Targeting the endothelial glycocalyx in acute critical illness as a challenge for clinical and laboratory medicine

References

• Tarbell JM, Cancel LM. The glycocalyx and its significance in human medicine. J Intern Med. 2016;280:97–113.
   PubMed Web of Science ®Google Scholar
• Schmidt EP, Yang Y, Janssen WJ, et al. The pulmonary endothelial glycocalyx regulates neutrophil adhesion and lung injury during experimental sepsis. Nat Med. 2012;18:1217–1223.
   PubMed Web of Science ®Google Scholar
• Nieuwdorp M, Meuwese MC, Vink H, et al. The endothelial glycocalyx: a potential barrier between health and vascular disease. Curr Opin Lipidol. 2005;16:507–511.
   PubMed Web of Science ®Google Scholar
• Chappell D, Jacob M. Role of the glycocalyx in fluid management: Small things matter. Best Pract Res Clin Anaesthesiol. 2014;28:227–234.
   PubMedGoogle Scholar
• Alphonsus CS, Rodseth RN. The endothelial glycocalyx: a review of the vascular barrier. Anaesthesia. 2014;69:777–784.
   PubMed Web of Science ®Google Scholar
• Chelazzi C, Villa G, Mancinelli P, et al. Glycocalyx and sepsis-induced alterations in vascular permeability. Crit Care. 2015;19:26.
   PubMed Web of Science ®Google Scholar
• Lipowsky HH. The endothelial glycocalyx as a barrier to leukocyte adhesion and its mediation by extracellular proteases. Ann Biomed Eng. 2012;40:840–848.
   PubMed Web of Science ®Google Scholar
• van den Berg B, Vink H. Glycocalyx perturbation: cause or consequence of damage to the vasculature? Am J Physiol Heart Circ Physiol. 2006;290:H2174–H2175.
   PubMed Web of Science ®Google Scholar
• Reitsma S, Slaaf DW, Vink H, et al. The endothelial glycocalyx: composition, functions, and visualization. Pflugers Arch – Eur J Physiol. 2007;454:345–359.
   PubMed Web of Science ®Google Scholar
• Schött U, Solomon C, Fries D, et al. The endothelial glycocalyx and its disruption, protection and regeneration: a narrative review. Scand J Trauma Resusc Emerg Med. 2016;24:48.
   PubMed Web of Science ®Google Scholar
• Donati A, Damiani E, Domizi R, et al. Alteration of the sublingual microvascular glycocalyx in critically ill patients. Microvasc Res. 2013;90:86–89.
   PubMed Web of Science ®Google Scholar
• Chappell D, Westphal M, Jacob M. The impact of the glycocalyx on microcirculatory oxygen distribution in critical illness. Curr Opin Anaesthesiol. 2009;22:155–162.
   PubMed Web of Science ®Google Scholar
• Schmidt EP, Li G, Li L, et al. The circulating glycosaminoglycan signature of respiratory failure in critically ill adults. J Biol Chem. 2014;289:8194–8202.
   PubMed Web of Science ®Google Scholar
• Edwards MR, Mythen MG. Fluid therapy in critical illness. Extrem Physiol Med. 2014;3:16.
   PubMedGoogle Scholar
• Yini S, Heng Z, Xin A, et al. Effect of unfractionated heparin on endothelial glycocalyx in a septic shock model. Acta Anaesthesiol Scand. 2015;59:160–169.
   PubMed Web of Science ®Google Scholar
• Xu L, Yu W-K, Lin Z-L, et al. Chemical sympathectomy attenuates inflammation, glycocalyx shedding and coagulation disorders in rats with acute traumatic coagulopathy. Blood Coagul Fibrinolysis. 2015;26:152–160.
   PubMed Web of Science ®Google Scholar
• Kolářová H, Ambrůzová B, Svihálková Šindlerová L, et al. Modulation of endothelial glycocalyx structure under inflammatory conditions. Mediators Inflamm. 2014;2014:694312.
   PubMed Web of Science ®Google Scholar
• Nurden AT. Platelet membrane glycoproteins: a historical review. Semin Thromb Hemost. 2014;40:577–584.
   PubMed Web of Science ®Google Scholar
• Ebong EE, Lopez-Quintero SV, Rizzo V, et al. Shear-induced endothelial NOS activation and remodeling via heparan sulfate, glypican-1, and syndecan-1. Integr Biol (Camb). 2014;6:338–347.
   PubMed Web of Science ®Google Scholar
• Nijst P, Verbrugge FH, Grieten L, et al. The pathophysiological role of interstitial sodium in heart failure. J Am Coll Cardiol. 2015;65:378–388.
   PubMed Web of Science ®Google Scholar
• Vink H, Constantinescu AA, Spaan JA. Oxidized lipoproteins degrade the endothelial surface layer : implications for platelet-endothelial cell adhesion. Circulation. 2000;101:1500–1502.
