The endothelial glycocalyx: Emerging concepts in pulmonary edema and acute lung injury

Anesthesia and Analgesia

Volumn 117, Issue 3, 2013, Pages 664-674

  Collins, Stephen R ^a   Blank, Randal S ^a   Deatherage, Lindy S ^b   Dull, Randal O ^a,c  

^a UNIVERSITY OF VIRGINIA HEALTH SYSTEM   (United States)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF ILLINOIS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACUTE LUNG INJURY; ADULT RESPIRATORY DISTRESS SYNDROME; ARTICLE; BLOOD VESSEL PERMEABILITY; ENDOTHELIAL DYSFUNCTION; GLYCOCALYX; HEART MUSCLE CAPILLARY; HUMAN; HYDRAULIC PERMEABILITY; HYPOXIC LUNG VASOCONSTRICTION; LOBECTOMY; LUNG ARTERY PRESSURE; LUNG CAPILLARY PRESSURE; LUNG EDEMA; LUNG RESECTION; LUNG VASCULAR RESISTANCE; LUNG VENTILATION; MECHANOTRANSDUCTION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; STARLING LAW; ALGORITHM; CAPILLARY PERMEABILITY; ENDOTHELIUM; LUNG; PATHOLOGY; PHYSIOLOGY; REVIEW;

ACUTE LUNG INJURY; ALGORITHMS; CAPILLARY PERMEABILITY; ENDOTHELIUM; GLYCOCALYX; HUMANS; LUNG; MECHANOTRANSDUCTION, CELLULAR; PULMONARY EDEMA;

EID: 84883740953     PISSN: 00032999     EISSN: 15267598     Source Type: Journal    
DOI: 10.1213/ANE.0b013e3182975b85     Document Type: Article

References (116)

