The endothelial glycocalyx and fluid therapy in critical care and perioperative medicine
Authors:
D. Astapenko 1,2; J. Pouska 3,4; V. Černý 1,2,5,8; J. Beneš 3,4,9
Authors‘ workplace:
Klinika anesteziologie, resuscitace a intenzivní medicíny, Fakultní nemocnice Hradec Králové
1; Lékařská fakulta v Hradci Králové, Univerzita Karlova
2; Klinika anesteziologie, resuscitace a intenzivní medicíny, Fakultní nemocnice Plzeň
3; Klinika anesteziologie, resuscitace a intenzivní medicíny, Lékařská fakulta v Plzni, Univerzita Karlova
4; Klinika anesteziologie, perioperační a intenzivní medicíny, Masarykova nemocnice Ústí nad Labem, Univerzita J. E. Purkyně v Ústí nad Labem
5; Institut postgraduálního vzdělávání ve zdravotnictví
6; Centrum pro výzkum a vývoj, Fakultní nemocnice Hradec Králové
7; Dept. of Anesthesia, Pain Management and Perioperative Medicine, Dalhousie University, Halifax, Kanada
8; Biomedicínské centrum, Lékařská fakulta v Plzni, Univerzita Karlova
9
Published in:
Anest. intenziv. Med., 28, 2017, č. 5, s. 289-296
Category:
Intensive Care Medicine - Review Article
Overview
The endothelial glycocalyx represents a key component of the endothelial barrier on its intraluminal side. It is vital for the maintenance of vascular integrity in physiological conditions and most probably also in pathophysiological conditions. Due to its sugar-based structure, it is highly vulnerable and in the context of critical conditions of patients, the development of endothelial dysfunction is always linked to a certain degree of damage of the glycocalyx. The current state of knowledge favours determining a presumption of a relationship between the function of the glycocalyx and volume replacement therapy. Attempts to minimize damage (and to allow spontaneous recovery) are the only available rational concepts of maintaining integrity of the endothelium and reaching the maximal effect of infusion therapy. This narrative review article brings a summary of this topic and discusses arguments for consideration of the significance of the glycocalyx in the decision-making in fluid therapy.
Keywords:
endothelial glycocalyx – fluid therapy – microcirculation
Sources
1. Oberleithner H. Vascular endothelium leaves fingerprints on the surface of erythrocytes. Pflügers Arch – Eur J Physiol. 2013;465:1451–1458.
2. Tarbell JM, Pahakis MY. Mechanotransduction and the glycocalyx. J Intern Med. 2006;259:339–350.
3. Reitsma S, Slaaf DW, Vink H, van Zandvoort MAMJ, oude Egbrink MGA. The endothelial glycocalyx: composition, functions, and visualization. Pflugers Arch. 2007;454:345–359.
4. Megens RTA, Reitsma S, Schiffers PHM, Hilgers RHP, De Mey JGR, Slaaf DW, et al. Two-photon microscopy of vital murine elastic and muscular arteries. Combined structural and functional imaging with subcellular resolution. J Vasc Res. 2007;44:87–98.
5. Huxley VH, Curry FE. Differential actions of albumin and plasma on capillary solute permeability. Am J Physiol. 1991;260(5 Pt 2):H1645–654.
6. Nijst P, Verbrugge FH, Grieten L, Dupont M, Steels P, Tang WHW, et al. The pathophysiological role of interstitial sodium in heart failure. J Am Coll Cardiol. 2015;65:378–388.
7. Korte S, Wiesinger A, Straeter AS, Peters W, Oberleithner H, Kusche-Vihrog K. Firewall function of the endothelial glycocalyx in the regulation of sodium homeostasis. Pflügers Arch Eur J Physiol. 2012;463:269–278.
8. Salmon AHJ, Satchell SC. Endothelial glycocalyx dysfunction in disease: albuminuria and increased microvascular permeability. J Pathol. 2012;226:562–574.
9. Rabelink TJ, de Zeeuw D. The glycocalyx – linking albuminuria with renal and cardiovascular disease. Nat Rev Nephrol. 2015;11:667–676.
10. Xiao H, Woods EC, Vukojicic P, Bertozzi CR. Precision glycocalyx editing as a strategy for cancer immunotherapy. Proc Natl Acad Sci. 2016;113:10304–10309.
11. Levick JR. Fluid exchange across endothelium. Int J Microcirc Clin Exp. 1997;17:241–247.
12. Gonzalez E, Moore EE, Moore HB, Theresa C, Chapman M, Ghasabyan A, et al. Syndecan-1 a Marker of Endothelial Injury is Associated with Increased Blood Product Requirement and Poor Outcomes in Trauma Patients. J Surg Res. Elsevier. 2014;186:588–589.
13. Pries AR, Secomb TW. Microvascular blood viscosity in vivo and the endothelial surface layer. Am J Physiol Heart Circ Physiol. 2005;289:H2657–2664.