   PubMed Web of Science ®Google Scholar
• Li Q, Bolli R, Qiu Y, et al. Gene therapy with extracellular superoxide dismutase attenuates myocardial stunning in conscious rabbits. Circulation. 1998;98:1438–1448.
   PubMed Web of Science ®Google Scholar
• Padberg J-S, Wiesinger A, di Marco GS, et al. Damage of the endothelial glycocalyx in chronic kidney disease. Atherosclerosis. 2014;234:335–343.
   PubMed Web of Science ®Google Scholar
• Kim K-J, Kim J-Y, Baek I-W, et al. Elevated serum levels of syndecan-1 are associated with renal involvement in patients with systemic lupus erythematosus. J Rheumatol. 2015;42:202–209.
   PubMed Web of Science ®Google Scholar
• Dane M, van den Berg B, Rabelink T. The endothelial glycocalyx: scratching the surface for cardiovascular disease in kidney failure. Atherosclerosis. 2014;235:56–57.
   PubMed Web of Science ®Google Scholar
• Meuwese MC, Mooij HL, Nieuwdorp M, et al. Partial recovery of the endothelial glycocalyx upon rosuvastatin therapy in patients with heterozygous familial hypercholesterolemia. J Lipid Res. 2009;50:148–153.
   PubMed Web of Science ®Google Scholar
• Wuethrich PY, Burkhard FC. New perioperative fluid and pharmacologic management protocol results in reduced blood loss, faster return of bowel function, and overall recovery. Curr Urol Rep. 2015;16:17.
   PubMed Web of Science ®Google Scholar
• Torres Filho IP, Torres LN, Salgado C, et al. 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–H1478.
   PubMed Web of Science ®Google Scholar
• Hahn RG. Hypervolaemia, the glycocalyx layer and the kinetics of infusion fluids. Acta Anaesthesiol Scand. 2015;59:814–815.
   PubMed Web of Science ®Google Scholar
• Nathan DM, Lachin J, Cleary P, et al. Intensive diabetes therapy and carotid intima-media thickness in type 1 diabetes mellitus. N Engl J Med. 2003;348:2294–2303.
   PubMed Web of Science ®Google Scholar
• Nieuwdorp M, van Haeften TW, Gouverneur MCLG, et al. Loss of endothelial glycocalyx during acute hyperglycemia coincides with endothelial dysfunction and coagulation activation in vivo. Diabetes. 2006;55:480–486.
   PubMed Web of Science ®Google Scholar
• Vlahu CA, Lemkes BA, Struijk DG, et al. Damage of the endothelial glycocalyx in dialysis patients. J Am Soc Nephrol. 2012;23:1900–1908.
   PubMed Web of Science ®Google Scholar
• VanTeeffelen JWGE, Constantinescu AA, Brands J, et al. Bradykinin- and sodium nitroprusside-induced increases in capillary tube haematocrit in mouse cremaster muscle are associated with impaired glycocalyx barrier properties. J Physiol. 2008;586:3207–3218.
   PubMed Web of Science ®Google Scholar
• Annecke T, Rehm M, Bruegger D, et al. Ischemia-reperfusion-induced unmeasured anion generation and glycocalyx shedding: sevoflurane versus propofol anesthesia. J Invest Surg. 2012;25:162–168.
   PubMed Web of Science ®Google Scholar
• Norgard-Sumnicht K, Varki A. Endothelial heparan sulfate proteoglycans that bind to L-selectin have glucosamine residues with unsubstituted amino groups. J Biol Chem. 1995;270:12012–12024.
   PubMed Web of Science ®Google Scholar
• Müller AM, Hermanns MI, Cronen C, et al. Comparative study of adhesion molecule expression in cultured human macro- and microvascular endothelial cells. Exp Mol. Pathology. 2002;73:171–180.
   Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Mulivor AW, Lipowsky HH. Inflammation- and ischemia-induced shedding of venular glycocalyx. Am J Physiol Heart Circ Physiol. 2004;286:H1672–H1680.
   PubMed Web of Science ®Google Scholar
• Henry CB, Duling BR. TNF-alpha increases entry of macromolecules into luminal endothelial cell glycocalyx. Am J Physiol Heart Circ Physiol. 2000;279:H2815–H2823.
   PubMed Web of Science ®Google Scholar
• Janssen GH, Tangelder GJ, Oude Egbrink MG, et al. Spontaneous leukocyte rolling in venules in untraumatized skin of conscious and anesthetized animals. Am J Physiol. 1994;267(3 Pt 2):H1199–H1204.
   Google Scholar
• Lennon FE, Singleton PA. Hyaluronan regulation of vascular integrity. Am J Cardiovasc Dis. 2011;1:200–213.
   PubMedGoogle Scholar
• Tkachenko E, Rhodes JM, Simons M. Syndecans: new kids on the signaling block. Circ Res. 2005;96:488–500.
