Abstract
Current concepts of vascular permeability are largely still based on the Starling principle of 1896. Starling’s contribution to understanding vascular fluid homeostasis comes from realising that the transport of fluid to and from the interstitial space of peripheral tissues follows the balance between opposing oncotic and hydrostatic pressures. It is presumed that in peripheral tissues fluid is readily filtered from blood to tissues at the arterial/arteriolar side of the circulation and largely reabsorbed at the venular/venous aspect, excess fluid being removed from the tissue by the lymphatic system. This balance is determined particularly by the properties of the vascular barrier. Recent studies have shown that the endothelial glycocalyx, located with a thickness of at least 200 nm on the luminal side of healthy vasculature, plays a vital role in vascular permeability by constituting the vascular barrier together with the endothelial cells themselves. While water and electrolytes can freely pass through the glycocalyx, plasma proteins, especially albumin, interact strongly. Binding and intercalating plasma constituents with the structural elements of the glycocalyx creates the so-called endothelial surface layer. This is the actual interface between flowing blood and the endothelial cell membrane in vivo. The oncotic pressure difference pertinent to fluid homeostasis is not built up between the intravascular and the interstitial tissue spaces, but within a small protein-free zone beneath the glycocalyx surface layer. This explains why perturbation of the glycocalyx leads to a breakdown of both fluid and protein handling in the coronary vascular bed. Preventing damage to the glycocalyx seems to be a promising goal in cardioprotection in many clinical scenarios, including acute ischaemia, hypoxia and inflammation, and chronic vascular disease as in atherosclerosis, diabetes and hypertension.
Similar content being viewed by others
References
Adamson RH, Clough G (1992) Plasma proteins modify the endothelial cell glycocalyx of frog mesenteric microvessels. J Physiol 445:473–486
Adamson RH, Lenz JF, Zhang X, Adamson GN, Weinbaum S, Curry FE (2004) Oncotic pressures opposing filtration across non-fenestrated rat microvessels. J Physiol 557:889–907
Annecke T, Chappell D, Chen C, Jacob M, Welsch U, Sommerhoff CP, Rehm M, Conzen PF, Becker BF (2010) Sevoflurane preserves the endothelial glycocalyx against ischaemia-reperfusion injury. Br J Anaesth 104:414–421
Areskog NH, Arturson G, Grotte G, Wallenius G (1964) Studies on heart lymph. Arch Dis Child 39:182–186
Becker BF, Chappell D, Bruegger D, Annecke T, Jacob M (2010) Therapeutic strategies targeting the endothelial glycocalyx: acute deficits, but great potential. Cardiovasc Res 87:300–310
Beresewicz A, Czarnowska E, Maczewski M (1998) Ischemic preconditioning and superoxide dismutase protect against endothelial dysfunction and endothelium glycocalyx disruption in the postischemic guinea-pig hearts. Mol Cell Biochem 186:87–97
Brands J, Spaan JA, van den Berg BM, Vink H, VanTeeffelen JW (2010) Acute attenuation of glycocalyx barrier properties increases coronary blood volume independently of coronary flow reserve. Am J Physiol Heart Circ Physiol 298:H515–H523