14. Constantinescu AA, Vink H, Spaan JAE. Endothelial cell glycocalyx modulates immobilization of leukocytes at the endothelial surface. Arterioscler Thromb Vasc Biol. 2003;23:1541–1547.
15. Mochizuki S, Vink H, Hiramatsu O, Kajita T, Shigeto F, Spaan JAE, et al. Role of hyaluronic acid glycosaminoglycans in shear-induced endothelium-derived nitric oxide release. Am J Physiol Heart Circ Physiol. 2003;285:H722–726.
16. Gouverneur M, Spaan JAE, 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:H458–462.
17. Pradhan RK, Chakravarthy VS. Informational dynamics of vasomotion in microvascular networks: a review. Acta Physiol (Oxf). 2011;201(2):193–218.
18. Oberleithner H, Riethmüller C, Schillers H, MacGregor GA, de Wardener HE, Hausberg M. Plasma sodium stiffens vascular endothelium and reduces nitric oxide release. Proc Natl Acad Sci U S A. 2007;104:16281–16286.
19. Seal JB, Gewertz BL. Vascular dysfunction in ischemia-reperfusion injury. Ann Vasc Surg. 2005;19:572–584.
20. Oliver MG, Specian RD, Perry MA, Granger DN. Morphologic assessment of leukocyte-endothelial cell interactions in mesenteric venules subjected to ischemia and reperfusion. Inflammation. 1991;15:331–346.
21. Rubio-Gayosso I. Reactive oxygen species mediate modification of glycocalyx during ischemia-reperfusion injury. AJP Hear Circ Physiol. 2006;290:H2247–2256.
22. Vollmar B, Glasz J, Menger MD, Messmer K. Leukocytes contribute to hepatic ischemia/reperfusion injury via intercellular adhesion molecule-1-mediated venular adherence. Surgery. 1995;117:195–200.
23. Kupinski AM, Shah DM, Bell DR. Transvascular albumin flux in rabbit hindlimb after tourniquet ischemia. Am J Physiol. 1993;264(3 Pt 2):H901–908.
24. Burke-Gaffney A, Evans TW. Lest we forget the endothelial glycocalyx in sepsis. Crit Care. 2012;16:121.
25. Goodall KJ, Poon IKH, Phipps S, Hulett MD. Soluble heparan sulfate fragments generated by heparanase trigger the release of pro-inflammatory cytokines through TLR-4. Srinivasula SM, editor. PLoS One. 2014;9:e109596.
26. Nelson A, Berkestedt I, Schmidtchen A, Ljunggren L, Bodelsson M. Increased levels of glycosaminoglycans during septic shock: relation to mortality and the antibacterial actions of plasma. Shock. 2008;30:623–627.
27. Johansson PI, Stensballe J, Rasmussen LS, Ostrowski SR. A high admission syndecan-1 level, a marker of endothelial glycocalyx degradation, is associated with inflammation, protein C depletion, fibrinolysis, and increased mortality in trauma patients. Ann Surg. 2011;254:194–200.
28. Bruegger D, Schwartz L, Chappell D, Jacob M, Rehm M, Vogeser M, et al. Release of atrial natriuretic peptide precedes shedding of the endothelial glycocalyx equally in patients undergoing on- and off-pump coronary artery bypass surgery. Basic Res Cardiol. 2011;106:1111–1121.
29. Chappell D, Bruegger D, Potzel J, Jacob M, Brettner F, Vogeser M, et al. Hypervolemia increases release of atrial natriuretic peptide and shedding of the endothelial glycocalyx. Crit Care. 2014;18:538.
30. Powell M, Mathru M, Brandon A, Patel R, Frölich M. Assessment of endothelial glycocalyx disruption in term parturients receiving a fluid bolus before spinal anesthesia: a prospective observational study. Int J Obstet Anesth. 2014;23:330–334.
31. Rehm M, Zahler S, Lötsch M, Welsch U, Conzen P, Jacob M, et al. Endothelial glycocalyx as an additional barrier determining extravasation of 6% hydroxyethyl starch or 5% albumin solutions in the coronary vascular bed. Anesthesiology. 2004;100:1211–1223.
32. Starling EH. On the Absorption of Fluids from the Connective Tissue Spaces. J Physiol. 1896;19:312–326.
33. Woodcock TE, Woodcock TM. Revised Starling equation and the glycocalyx model of transvascular fluid exchange: an improved paradigm for prescribing intravenous fluid therapy. Br J Anaesth. 2012;108:384–394.
34. James MFM, Michell WL, Joubert IA, Nicol AJ, Navsaria PH, Gillespie RS. Resuscitation with hydroxyethyl starch improves renal function and lactate clearance in penetrating trauma in a randomized controlled study: the FIRST trial (Fluids in Resuscitation of Severe Trauma). Br J Anaesth. Oxford University Press; 2011;107:693–702.