   PubMed Web of Science ®Google Scholar
• Stewart RJ, Kashour TS, Marsden PA. Vascular endothelial platelet endothelial adhesion molecule-1 (PECAM-1) expression is decreased by TNF-alpha and IFN-gamma. Evidence for cytokine-induced destabilization of messenger ribonucleic acid transcripts in bovine endothelial cells. J Immunol. 1996;156:1221–1228.
   PubMed Web of Science ®Google Scholar
• Pejler G, Abrink M, Ringvall M, et al. Mast cell proteases. Adv Immunol. 2007;95:167–255.
   PubMed Web of Science ®Google Scholar
• Chappell D, Jacob M, Rehm M, et al. Heparinase selectively sheds heparan sulphate from the endothelial glycocalyx. Biol Chem. 2008;389:79–82.
   PubMed Web of Science ®Google Scholar
• Xiao J, Song Q, Li T, et al. Bacterial endotoxin-induced endothelial cell injury and calcium overload associated with Toll-like receptor and calcium signal. Zhonghua Wei Zhong Bing Ji Jiu Yi Xue. 2017;29:150–155.
   PubMedGoogle Scholar
• Becker BF, Jacob M, Leipert S, et al. Degradation of the endothelial glycocalyx in clinical settings: searching for the sheddases. Br J Clin Pharmacol. 2015;80:389–402.
   PubMed Web of Science ®Google Scholar
• Johansson P, Stensballe J, Ostrowski S. Shock induced endotheliopathy (SHINE) in acute critical illness – a unifying pathophysiologic mechanism. Crit Care. 2017;21:25.
   PubMed Web of Science ®Google Scholar
• Radeva MY, Waschke J. Mind the gap: mechanisms regulating the endothelial barrier. Acta Physiol. 2017 [cited Feb 23]. DOI:10.1111/apha.12860.
   PubMedGoogle Scholar
• Chappell D, Hofmann-Kiefer K, Jacob M, et al. TNF-alpha induced shedding of the endothelial glycocalyx is prevented by hydrocortisone and antithrombin. Basic Res Cardiol. 2008;104:78–89.
   PubMed Web of Science ®Google Scholar
• Colburn P, Kobayashi E, Buonassisi V. Depleted level of heparan sulfate proteoglycan in the extracellular matrix of endothelial cell cultures exposed to endotoxin. J Cell Physiol. 1994;159:121–130.
   PubMed Web of Science ®Google Scholar
• Becker BF, Chappell D, Bruegger D, et al. Therapeutic strategies targeting the endothelial glycocalyx: acute deficits, but great potential. Cardiovasc Res. 2010;87:300–310.
   PubMed Web of Science ®Google Scholar
• Becker BF, Chappell D, Jacob M. Endothelial glycocalyx and coronary vascular permeability: the fringe benefit. Basic Res Cardiol. 2010;105:687–701.
   PubMed Web of Science ®Google Scholar
• Henrich M, Gruss M, Weigand MA. Sepsis-induced degradation of endothelial glycocalix. Sci World J. 2010;10:917–923.
   Web of Science ®Google Scholar
• Chappell D, Jacob M, Hofmann-Kiefer K, et al. A rational approach to perioperative fluid management. Anesthesiology. 2008;109:723–740.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Jiang D, Liang J, Noble PW. Hyaluronan as an immune regulator in human diseases. Physiol Rev. 2011;91:221–264.
   PubMed Web of Science ®Google Scholar
• Kim MY, Muto J, Gallo RL. Hyaluronic acid oligosaccharides suppress TLR3-dependent cytokine expression in a TLR4-dependent manner. PLoS One. 2013;8:e72421.
   PubMed Web of Science ®Google Scholar
• Rops A, Loeven MA, van Gemst JJ, et al. Modulation of heparan sulfate in the glomerular endothelial glycocalyx decreases leukocyte influx during experimental glomerulonephritis. Kidney Int. 2014;86:932–942.
   PubMed Web of Science ®Google Scholar
• van Golen RF, van Gulik TM, Heger M. Mechanistic overview of reactive species-induced degradation of the endothelial glycocalyx during hepatic ischemia/reperfusion injury. Free Radic Biol Med. 2012;52:1382–1402.
   PubMed Web of Science ®Google Scholar
• Kaushal SWB. Cardiopulmonary bypass and the endothelial glycocalyx: shedding new light. 2015;150:1482–1483.
   Google Scholar
• Svennevig K, Hoel T, Thiara A, et al. Syndecan-1 plasma levels during coronary artery bypass surgery with and without cardiopulmonary bypass. Perfusion. 2008;23:165–171.
   PubMed Web of Science ®Google Scholar
• Endo K, Takino T, Miyamori H, et al. Cleavage of syndecan-1 by membrane type matrix metalloproteinase-1 stimulates cell migration. J Biol Chem. 2003;278:40764–40770.
   PubMed Web of Science ®Google Scholar
• Gronski TJ, Martin RL, Kobayashi DK, et al. Hydrolysis of a broad spectrum of extracellular matrix proteins by human macrophage elastase. J Biol Chem. 1997;272:12189–12194.