Brandstrup B, Tonnesen H, Beier-Holgersen R, Hjortso E, Ording H, Lindorff-Larsen K, Rasmussen MS, Lanng C, Wallin L, Iversen LH, Gramkow CS, Okholm M, Blemmer T, Svendsen PE, Rottensten HH, Thage B, Riis J, Jeppesen IS, Teilum D, Christensen AM, Graungaard B, Pott F (2003) Effects of intravenous fluid restriction on postoperative complications: comparison of two perioperative fluid regimens: a randomized assessor-blinded multicenter trial. Ann Surg 238:641–648
Breuckmann F, Nassenstein K, Bucher C, Konietzka I, Kaiser G, Konorza T, Naber C, Skyschally A, Gres P, Heusch G, Erbel R, Barkhausen J (2009) Systematic analysis of functional and structural changes after coronary microembolization: a cardiac magnetic resonance imaging study. JACC Cardiovasc Imaging 2:121–130
Bruegger D, Jacob M, Rehm M, Loetsch M, Welsch U, Conzen P, Becker BF (2005) Atrial natriuretic peptide induces shedding of endothelial glycocalyx in coronary vascular bed of guinea pig hearts. Am J Physiol Heart Circ Physiol 289:H1993–H1999
Bruegger D, Rehm M, Abicht J, Paul JO, Stoeckelhuber M, Pfirrmann M, Reichart B, Becker BF, Christ F (2009) Shedding of the endothelial glycocalyx during cardiac surgery: on-pump versus off-pump coronary artery bypass graft surgery. J Thorac Cardiovasc Surg 138:1445–1447
Bruegger D, Rehm M, Jacob M, Chappell D, Stoeckelhuber M, Welsch U, Conzen P, Becker BF (2008) Exogenous nitric oxide requires an endothelial glycocalyx to prevent postischemic coronary vascular leak in guinea pig hearts. Crit Care 12:R73
Carden DL, Granger DN (2000) Pathophysiology of ischaemia-reperfusion injury. J Pathol 190:255–266
Chappell D, Doerfler N, Jacob M, Rehm M, Welsch U, Conzen P, Becker BF (2010) Glycocalyx protection reduces leukocyte adhesion following ischemia/reperfusion. Shock 34:133–139
Chappell D, Hofmann-Kiefer K, Jacob M, Rehm M, Briegel J, Welsch U, Conzen P, Becker BF (2009) TNF-alpha induced shedding of the endothelial glycocalyx is prevented by hydrocortisone and antithrombin. Basic Res Cardiol 104:78–89
Chappell D, Jacob M, Becker BF, Hofmann-Kiefer K, Conzen P, Rehm M (2008) Expedition glycocalyx: a newly discovered “Great Barrier Reef”. Anaesthesist 57:959–969
Chappell D, Jacob M, Hofmann-Kiefer K, Bruegger D, Rehm M, Conzen P, Welsch U, Becker BF (2007) Hydrocortisone preserves the vascular barrier by protecting the endothelial glycocalyx. Anesthesiology 107:776–784
Chappell D, Jacob M, Hofmann-Kiefer K, Conzen P, Rehm M (2008) A rational approach to perioperative fluid management. Anesthesiology 109:723–740
Chappell D, Jacob M, Hofmann-Kiefer K, Rehm M, Welsch U, Conzen P, Becker BF (2009) Antithrombin reduces shedding of the endothelial glycocalyx following ischaemia/reperfusion. Cardiovasc Res 83:388–396
Chappell D, Jacob M, Paul O, Mehringer L, Newman W, Becker BF (2008) Impaired glycocalyx barrier properties and increased capillary tube haematocrit. J Physiol 586:4585–4586
Chappell D, Jacob M, Paul O, Rehm M, Welsch U, Stoeckelhuber M, Conzen P, Becker BF (2009) The glycocalyx of the human umbilical vein endothelial cell: an impressive structure ex vivo but not in culture. Circ Res 104:1313–1317
Chappell D, Jacob M, Rehm M, Stoeckelhuber M, Welsch U, Conzen P, Becker BF (2008) Heparinase selectively sheds heparan sulphate from the endothelial glycocalyx. Biol Chem 389:79–82
Collard CD, Gelman S (2001) Pathophysiology, clinical manifestations, and prevention of ischemia-reperfusion injury. Anesthesiology 94:1133–1138
Curry FE, Michel CC (1980) A fiber matrix model of capillary permeability. Microvasc Res 20:96–99
