malehsa D, Budde U, Bara C, Haverich A, Strueber M. Acquired von Willebrand syndrome in patients with a centrifugal or axial continuous flow left ventricular assist device. JACC Heart Failure 2014; 2: 141–5.
6. Crow S, John R, Boyle A, Shumway S, Liao K, Colvin-Adams M, Toninato C, Missov E, Pritzker M, Martin C, Garry D, Thomas W, Joyce L. Gastrointestinal bleeding rates in recipients of nonpulsatile and pulsatile left ventricular assist devices. J Thorac Cardiovasc Surg 2009; 137: 208–15.
7. Kurien S, Hughes KA. Anticoagulation and bleeding in patients with ventricular assist devices: walking the tightrope. AACN Adv Crit Care 2012; 23: 91–8.
8. Gaffney AM, Wildhirt SM, Griffin MJ, Annich GM, Radomski MW. Extracorporeal life support. BMJ 2010; 341: c5317.
9. Heilmann C, Geisen U, Beyersdorf F, Nakamura L, Benk C, Trummer G, Berchtold-Herz M, Schlensak C, Zieger B. Acquired von Willebrand syndrome in patients with extracorporeal life support (ECLS). Intensive Care Med 2012; 38: 62–8.
10. Murphy DA, Hockings LE, Andrews RK, Aubron C, Gardiner EE, Pellegrino VA, Davis AK. Extracorporeal membrane oxygenation – hemostatic complications. Transf Med Rev. 2015; 29: 90–101.
11. Susen S, Rauch A, van Belle E, Vincentelli A, Lenting PJ. Circulatory support devices: fundamental aspects and clinical management of bleeding and thrombosis. J Thromb Haemost 2015; 13: 1757–67.
12. Nascimbene A, Neelamegham S, Frazier OH, Moake JL, Dong JF. Acquired von Willebrand syndrome associated with left ventricular assist device. Blood 2016; 127: 3133–41.
13. Baldauf C, Schneppenheim R, Stacklies W, Obser T, Pieconka A, Schneppenheim S, Budde U, Zhou J, Grater F. Shear-induced unfolding activates von Willebrand factor A2 domain for proteolysis. J Thromb Haemost 2009; 7: 2096–105.
14. Tsai HM, Sussman II, Nagel RL. Shear stress enhances the proteolysis of von Willebrand factor in normal plasma. Blood 1994; 83: 2171–9.
15. Davis ME, Haglund NA, Tricarico NM, Matafonov A, Gailani D, Maltais S. Immediate recovery of acquired von Willebrand syndrome after left ventricular assist device explantation: implications for heart transplantation. ASAIO J 2015; 61: e1–4.
16. Klovaite J, Gustafsson F, Mortensen SA, Sander K, Nielsen LB. Severely impaired von Willebrand factor-dependent platelet aggregation in patients with a continuous-flow left ventricular assist device (HeartMate II). J Am Coll Cardiol 2009; 53: 2162–7.
17. Steinlechner B, Dworschak M, Birkenberg B, Duris M, Zeidler P, Fischer H, Milosevic L, Wieselthaler G, Wolner E, Quehenberger P, Jilma B. Platelet dysfunction in outpatients with left ventricular assist devices. Ann Thorac Surg 2009; 87: 131–7.
18. Massberg S, Gawaz M, Gruner S, Schulte V, Konrad I, Zohlnhofer D, Heinzmann U, Nieswandt B. A crucial role of glycoprotein VI for platelet recruitment to the injured arterial wall in vivo. J Exp Med 2003; 197: 41–9.
19. Bergmeier W, Piffath CL, Goerge T, Cifuni SM, Ruggeri ZM, Ware J, Wagner DD. The role of platelet adhesion receptor GPIbα far exceeds that of its main ligand, von Willebrand factor, in arterial thrombosis. Proc Natl Acad Sci USA 2006; 103: 16900–5.
20. Al-Tamimi M, Tan C, Qiao J, Pennings GJ, Javadzadegan A, Yong ASC, Arthur JF, Davis AK, Jing J, Mu FT, Hamilton JR, Jackson SP, Ludwig A, Berndt MC, Ward CM, Kritharides L, Andrews RK, Gardiner EE. Pathological shear triggers shedding of vascular receptors: a novel mechanism for downregulation of platelet glycoprotein (GP)VI in stenosed coronary vessels. Blood 2012; 119: 4311–20.
21. Chen Z, Mondal NK, Ding J, Koenig SC, Slaughter MS, Wu ZJ. Paradoxical effect of nonphysiological shear stress on platelets and von Willebrand factor. Artif Organs 2016; 40: 659–68.
22. Al-Tamimi M, Mu FT, Moroi M, Gardiner EE, Berndt MC, Andrews RK. Measuring soluble platelet glycoprotein VI in human plasma by ELISA. Platelets 2009; 20: 143–9.