   PubMed Web of Science ®Google Scholar
• Suenaga N, Mori H, Itoh Y, et al. CD44 binding through the hemopexin-like domain is critical for its shedding by membrane-type 1 matrix metalloproteinase. Oncogene. 2005;24:859–868.
   PubMed Web of Science ®Google Scholar
• Rubio-Gayosso I. Reactive oxygen species mediate modification of glycocalyx during ischemia-reperfusion injury. AJP Hear Circ Physiol. 2006;290:H2247–H2256.
   PubMed Web of Science ®Google Scholar
• Vink H, Duling BR. Capillary endothelial surface layer selectively reduces plasma solute distribution volume. Am J Physiol Heart Circ Physiol. 2000;278:H285–H289.
   PubMed Web of Science ®Google Scholar
• Czarnowska E, Karwatowska-Prokopczuk E. Ultrastructural demonstration of endothelial glycocalyx disruption in the reperfused rat heart. Involvement of oxygen free radicals. Basic Res Cardiol. 1995;90:357–364.
   PubMed Web of Science ®Google Scholar
• Bruegger D, Rehm M, Jacob M, et al. Exogenous nitric oxide requires an endothelial glycocalyx to prevent postischemic coronary vascular leak in guinea pig hearts. Crit Care. 2008;12:R73.
   PubMed Web of Science ®Google Scholar
• van Golen RF, Reiniers MJ, Vrisekoop N, et al. The mechanisms and physiological relevance of glycocalyx degradation in hepatic ischemia/reperfusion injury. Antioxid Redox Signal. 2014;21:1098–1118.
   PubMed Web of Science ®Google Scholar
• Granger DN. Ischemia-reperfusion: mechanisms of microvascular dysfunction and the influence of risk factors for cardiovascular disease. Microcirculation. 1999;6:167–178.
   PubMed Web of Science ®Google Scholar
• Seal JB, Gewertz BL. Vascular dysfunction in ischemia-reperfusion injury. Ann Vasc Surg. 2005;19:572–584.
   PubMed Web of Science ®Google Scholar
• Kurose I, Argenbright LW, Wolf R, et al. Ischemia/reperfusion-induced microvascular dysfunction: role of oxidants and lipid mediators. Am J Physiol. 1997;272(6 Pt 2):H2976–H2982.
   Google Scholar
• Rehm M, Bruegger D, Christ F, et al. Shedding of the endothelial glycocalyx in patients undergoing major vascular surgery with global and regional ischemia. Circulation. 2007;116:1896–1906.
   PubMed Web of Science ®Google Scholar
• Oliver MG, Specian RD, Perry MA, et al. Morphologic assessment of leukocyte-endothelial cell interactions in mesenteric venules subjected to ischemia and reperfusion. Inflammation. 1991;15:331–346.
   PubMed Web of Science ®Google Scholar
• Beuk RJ, Heineman E, Tangelder GJ, et al. Total warm ischemia and reperfusion impairs flow in all rat gut layers but increases leukocyte–vessel wall interactions in the submucosa only. Ann Surg. 2000;231:96–104.
   PubMed Web of Science ®Google Scholar
• Vollmar B, Glasz J, Menger MD, et al. Leukocytes contribute to hepatic ischemia/reperfusion injury via intercellular adhesion molecule-1-mediated venular adherence. Surgery. 1995;117:195–200.
   PubMed Web of Science ®Google Scholar
• Kupinski AM, Shah DM, Bell DR. Transvascular albumin flux in rabbit hindlimb after tourniquet ischemia. Am J Physiol. 1993;264:H901–H908.
   PubMed Web of Science ®Google Scholar
• Beresewicz A, Czarnowska E, Maczewski M. Ischemic preconditioning and superoxide dismutase protect against endothelial dysfunction and endothelium glycocalyx disruption in the postischemic guinea-pig hearts. Mol Cell Biochem. 1998;186:87–97.
   PubMed Web of Science ®Google Scholar
• Ward BJ, Donnelly JL. Hypoxia induced disruption of the cardiac endothelial glycocalyx: implications for capillary permeability. Cardiovasc Res. 1993;27:384–389.
   PubMed Web of Science ®Google Scholar
• Onat D, Brillon D, Colombo PC, et al. Human vascular endothelial cells: a model system for studying vascular inflammation in diabetes and atherosclerosis. Curr Diab Rep. 2011;11:193–202.
   PubMed Web of Science ®Google Scholar
• Snoeijs MG, Vink H, Voesten N, et al. Acute ischemic injury to the renal microvasculature in human kidney transplantation. Am J Physiol Renal Physiol. 2010;299:F1134–F1140.
   PubMed Web of Science ®Google Scholar
• Arroyo-Flores B, Chi-Ahumada E, Briones-Cerecero E, et al. Cardiac ischemia and ischemia/reperfusion cause wide proteolysis of the coronary endothelial luminal membrane: possible dysfunctions. Tocmj. 2011;5:239–245.