Curry FR (2005) Atrial natriuretic peptide: an essential physiological regulator of transvascular fluid, protein transport, and plasma volume. J Clin Invest 115:1458–1461
Curry FR, Adamson RH (2010) Vascular permeability modulation at the cell, microvessel, or whole organ level: towards closing gaps in our knowledge. Cardiovasc Res 87:218–229
Curry FR, Rygh CB, Karlsen T, Wiig H, Adamson RH, Clark JF, Lin YC, Gassner B, Thorsen F, Moen I, Tenstad O, Kuhn M, Reed RK (2010) Atrial natriuretic peptide modulation of albumin clearance and contrast agent permeability in mouse skeletal muscle and skin: role in regulation of plasma volume. J Physiol 588:325–339
Czarnowska E, Karwatowska-Prokopczuk E (1995) Ultrastructural demonstration of endothelial glycocalyx disruption in the reperfused rat heart. Involvement of oxygen free radicals. Basic Res Cardiol 90:357–364
Danielli JF (1940) Capillary permeability and oedema in the perfused frog. J Physiol 98:109–129
Desai KV, Laine GA, Stewart RH, Cox CS Jr, Quick CM, Allen SJ, Fischer UM (2008) Mechanics of the left ventricular myocardial interstitium: effects of acute and chronic myocardial edema. Am J Physiol Heart Circ Physiol 294:H2428–H2434
Desjardins C, Duling BR (1990) Heparinase treatment suggests a role for the endothelial cell glycocalyx in regulation of capillary hematocrit. Am J Physiol 258:H647–H654
Dhalla NS, Elmoselhi AB, Hata T, Makino N (2000) Status of myocardial antioxidants in ischemia-reperfusion injury. Cardiovasc Res 47:446–456
Dongaonkar RM, Stewart RH, Geissler HJ, Laine GA (2010) Myocardial microvascular permeability, interstitial oedema, and compromised cardiac function. Cardiovasc Res 87:331–339
Drake TA, Morrissey JH, Edgington TS (1989) Selective cellular expression of tissue factor in human tissues. Implications for disorders of hemostasis and thrombosis. Am J Pathol 134:1087–1097
Dull RO, Mecham I, McJames S (2007) Heparan sulfates mediate pressure-induced increase in lung endothelial hydraulic conductivity via nitric oxide/reactive oxygen species. Am J Physiol Lung Cell Mol Physiol 292:L1452–L1458
Esmon CT (2002) Protein C pathway in sepsis. Ann Med 34:598–605
Field MC, Lumb JH, Adung’a VO, Jones NG, Engstler M (2009) Macromolecular trafficking and immune evasion in african trypanosomes. Int Rev Cell Mol Biol 278:1–67
Gebhard C, Akhmedov A, Mocharla P, Angstenberger J, Sahbai S, Camici GG, Luscher TF, Tanner FC (2010) PDGF-CC induces tissue factor expression: role of PDGF receptor alpha/beta. Basic Res Cardiol 105:349–356
Gilles S, Zahler S, Welsch U, Sommerhoff CP, Becker BF (2003) Release of TNF-alpha during myocardial reperfusion depends on oxidative stress and is prevented by mast cell stabilizers. Cardiovasc Res 60:608–616
Gotte M (2003) Syndecans in inflammation. FASEB J 17:575–591
Heindl B, Reichle FM, Zahler S, Conzen PF, Becker BF (1999) Sevoflurane and isoflurane protect the reperfused guinea pig heart by reducing postischemic adhesion of polymorphonuclear neutrophils. Anesthesiology 91:521–530
Huxley VH, Curry FE (1985) Albumin modulation of capillary permeability: test of an adsorption mechanism. Am J Physiol 248:H264–H273
Huxley VH, Curry FE (1987) Effect of superfusate albumin on single capillary hydraulic conductivity. Am J Physiol 252:H395–H401
Huxley VH, Curry FE (1991) Differential actions of albumin and plasma on capillary solute permeability. Am J Physiol 260:H1645–H1654