23. Qiao J, Schoenwaelder SM, Mason KD, Tran H, Davis AK, Kaplan ZS, Jackson SP, Kile BT, Andrews RK, Roberts AW, Gardiner EE. Low adhesion receptor levels on circulating platelets in patients with lymphoproliferative diseases prior to receiving Navitoclax (ABT-263). Blood 2013; 121: 1479–81.
24. Trevillyan JM, Arthur JF, Jing J, Andrews RK, Gardiner EE, Hoy JF. Effects of abacavir administration on structural and functional markers of platelet activation. AIDS 2015; 29: 2309–13.
25. Uriel N, Pak SW, Jorde UP, Jude B, Susen S, Vincentelli A, Ennezat PV, Cappleman S, Naka Y, Mancini D. Acquired von Willebrand syndrome after continuous-flow mechanical device support contributes to a high prevalence of bleeding during long-term support and at the time of transplantation. J Am Coll Cardiol 2010; 56: 1207–13.
26. Genovese EA, Dew MA, Teuteberg JJ, Simon MA, Kay J, Siegenthaler MP, Bhama JK, Bermudez CA, Lockard KL, Winowich S, Kormos RL. Incidence and patterns of adverse event onset during the first 60 days after ventricular assist device implantation. Ann Thorac Surg 2009; 88: 1162–70.
27. Vincentelli A, Susen S, Le Tourneau T, Six I, Fabre O, Juthier F, Bauters A, Decoene C, Goudemand J, Prat A, Jude B. Acquired von Willebrand syndrome in aortic stenosis. N Engl J Med 2003; 349: 343–9.
28. Muthiah K, Connor D, Ly K, Gardiner EE, Andrews RK, Qiao J, Rutgers D, Robson D, Low J, Jarvis S, Macdonald P, Dhital K, Jansz P, Joseph J, Hayward C. Longitudinal changes in haemostatic parameters and reduced pulsatility contribute to non-surgical bleeding in patients with centrifugal continuous flow left ventricular assist devices. J Heart Lung Transpl 2016; 35: 743–51.
29. Hu J, Mondal NK, Sorensen EN, Cai L, Fang HB, Griffith BP, Wu ZJ. Platelet glycoprotein Ibα ectodomain shedding and non-surgical bleeding in heart failure patients supported by continuous-flow left ventricular assist devices. J Heart Lung Transpl 2014; 33: 71–9.
30. Chen Z, Mondal NK, Ding J, Gao J, Griffith BP, Wu ZJ. Shear-induced platelet receptor shedding by non-physiological high shear stress with short exposure time: glycoprotein Ibα and glycoprotein VI. Thromb Res 2015; 135: 692–8.
31. Gardiner EE, Andrews RK. Platelet receptor expression and shedding: glycoprotein Ib-IX-V and glycoprotein VI. Transf Med Rev 2014; 28: 56–60.
32. Al-Tamimi M, Grigoriadis G, Tran H, Paul E, Servadei P, Berndt MC, Gardiner EE, Andrews RK. Coagulation-induced shedding of platelet glycoprotein VI mediated by factor Xa. Blood 2011; 117: 3912–20.
33. Al-Tamimi M, Gardiner EE, Thom JY, Shen Y, Cooper MN, Hankey GJ, Berndt MC, Baker RI, Andrews RK. Soluble glycoprotein VI is raised in the plasma of patients with acute ischemic stroke. Stroke 2011; 42: 498–500.
34. Wurster T, Poetz O, Stellos K, Kremmer E, Melms A, Schuster A, Nagel E, Joos T, Gawaz M, Bigalke B. Plasma levels of soluble glycoprotein VI (sGPVI) are associated with ischemic stroke. Platelets 2013; 24: 560–5.
35. Gardiner EE, Al-Tamimi M, Mu FT, Karunakaran D, Thom JY, Moroi M, Andrews RK, Berndt MC, Baker RI. Compromised ITAM-based platelet receptor function in a patient with immune thrombocytopenic purpura. J Thromb Haemost 2008; 6: 1175–82.
36. Yamashita Y, Naitoh K, Wada H, Ikejiri M, Mastumoto T, Ohishi K, Hosaka Y, Nishikawa M, Katayama N. Elevated plasma levels of soluble platelet glycoprotein VI (GPVI) in patients with thrombotic microangiopathy. Thromb Res 2014; 133: 440–4.
37. Mondal NK, Sorensen EN, Feller ED, Pham SM, Griffith BP, Wu ZJ. Comparison of intraplatelet reactive oxygen species, mitochondrial damage, and platelet apoptosis after implantation of three continuous flow left ventricular assist devices: HeartMate II, Jarvik 2000, and HeartWare. ASAIO J 2015; 61: 244–52.
38. Grosman-Rimon L, McDonald MA, Jacobs I, Tumiati LC, Pollock Bar-Ziv S, Shogilev DJ, Mociornita AG, Ghashghai A, Chruscinski A, Cherney DZI, Rao V. Markers of inflammation in recipients of continuous-flow left ventricular assist devices. ASAIO J 2014; 60: 657–63.