   Google Scholar
• Chappell D, Brettner F, Doerfler N, et al. Protection of glycocalyx decreases platelet adhesion after ischaemia/reperfusion. An animal study. Eur J Anaesthesiol. 2014;31:474–481.
   PubMed Web of Science ®Google Scholar
• Chappell D, Jacob M, Hofmann-Kiefer K, et al. Hydrocortisone preserves the vascular barrier by protecting the endothelial glycocalyx. Anesthesiology. 2007;107:776–784.
   PubMed Web of Science ®Google Scholar
• Bruegger D, Brettner F, Rossberg I, et al. Acute degradation of the endothelial glycocalyx in infants undergoing cardiac surgical procedures. Ann Thorac Surg. 2015;99:926–931.
   PubMed Web of Science ®Google Scholar
• Bruegger D, Schwartz L, Chappell D, 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.
   PubMed Web of Science ®Google Scholar
• Singer M, Deutschman CS, Seymour CW, et al. The Third International Consensus Definitions for Sepsis and Septic Shock (Sepsis-3). JAMA. 2016;315:801–810.
   PubMed Web of Science ®Google Scholar
• Schouten M, Wiersinga WJ, Levi M, et al. Inflammation, endothelium, and coagulation in sepsis. J Leukoc Biol. 2008;83:536–545.
   PubMed Web of Science ®Google Scholar
• Nelson A, Berkestedt I, Schmidtchen A, et al. Increased levels of glycosaminoglycans during septic shock: relation to mortality and the antibacterial actions of plasma. Shock. 2008;30:623–627.
   PubMed Web of Science ®Google Scholar
• Steppan J, Hofer S, Funke B, et al. Sepsis and major abdominal surgery lead to flaking of the endothelial glycocalix. J Surg Res. 2011;165:136–141.
   PubMed Web of Science ®Google Scholar
• Sallisalmi M, Tenhunen J, Yang R, et al. Vascular adhesion protein-1 and syndecan-1 in septic shock. Acta Anaesthesiol Scand. 2012;56:316–322.
   PubMed Web of Science ®Google Scholar
• Anand D, Ray S, Srivastava LM, et al. Evolution of serum hyaluronan and syndecan levels in prognosis of sepsis patients. Clin Biochem. 2016;49:768–776.
   PubMed Web of Science ®Google Scholar
• Rahbar E, Cardenas JC, Baimukanova G, et al. Endothelial glycocalyx shedding and vascular permeability in severely injured trauma patients. J Transl Med. 2015;13:117.
   PubMed Web of Science ®Google Scholar
• Torres Filho I, Torres LN, Sondeen JL, et al. In vivo evaluation of venular glycocalyx during hemorrhagic shock in rats using intravital microscopy. Microvasc Res. 2013;85:128–133.
   PubMed Web of Science ®Google Scholar
• Johansson PI, Stensballe J, Rasmussen LS, et al. 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.
   PubMed Web of Science ®Google Scholar
• Schmidt EP, Overdier KH, Sun X, et al. Urinary glycosaminoglycans predict outcomes in septic shock and Acute Respiratory Distress Syndrome. Am J Respir Crit Care Med. 2016;194:439–449.
   PubMed Web of Science ®Google Scholar
• De Backer D, Orbegozo Cortes D, Donadello K, et al. Pathophysiology of microcirculatory dysfunction and the pathogenesis of septic shock. Virulence. 2014;5:73–79.
   PubMed Web of Science ®Google Scholar
• Chappell D, Dörfler N, Jacob M, et al. Glycocalyx protection reduces leukocyte adhesion after ischemia/reperfusion. Shock. 2010;34:133–139.
   PubMed Web of Science ®Google Scholar
• Torres LN, Sondeen JL, Ji L, et al. Evaluation of resuscitation fluids on endothelial glycocalyx, venular blood flow, and coagulation function after hemorrhagic shock in rats. J Trauma Acute Care Surg. 2013;75:759–766.
   PubMed Web of Science ®Google Scholar
• Nelson A, Statkevicius S, Schött U, et al. Effects of fresh frozen plasma, Ringer’s acetate and albumin on plasma volume and on circulating glycocalyx components following haemorrhagic shock in rats. Icmx. 2016;4:6.
   Google Scholar
• Kim Y-H, Nijst P, Kiefer K, et al. Endothelial glycocalyx as biomarker for cardiovascular diseases: mechanistic and clinical implications. Curr Heart Fail Rep. 2017;14:117–126.
   PubMedGoogle Scholar
• Haeren RHL, Vink H, Staals J, et al. Protocol for intraoperative assessment of the human cerebrovascular glycocalyx. BMJ Open. 2017;7:e013954.
   PubMed Web of Science ®Google Scholar
• Noble MIM, Drake-Holland AJ, Vink H. Hypothesis: arterial glycocalyx dysfunction is the first step in the atherothrombotic process. Qjm. 2008;101:513–518.
   PubMed Web of Science ®Google Scholar
• Cahill PA, Redmond EM. Vascular endothelium – Gatekeeper of vessel health. Atherosclerosis. 2016;248:97–109.