Huxley VH, Tucker VL, Verburg KM, Freeman RH (1987) Increased capillary hydraulic conductivity induced by atrial natriuretic peptide. Circ Res 60:304–307
Huxley VH, Wang J (2010) Cardiovascular sex differences influencing microvascular exchange. Cardiovasc Res 87:230–242
Jacob M, Bruegger D, Rehm M, Stoeckelhuber M, Welsch U, Conzen P, Becker BF (2007) The endothelial glycocalyx affords compatibility of Starling’s principle and high cardiac interstitial albumin levels. Cardiovasc Res 73:575–586
Jacob M, Bruegger D, Rehm M, Welsch U, Conzen P, Becker BF (2006) Contrasting effects of colloid and crystalloid resuscitation fluids on cardiac vascular permeability. Anesthesiology 104:1223–1231
Jacob M, Chappell D, Conzen P, Finsterer U, Krafft A, Becker BF, Rehm M (2008) Impact of the time window on plasma volume measurement with indocyanine green. Physiol Meas 29:761–770
Jacob M, Chappell D, Rehm M (2007) Clinical update: perioperative fluid management. Lancet 369:1984–1986
Jacob M, Chappell D, Rehm M (2009) Third space—fact or fiction? Best Pract Res Clin Anaesthesiol 23:145–157
Jacob M, Chappell D, Stoeckelhuber M, Welsch U, Rehm M, Bruegger D, Kaczmarek I, Conzen P, Becker BF (2010) Perspectives in microvascular fluid handling: does distribution of coagulation factors in human myocardium comply with plasma extravasation in venular coronary segments? J Vasc Res (in press)
Jacob M, Conzen P, Finsterer U, Krafft A, Becker BF, Rehm M (2007) Technical and physiological background of plasma volume measurement with indocyanine green: a clarification of misunderstandings. J Appl Physiol 102:1235–1242
Jacob M, Paul O, Mehringer L, Chappell D, Rehm M, Welsch U, Kaczmarek I, Conzen P, Becker BF (2009) Albumin augmentation improves condition of guinea pig hearts after 4 hours of cold ischemia. Transplantation 87:956–965
Jacob M, Rehm M, Loetsch M, Paul JO, Bruegger D, Welsch U, Conzen P, Becker BF (2007) The endothelial glycocalyx prefers albumin for evoking shear stress-induced, nitric oxide-mediated coronary dilatation. J Vasc Res 44:435–443
Juchem G, Weiss DR, Gansera B, Kemkes BM, Mueller-Hoecker J, Nees S (2010) Pericytes in the macrovascular intima: possible physiological and pathogenetic impact. Am J Physiol Heart Circ Physiol 298:H754–H770
Kanwar S, Hickey MJ, Kubes P (1998) Postischemic inflammation: a role for mast cells in intestine but not in skeletal muscle. Am J Physiol 275:G212–G218
Kellman P, Aletras AH, Mancini C, McVeigh ER, Arai AE (2007) T2-prepared SSFP improves diagnostic confidence in edema imaging in acute myocardial infarction compared to turbo spin echo. Magn Reson Med 57:891–897
Kleinbongard P, Heusch G, Schulz R (2010) TNFalpha in atherosclerosis, myocardial ischemia/reperfusion and heart failure. Pharmacol Ther 127:295–314
Kupatt C, Habazettl H, Zahler S, Weber C, Becker BF, Messmer K, Gerlach E (1997) ACE-inhibition prevents postischemic coronary leukocyte adhesion and leukocyte-dependent reperfusion injury. Cardiovasc Res 36:386–395
Langdell RD, Bowersox LW, Weaver RA, Gibson WS (1960) Coagulation properties of canine thoracic-duct lymph. Am J Physiol 199:626–628
Levick JR (1991) Capillary filtration-absorption balance reconsidered in light of dynamic extravascular factors. Exp Physiol 76:825–857
Levick JR, Michel CC (2010) Microvascular fluid exchange and the revised Starling principle. Cardiovasc Res 87:198–210