35. Guidet B, Martinet O, Boulain T, Philippart F, Poussel JF, Maizel J, et al. Assessment of hemodynamic efficacy and safety of 6% hydroxyethylstarch 130/0.4 vs. 0.9% NaCl fluid replacement in patients with severe sepsis: the CRYSTMAS study. Crit Care. 2012;16:R94.
36. Bruegger D, Jacob M, Rehm M, Loetsch M, Welsch U, Conzen P, et al. Atrial natriuretic peptide induces shedding of endothelial glycocalyx in coronary vascular bed of guinea pig hearts. Am J Physiol Heart Circ Physiol. 2005;289:H1993–1999.
37. Hooijmans CR, Rovers MM, de Vries RB, Leenaars M, Ritskes-Hoitinga M, Langendam MW. SYRCLE’s risk of bias tool for animal studies. BMC Med Res Methodol. 2014;14:43.
38. Naumann DN, Beaven A, Dretzke J, Hutchings S, Midwinter MJ. Searching For the Optimal Fluid to Restore Microcirculatory Flow Dynamics After Haemorrhagic Shock. SHOCK. 2016;46:609–622.
39. Pati S, Matijevic N, Doursout M-F, Ko T, Cao Y, Deng X, et al. Protective effects of fresh frozen plasma on vascular endothelial permeability, coagulation, and resuscitation after hemorrhagic shock are time dependent and diminish between days 0 and 5 after thaw. J Trauma. 2010;69 Suppl 1(Supplement):S55–63.
40. Kozar RA, Peng Z, Zhang R, Holcomb JB, Pati S, Park P, et al. Plasma restoration of endothelial glycocalyx in a rodent model of hemorrhagic shock. Anesth Analg. 2011; 112:1289–1295.
41. Peng Z, Pati S, Potter D, Brown R, Holcomb JB, Grill R, et al. Fresh Frozen Plasma Lessens Pulmonary Endothelial Inflammation and Hyperpermeability After Hemorrhagic Shock and Is Associated With Loss of Syndecan 1. Shock. 2013;40:195–202.
42. Baimukanova G, Miyazawa B, Potter DR, Muench MO, Bruhn R, Gibb SL, et al. Platelets regulate vascular endothelial stability: assessing the storage lesion and donor variability of apheresis platelets. Transfusion. 2016;56:S65–75.
43. Torres Filho IP, Torres LN, Salgado C, Dubick MA. Plasma syndecan-1 and heparan sulfate correlate with microvascular glycocalyx degradation in hemorrhaged rats after different resuscitation fluids. Am J Physiol Heart Circ Physiol. 2016;310:H1468–478.
44. Brettner F, von Dossow V, Chappell D. The endothelial glycocalyx and perioperative lung injury. Curr Opin Anaesthesiol. 2016;30:1.
45. Nussbaum C, Haberer A, Tiefenthaller A, Januszewska K, Chappell D, Brettner F, et al. Perturbation of the microvascular glycocalyx and perfusion in infants after cardiopulmonary bypass. J Thorac Cardiovasc Surg. 2015;150:1474–1481.
46. Puskarich MA, Cornelius DC, Tharp J, Nandi U, Jones AE. Plasma syndecan-1 levels identify a cohort of patients with severe sepsis at high risk for intubation after large-volume intravenous fluid resuscitation. J Crit Care. 2016;36:125–129.
47. Straat M, Müller MCA, Meijers JCM, Arbous MS, Spoelstra-de Man AME, Beurskens CJP, et al. Effect of transfusion of fresh frozen plasma on parameters of endothelial condition and inflammatory status in non-bleeding critically ill patients: a prospective substudy of a randomized trial. Crit Care. 2015;19:163.
48. Kim TK, Nam K, Cho YJ, Min JJ, Hong YJ, Park KU, et al. Microvascular reactivity and endothelial glycocalyx degradation when administering hydroxyethyl starch or crystalloid during off-pump coronary artery bypass graft surgery: a randomised trial. Anaesthesia. 2017;72:204–213.
49. Hoste EA, Maitland K, Brudney CS, Mehta R, Vincent J-L, Yates D, et al. Four phases of intravenous fluid therapy: a conceptual model. Br J Anaesth. 2014;113:740–747.
50. Moore JPR, Dyson A, Singer M, Fraser J. Microcirculatory dysfunction and resuscitation: why, when, and how. Hardman JG, editor. Br J Anaesth. 2015;115:366–375.
51. Tatara T. Context-sensitive fluid therapy in critical illness. J intensive care. 2016;4:20.
Labels
Anaesthesiology, Resuscitation and Inten Intensive Care MedicineArticle was published in
Anaesthesiology and Intensive Care Medicine
2017 Issue 5
Most read in this issue
- Succesful use of methylene blue in a patient with refractory shock on veno-arterial extracorporeal membrane oxygenation
- Cognitive disorders in perioperative and intensive care
- Neurotoxicity of anaesthetics on the developing brain
- The endothelial glycocalyx and fluid therapy in critical care and perioperative medicine