   PubMed Web of Science ®Google Scholar
• Majerczak J, Grandys M, Duda K, et al. Moderate-intensity endurance training improves endothelial glycocalyx layer in healthy young men. Exp Physiol. 2017;102:70–85.
   PubMed Web of Science ®Google Scholar
• Al-Agha OM, Liu W, Chandrasekhar R, et al. CD138 (Syndecan-1) in thymic tumors: correlation with various World Health Organization types and clinical outcome. Int J Clin Exp Pathol. 2010;3:280–287.
   PubMed Web of Science ®Google Scholar
• Subramanian SV, Fitzgerald ML, Bernfield M. Regulated shedding of syndecan-1 and -4 ectodomains by thrombin and growth factor receptor activation. J Biol Chem. 1997;272:14713–14720.
   PubMed Web of Science ®Google Scholar
• Stern R. Hyaluronan catabolism: a new metabolic pathway. Eur J Cell Biol. 2004;83:317–325.
   PubMed Web of Science ®Google Scholar
• Stern R, Asari AASK. Hyaluronan fragments: an information-rich system. – PubMed – NCBI. Eur J Cell Biol. 2006;85:699–715.
   PubMed Web of Science ®Google Scholar
• Fraser JR, Laurent TC, Pertoft H, et al. Plasma clearance, tissue distribution and metabolism of hyaluronic acid injected intravenously in the rabbit. Biochem J. 1981;200:415–424.
   PubMed Web of Science ®Google Scholar
• Kataoka H, Ushiyama A, Kawakami H, et al. Fluorescent imaging of endothelial glycocalyx layer with wheat germ agglutinin using intravital microscopy. Microsc Res Tech. 2016;79:31–37.
   PubMed Web of Science ®Google Scholar
• Kataoka H, Ushiyama A, Akimoto Y, et al. Structural behavior of the endothelial glycocalyx is associated with pathophysiologic status in septic mice. Anesth Analg. 2017;125:874–883.
   PubMed Web of Science ®Google Scholar
• Lee DH, Dane MJC, van den Berg BM, et al. Deeper penetration of erythrocytes into the endothelial glycocalyx is associated with impaired microvascular perfusion. PLoS One. 2014;9:e96477.
   PubMed Web of Science ®Google Scholar
• Hutchings S, Watts S, Kirkman E. The Cytocam video microscope. A new method for visualising the microcirculation using Incident Dark Field technology. Clin Hemorheol Microcirc. 2015;62:261–271.
   Web of Science ®Google Scholar
• Lindert J, Werner J, Redlin M, et al. OPS imaging of human microcirculation: a short technical report. J Vasc Res. 2002;39:368–372.
   Google Scholar
• Goedhart PT, Khalilzada M, Bezemer R, et al. Sidestream Dark Field (SDF) imaging: a novel stroboscopic LED ring-based imaging modality for clinical assessment of the microcirculation. Opt Express. 2007;15:15101–15114.
   PubMed Web of Science ®Google Scholar
• Damiani E, Adrario E, Luchetti MM, et al. Plasma free hemoglobin and microcirculatory response to fresh or old blood transfusions in sepsis. PLoS One. 2015;10:e0122655.
   PubMed Web of Science ®Google Scholar
• Dane MJC, Khairoun M, Lee DH, et al. Association of kidney function with changes in the endothelial surface layer. Clin J Am Soc Nephrol. 2014;9:698–704.
   PubMed Web of Science ®Google Scholar
• Donati A, Damiani E, Botticelli L, et al. The aPC treatment improves microcirculation in severe sepsis/septic shock syndrome. BMC Anesthesiol. 2013;13:25.
   PubMed Web of Science ®Google Scholar
• Aykut G, Veenstra G, Scorcella C, et al. Cytocam-IDF (incident dark field illumination) imaging for bedside monitoring of the microcirculation. Intensive Care Med Exp. 2015;3:40.
   PubMedGoogle Scholar
• Oberleithner H. Vascular endothelium leaves fingerprints on the surface of erythrocytes. Pflugers Arch. 2013;465:1451–1458.
   PubMed Web of Science ®Google Scholar
• Oberleithner H. Sodium selective erythrocyte glycocalyx and salt sensitivity in man. Pflugers Arch. 2015;467:1319–1325.
   PubMed Web of Science ®Google Scholar
• Gao S-L, Zhang Y, Zhang S-Y, et al. The hydrocortisone protection of glycocalyx on the intestinal capillary endothelium during severe acute pancreatitis. Shock. 2015;43:512–517.
   PubMed Web of Science ®Google Scholar
• Pesonen E, Keski-Nisula J, Andersson S, et al. High-dose methylprednisolone and endothelial glycocalyx in paediatric heart surgery. Acta Anaesthesiol Scand. 2016;60:1386–1394.