Lieleg O, Baumgartel RM, Bausch AR (2009) Selective filtering of particles by the extracellular matrix: an electrostatic bandpass. Biophys J 97:1569–1577
Lobo DN, Bostock KA, Neal KR, Perkins AC, Rowlands BJ, Allison SP (2002) Effect of salt and water balance on recovery of gastrointestinal function after elective colonic resection: a randomised controlled trial. Lancet 359:1812–1818
Lowell JA, Schifferdecker C, Driscoll DF, Benotti PN, Bistrian BR (1990) Postoperative fluid overload: not a benign problem. Crit Care Med 18:728–733
Luft JH (1966) Fine structures of capillary and endocapillary layer as revealed by ruthenium red. Fed Proc 25:1773–1783
McDonagh PF, Rauzzino MJ (1993) Stimulated leukocyte adhesion in coronary microcirculation is reduced by a calcium antagonist. Am J Physiol 265:H476–H483
Mehlhorn U, Geissler HJ, Laine GA, Allen SJ (2001) Myocardial fluid balance. Eur J Cardiothorac Surg 20:1220–1230
Meuwese MC, Mooij HL, Nieuwdorp M, van LB, Marck R, Vink H, Kastelein JJ, Stroes ES (2009) Partial recovery of the endothelial glycocalyx upon rosuvastatin therapy in patients with heterozygous familial hypercholesterolemia. J Lipid Res 50:148–153
Michel CC, Curry FR (2009) Glycocalyx volume: a critical review of tracer dilution methods for its measurement. Microcirculation 16:213–219
Miura T, Miki T (2008) Limitation of myocardial infarct size in the clinical setting: current status and challenges in translating animal experiments into clinical therapy. Basic Res Cardiol 103:501–513
Mulivor AW, Lipowsky HH (2004) Inflammation- and ischemia-induced shedding of venular glycocalyx. Am J Physiol Heart Circ Physiol 286:H1672–H1680
Nelson A, Berkestedt I, Schmidtchen A, Ljunggren L, Bodelsson M (2008) Increased levels of glycosaminoglycans during septic shock: relation to mortality and the antibacterial actions of plasma. Shock 30:623–627
Nieuwdorp M, Meuwese MC, Mooij HL, Ince C, Broekhuizen LN, Kastelein JJ, Stroes ES, Vink H (2008) Measuring endothelial glycocalyx dimensions in humans: a potential novel tool to monitor vascular vulnerability. J Appl Physiol 104:845–852
Nieuwdorp M, van Haeften TW, Gouverneur MC, Mooij HL, van Lieshout MH, Levi M, Meijers JC, Holleman F, Hoekstra JB, Vink H, Kastelein JJ, Stroes ES (2006) Loss of endothelial glycocalyx during acute hyperglycemia coincides with endothelial dysfunction and coagulation activation in vivo. Diabetes 55:480–486
Nisanevich V, Felsenstein I, Almogy G, Weissman C, Einav S, Matot I (2005) Effect of intraoperative fluid management on outcome after intraabdominal surgery. Anesthesiology 103:25–32
Noble MI, Drake-Holland AJ, Vink H (2008) Hypothesis: arterial glycocalyx dysfunction is the first step in the atherothrombotic process. QJM 101:513–518
Pahakis MY, Kosky JR, Dull RO, Tarbell JM (2007) The role of endothelial glycocalyx components in mechanotransduction of fluid shear stress. Biochem Biophys Res Commun 355:228–233
Parish CR (2006) The role of heparan sulphate in inflammation. Nat Rev Immunol 6:633–643
Platts SH, Duling BR (2004) Adenosine A3 receptor activation modulates the capillary endothelial glycocalyx. Circ Res 94:77–82
Platts SH, Linden J, Duling BR (2003) Rapid modification of the glycocalyx caused by ischemia-reperfusion is inhibited by adenosine A2A receptor activation. Am J Physiol Heart Circ Physiol 284:H2360–H2367