   PubMed Web of Science ®Google Scholar
• Flameng W, Borgers M, Van der Vusse GJ, et al. Cardioprotective effects of lidoflazine in extensive aorta-coronary bypass grafting. J Thorac Cardiovasc Surg. 1983;85:758–768.
   PubMed Web of Science ®Google Scholar
• Eskens BJM, Zuurbier CJ, van Haare J, et al. Effects of two weeks of metformin treatment on whole-body glycocalyx barrier properties in db/db mice. Cardiovasc Diabetol. 2013;12:175.
   PubMed Web of Science ®Google Scholar
• van Haare J, Kooi ME, van Teeffelen JWGE, et al. Metformin and sulodexide restore cardiac microvascular perfusion capacity in diet-induced obese rats. Cardiovasc Diabetol. 2017;16:47.
   PubMed Web of Science ®Google Scholar
• Haywood-Watson RJ, Holcomb JB, Gonzalez EA, et al. Modulation of syndecan-1 shedding after hemorrhagic shock and resuscitation. PLoS One. 2011;6:e23530.
   PubMed Web of Science ®Google Scholar
• Jacob M, Paul O, Mehringer L, et al. Albumin augmentation improves condition of guinea pig hearts after 4 hr of cold ischemia. Transplantation. 2009;87:956–965.
   PubMed Web of Science ®Google Scholar
• Chappell D, Jacob M, Hofmann-Kiefer K, et al. Antithrombin reduces shedding of the endothelial glycocalyx following ischaemia/reperfusion. Cardiovasc Res. 2009;83:388–396.
   PubMed Web of Science ®Google Scholar
• Marechal X, Favory R, Joulin O, et al. Endothelial glycocalyx damage during endotoxemia coincides with microcirculatory dysfunction and vascular oxidative stress. Shock. 2008;29:572–576.
   PubMed Web of Science ®Google Scholar
• Henry CB, Duling BR. Permeation of the luminal capillary glycocalyx is determined by hyaluronan. Am J Physiol. 1999;277:H508–H514.
   PubMed Web of Science ®Google Scholar
• Jacob M, Bruegger D, Rehm M, et al. Contrasting effects of colloid and crystalloid resuscitation fluids on cardiac vascular permeability. Anesthesiology. 2006;J104:1223–1231.
   PubMed Web of Science ®Google Scholar
• Rehm M, Zahler S, Lötsch 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.
   PubMed Web of Science ®Google Scholar
• Lipowsky HH, Lescanic A. Inhibition of inflammation induced shedding of the endothelial glycocalyx with low molecular weight heparin. Microvasc Res. 2017;112:72–78.
   PubMed Web of Science ®Google Scholar
• Li J, Yuan T, Zhao X, et al. Protective effects of sevoflurane in hepatic ischemia-reperfusion injury. Int J Immunopathol Pharmacol. 2016;29:300–307.
   PubMed Web of Science ®Google Scholar
• Annecke T, Chappell D, Chen C, et al. Sevoflurane preserves the endothelial glycocalyx against ischaemia-reperfusion injury. Br J Anaesth. 2010;104:414–421.
   PubMed Web of Science ®Google Scholar
• Starling EH. On the absorption of fluids from the connective tissue spaces. J Physiol (Lond). 1896;19:312–326.
   Google Scholar
• Levick JR, Michel CC. Microvascular fluid exchange and the revised Starling principle. Cardiovasc Res. 2010;87:198–210.
   PubMed Web of Science ®Google Scholar
• Adamson RH, Lenz JF, Zhang X, et al. Oncotic pressures opposing filtration across non-fenestrated rat microvessels. J Physiol (Lond). 2004;557:889–907.
   Google Scholar
• Zhang X, Adamson RH, Curry FE, et al. Transient regulation of transport by pericytes in venular microvessels via trapped microdomains. Proc Natl Acad Sci USA. 2008;105:1374–1379.
   PubMed Web of Science ®Google Scholar
• Myburgh JA, Finfer S, Bellomo R, et al. Hydroxyethyl starch or saline for fluid resuscitation in intensive care. N Engl J Med. 2012;367:1901–1911.
   PubMed Web of Science ®Google Scholar
• Guidet B, Martinet O, Boulain T, 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.
   PubMed Web of Science ®Google Scholar
• James MFM, Michell WL, Joubert IA, et al. 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. 2011;107:693–702.
   PubMed Web of Science ®Google Scholar
• Rehm M, Orth VH, Kreimeier U, et al. Changes in blood volume during acute normovolemic hemodilution with 5% albumin or 6% hydroxyethylstarch and intraoperative retransfusion. Anaesthesist. 2001;50:569–579.
   PubMed Web of Science ®Google Scholar
• Rehm M, Orth V, Kreimeier U, et al. Changes in intravascular volume during acute normovolemic hemodilution and intraoperative retransfusion in patients with radical hysterectomy. Anesthesiology. 2000;92:657–664.
   PubMed Web of Science ®Google Scholar
• Jacob M, Chappell D, Hofmann-Kiefer K, et al. The intravascular volume effect of Ringer's lactate is below 20%: a prospective study in humans. Crit Care. 2012;16:R86.