Potter DR, Damiano ER (2008) The hydrodynamically relevant endothelial cell glycocalyx observed in vivo is absent in vitro. Circ Res 102:770–776
Potter DR, Jiang J, Damiano ER (2009) The recovery time course of the endothelial cell glycocalyx in vivo and its implications in vitro. Circ Res 104:1318–1325
Pries AR, Kuebler WM (2006) Normal endothelium. Handb Exp Pharmacol 1:1–40
Pries AR, Secomb TW, Gaehtgens P (2000) The endothelial surface layer. Pflugers Arch 440:653–666
Raschke P, Becker BF, Leipert B, Schwartz LM, Zahler S, Gerlach E (1993) Postischemic dysfunction of the heart induced by small numbers of neutrophils via formation of hypochlorous acid. Basic Res Cardiol 88:321–339
Rehm M, Bruegger D, Christ F, Thiel M, Conzen P, Jacob M, Chappell D, Stoeckelhuber M, Welsch U, Reichart B, Peter K, Becker BF (2007) Shedding of the endothelial glycocalyx in patients undergoing major vascular surgery with global and regional ischemia. Circulation 116:1896–1906
Rehm M, Haller M, Orth V, Kreimeier U, Jacob M, Dressel H, Mayer S, Brechtelsbauer H, Finsterer U (2001) Changes in blood volume and hematocrit during acute preoperative volume loading with 5% albumin or 6% hetastarch solutions in patients before radical hysterectomy. Anesthesiology 95:849–856
Rehm M, Orth V, Kreimeier U, Thiel M, Haller M, Brechtelsbauer H, Finsterer U (2000) Changes in intravascular volume during acute normovolemic hemodilution and intraoperative retransfusion in patients with radical hysterectomy. Anesthesiology 92:657–664
Rehm M, Zahler S, Lotsch M, Welsch U, Conzen P, Jacob M, Becker BF (2004) Endothelial glycocalyx as an additional barrier determining extravasation of 6% hydroxyethyl starch or 5% albumin solutions in the coronary vascular bed. Anesthesiology 100:1211–1223
Reil JC, Gilles S, Zahler S, Brandl A, Drexler H, Hultner L, Matrisian LM, Welsch U, Becker BF (2007) Insights from knock-out models concerning postischemic release of TNFalpha from isolated mouse hearts. J Mol Cell Cardiol 42:133–141
Reitsma S, Slaaf DW, Vink H, van Zandvoort MA, oude Egbrink MG (2007) The endothelial glycocalyx: composition, functions, and visualization. Pflugers Arch 454:345–359
Ross AM, Gibbons RJ, Stone GW, Kloner RA, Alexander RW (2005) A randomized, double-blinded, placebo-controlled multicenter trial of adenosine as an adjunct to reperfusion in the treatment of acute myocardial infarction (AMISTAD-II). J Am Coll Cardiol 45:1775–1780
Rubio-Gayosso I, Platts SH, Duling BR (2006) Reactive oxygen species mediate modification of glycocalyx during ischemia-reperfusion injury. Am J Physiol Heart Circ Physiol 290:H2247–H2256
Sabrane K, Kruse MN, Fabritz L, Zetsche B, Mitko D, Skryabin BV, Zwiener M, Baba HA, Yanagisawa M, Kuhn M (2005) Vascular endothelium is critically involved in the hypotensive and hypovolemic actions of atrial natriuretic peptide. J Clin Invest 115:1666–1674
Salmon AH, Neal CR, Sage LM, Glass CA, Harper SJ, Bates DO (2009) Angiopoietin-1 alters microvascular permeability coefficients in vivo via modification of endothelial glycocalyx. Cardiovasc Res 83:24–33
Singh A, Satchell SC, Neal CR, McKenzie EA, Tooke JE, Mathieson PW (2007) Glomerular endothelial glycocalyx constitutes a barrier to protein permeability. J Am Soc Nephrol 18:2885–2893