   PubMed Web of Science ®Google Scholar
• Chappell D, Jacob M, Becker BF, et al. Expedition glycocalyx. A newly discovered “Great Barrier Reef”. Anaesthesist. 2008;57:959–969.
   PubMed Web of Science ®Google Scholar
• Chappell D, Bruegger D, Potzel J, et al. Hypervolemia increases release of atrial natriuretic peptide and shedding of the endothelial glycocalyx. Crit Care. 2014;18:538.
   PubMed Web of Science ®Google Scholar
• Bruegger D, Jacob M, Rehm M, 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–H1999.
   PubMed Web of Science ®Google Scholar
• Marik P, Bellomo R. A rational approach to fluid therapy in sepsis. Br J Anaesth. 2016;116:339–349.
   PubMed Web of Science ®Google Scholar
• Omar AS, Ur Rahman M, Dhatt GS, et al. Dynamics of brain natriuretic peptide in critically ill patients with severe sepsis and septic shock. Saudi J Anaesth. 2013;7:270–276.
   PubMedGoogle Scholar
• Post F, Weilemann LS, Messow C-M, et al. B-type natriuretic peptide as a marker for sepsis-induced myocardial depression in intensive care patients. Crit Care Med. 2008;36:3030–3037.
   PubMed Web of Science ®Google Scholar
• Wang F, Wu Y, Tang L, et al. Brain natriuretic peptide for prediction of mortality in patients with sepsis: a systematic review and meta-analysis. Crit Care. 2012;16:R74.
   PubMed Web of Science ®Google Scholar
• Berg S, Golster M, Lisander B. Albumin extravasation and tissue washout of hyaluronan after plasma volume expansion with crystalloid or hypooncotic colloid solutions. Acta Anaesthesiol Scand. 2002;46:166–172.
   PubMed Web of Science ®Google Scholar
• De Backer D, Durand A. Monitoring the microcirculation in critically ill patients. Best Pract Res Clin Anaesthesiol. 2014;28:441–451.
   PubMedGoogle Scholar
• Aya HD, Ster IC, Fletcher N, et al. Pharmacodynamic analysis of a fluid challenge. Crit Care Med. 2016;44:880–891.
   PubMed Web of Science ®Google Scholar
• Kozar RA, Peng Z, Zhang R, et al. Plasma restoration of endothelial glycocalyx in a rodent model of hemorrhagic shock. Anesth Analg. 2011;112:1289–1295.
   PubMed Web of Science ®Google Scholar
• Bashandy GMN. Implications of recent accumulating knowledge about endothelial glycocalyx on anesthetic management. J Anesth. 2015;29:269–278.
   PubMed Web of Science ®Google Scholar
• Chappell D, Heindl B, Jacob M, et al. Sevoflurane reduces leukocyte and platelet adhesion after ischemia–reperfusion by protecting the endothelial glycocalyx. Anesthesiology. 2011;115:483–491.
   PubMed Web of Science ®Google Scholar
• Casanova J, Simon C, Vara E, et al. Sevoflurane anesthetic preconditioning protects the lung endothelial glycocalyx from ischemia reperfusion injury in an experimental lung autotransplant model. J Anesth. 2016;30:755–762.
   PubMed Web of Science ®Google Scholar
• Becker BF, Chen C, Chappell D, et al. Sevoflurane mitigates shedding of hyaluronan from the coronary endothelium, also during ischemia/reperfusion: an ex vivo animal study. Hypoxia (Auckl). 2016;4:81.
   PubMed Web of Science ®Google Scholar
• Lin M-C, Lin C-F, Li C-F, et al. Anesthetic propofol overdose causes vascular hyperpermeability by reducing endothelial glycocalyx and ATP production. Ijms. 2015;16:12092–12107.
   Web of Science ®Google Scholar
• Zeng Y, Liu XH, Tarbell JFB. Sphingosine 1-phosphate induced synthesis of glycocalyx on endothelial cells. Exp Cell Res. 2015;339:90–95.
   PubMed Web of Science ®Google Scholar
• Zeng Y, Adamson RH, Curry F-RE, et al. Sphingosine-1-phosphate protects endothelial glycocalyx by inhibiting syndecan-1 shedding. Am J Physiol Heart Circ Physiol. 2014;306:H363–H372.
   PubMed Web of Science ®Google Scholar
• Liu B, Ding X, Yang J. Effect of early goal directed therapy in the treatment of severe sepsis and/or septic shock: a meta-Analysis. Curr Med Res Opin. 2016;36:1–28.
   PubMed Web of Science ®Google Scholar
• Lekakis J, Abraham P, Balbarini A, et al. Methods for evaluating endothelial function: a position statement from the European Society of Cardiology Working Group on Peripheral Circulation. Eur J Cardiovasc Prev Rehabil. 2011;18:775–789.
   PubMed Web of Science ®Google Scholar