Stafford-Smith M, Lefrak EA, Qazi AG, Welsby IJ, Barber L, Hoeft A, Dorenbaum A, Mathias J, Rochon JJ, Newman MF (2005) Efficacy and safety of heparinase I versus protamine in patients undergoing coronary artery bypass grafting with and without cardiopulmonary bypass. Anesthesiology 103:229–240
Starling E (1896) On the absorption of fluid from the connective tissue spaces. J Physiol 19:312–326
Szotowski B, Antoniak S, Rauch U (2006) Alternatively spliced tissue factor: a previously unknown piece in the puzzle of hemostasis. Trends Cardiovasc Med 16:177–182
Tarbell JM (2010) Shear stress and the endothelial transport barrier. Cardiovasc Res 87:320–330
Tarbell JM, Pahakis MY (2006) Mechanotransduction and the glycocalyx. J Intern Med 259:339–350
Tucker VL (1996) Plasma ANP levels and protein extravasation during graded expansion with equilibrated whole blood. Am J Physiol 271:R601–R609
van den Berg BM, Spaan JA, Vink H (2009) Impaired glycocalyx barrier properties contribute to enhanced intimal low-density lipoprotein accumulation at the carotid artery bifurcation in mice. Pflugers Arch 457:1199–1206
van den Berg BM, Vink H, Spaan JA (2003) The endothelial glycocalyx protects against myocardial edema. Circ Res 92:592–594
VanTeeffelen JW, Brands J, Vink H (2010) Agonist-induced impairment of glycocalyx exclusion properties: contribution to coronary effects of adenosine. Cardiovasc Res 87:311–319
Vink H, Constantinescu AA, Spaan JA (2000) Oxidized lipoproteins degrade the endothelial surface layer: implications for platelet-endothelial cell adhesion. Circulation 101:1500–1502
Vink H, Duling BR (1996) Identification of distinct luminal domains for macromolecules, erythrocytes, and leukocytes within mammalian capillaries. Circ Res 79:581–589
Vink H, Duling BR (2000) Capillary endothelial surface layer selectively reduces plasma solute distribution volume. Am J Physiol Heart Circ Physiol 278:H285–H289
Vogel J, Sperandio M, Pries AR, Linderkamp O, Gaehtgens P, Kuschinsky W (2000) Influence of the endothelial glycocalyx on cerebral blood flow in mice. J Cereb Blood Flow Metab 20:1571–1578
Ward BJ, Donnelly JL (1993) Hypoxia induced disruption of the cardiac endothelial glycocalyx: implications for capillary permeability. Cardiovasc Res 27:384–389
Ward BJ, Firth JA (1989) Effect of hypoxia on endothelial morphology and interendothelial junctions in the isolated perfused rat heart. J Mol Cell Cardiol 21:1337–1347
Weinbaum S, Tarbell JM, Damiano ER (2007) The structure and function of the endothelial glycocalyx layer. Annu Rev Biomed Eng 9:121–167
Yuan W, Li G, Zeng M, Fu BM (2010) Modulation of the blood-brain barrier permeability by plasma glycoprotein orosomucoid. Microvasc Res 80:148–157
Zahler S, Becker BF, Raschke P, Gerlach E (1994) Stimulation of endothelial adenosine A1 receptors enhances adhesion of neutrophils in the intact guinea pig coronary system. Cardiovasc Res 28:1366–1372
Zhang C (2008) The role of inflammatory cytokines in endothelial dysfunction. Basic Res Cardiol 103:398–406
Zhang C, Wu J, Xu X, Potter BJ, Gao X (2010) Direct relationship between levels of TNF-alpha expression and endothelial dysfunction in reperfusion injury. Basic Res Cardiol 105:453–464
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Becker, B.F., Chappell, D. & Jacob, M. Endothelial glycocalyx and coronary vascular permeability: the fringe benefit. Basic Res Cardiol 105, 687–701 (2010). https://doi.org/10.1007/s00395-010-0118-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00395-010-0118-z