1. Reitsma S, Slaaf DW, Vink H, van Zandvoort MA, oude Egbrink MG. The endothelial glycocalyx: composition, functions, and visualization. Pflugers Arch 2007;454:345-59 (Pubitemid 46742429)
2. Weinbaum S, Tarbell JM, Damiano ER. The structure and function of the endothelial glycocalyx layer. Annu Rev Biomed Eng 2007;9:121-67 (Pubitemid 350246654)
3. Vink H, Duling BR. Capillary endothelial surface layer selectively reduces plasma solute distribution volume. Am J Physiol Heart Circ Physiol 2000;278:H285-9 (Pubitemid 30101882)
4. van den Berg BM, Vink H, Spaan JA. The endothelial glycocalyx protects against myocardial edema. Circ Res 2003;92:592-4 (Pubitemid 36417691)
5. van Haaren PM, Van Bavel E, Vink H, Spaan JA. Charge modification of the endothelial surface layer modulates the permeability barrier of isolated rat mesenteric small arteries. Am J Physiol Heart Circ Physiol 2005;289:H2503-7 (Pubitemid 41698564)
6. Mochizuki S, Vink H, Hiramatsu O, Kajita T, Shigeto F, Spaan JA, Kajiya F. Role of hyaluronic acid in shear-induced endotheliumderived nitric oxide release. Am J Physiol Heart Circ Physiol 2003;285:H722-26 (Pubitemid 36885905)
7. Constantinescu AA, Vink H, Spaan JA. Endothelial cell glycocalyx modulates immobilization of leukocytes at the endothelial surface. Arterioscler Thromb Vasc Biol 2003;23:1541-7 (Pubitemid 37108195)
8. Mulivor AW, Lipowsky HH. Inflammation-and ischemiainduced shedding of venular glycocalyx. Am J Physiol Heart Circ Physiol 2004;286:H1672-80 (Pubitemid 38525453)
9. Lipowsky HH. The endothelial glycocalyx as a barrier to leukocyte adhesion and its mediation by extracellular proteases. Ann Biomed Eng 2012;40:840-8
10. Starling EH. On the absorption of fluids from the connective tissue spaces. J Physiol 1896;19:312-26
11. Adamson RH, Lenz JF, Zhang X, Adamson GN, Weinbaum S, Curry FE. Oncotic pressures opposing filtration across nonfenestrated rat microvessels. J Physiol 2004;557:889-907 (Pubitemid 38961624)
12. Levick JR. Revision of the Starling principle: new views of tissue fluid balance. J Physiol 2004;557:704 (Pubitemid 38961609)
13. Landis EM. Micro-injection studies of capillary permeability. The relation between capillary pressure and the rate at which fluid passes through the walls of single capillaries. Am J Physiol 1927;82:217-38
14. Pappenheimer JR, Soto-Rivera A. Effective osmotic pressure of the plasma proteins and other quantities associated with the capillary circulation in the hindlimbs of cats and dogs. Am J Physiol 1948;152:471-91
15. Michel CC. Starling: the formulation of his hypothesis of microvascular fluid exchange and its significance after 100 years. Exp Physiol 1997;82:1-30 (Pubitemid 27060847)
16. Weinbaum S. 1997 Whitaker distinguished lecture: models to solve mysteries in biomechanics at the cellular level; a new view of fiber matrix layers. Ann Biomed Eng 1998;26:627-43 (Pubitemid 128609662)
17. Zhang X, Adamson RH, Curry FR, Weinbaum S. A 1-D model to explore the effects of tissue loading and tissue concentration gradients in the revised Starling principle. Am J Physiol Heart Circ Physiol 2006;291:H2950-64 (Pubitemid 44904097)
18. Effros RM, Parker JC. Pulmonary vascular heterogeneity and the Starling hypothesis. Microvasc Res 2009;78:71-7
19. Parker JC, Yoshikawa S. Vascular segmental permeabilities at high peak inflation pressure in isolated rat lungs. Am J Physiol Lung Cell Mol Physiol 2002;283:L1203-9 (Pubitemid 35379253)
20. Rippe B, Townsley M, Thigpen J, Parker JC, Korthuis RJ, Taylor AE. Effects of vascular pressure on the pulmonary microvasculature in isolated dog lungs. J Appl Physiol 1984;57:233-9 (Pubitemid 14055718)
21. Ehrhart IC, Hofman WF. Pressure-dependent increase in lung vascular permeability to water but not protein. J Appl Physiol 1992;72:211-8
22. Ehrhart IC, McCloud LL, Orfanos SE, Catravas JD, Hofman WF. Effect of high blood flow on pulmonary vascular permeability to protein. J Appl Physiol 1994;76:2342-7 (Pubitemid 24184751)
23. Parker JC, Ivey CL. Isoproterenol attenuates high vascular pressure-induced permeability increases in isolated rat lungs. J Appl Physiol 1997;83:1962-7 (Pubitemid 28006497)
24. Parker RE, Roselli RJ, Harris TR, Brigham KL. Effects of graded increases in pulmonary vascular pressures on lung fluid balance in unanesthetized sheep. Circ Res 1981;49:1164-72 (Pubitemid 11029253)
25. Dull RO, Cluff M, Kingston J, Hill D, Chen H, Hoehne S, Malleske DT, Kaur R. Lung heparan sulfates modulate K (fc) during increased vascular pressure: evidence for glycocalyxmediated mechanotransduction. Am J Physiol Lung Cell Mol Physiol 2012;302:L816-28
26. Tarbell JM, Demaio L, Zaw MM. Effect of pressure on hydraulic conductivity of endothelial monolayers: role of endothelial cleft shear stress. J Appl Physiol 1999;87:261-8 (Pubitemid 29330690)
27. Dull RO, Mecham I, McJames S. Heparan sulfates mediate pressureinduced increase in lung endothelial hydraulic conductivity via nitric oxide/reactive oxygen species. Am J Physiol Lung Cell Mol Physiol 2007;292:L1452-8 (Pubitemid 47077361)
28. Majno G, Palade GE. Studies on inflammation. The effect of histamine and serotonin on vascular permeability: an electron microscopic study. J Cell Biol 1961;11:571-605
29. Dudek SM, Garcia JG. Cytoskeletal regulation of pulmonary vascular permeability. J Appl Physiol 2001;91:1487-500 (Pubitemid 32900340)
30. Hirata A, Baluk P, Fujiwara T, McDonald DM. Localization of focal silver staining at endothelial gaps in inflamed venules examined by scanning electron microscopy. Am J Physiol Lung Cell Mol Physiol 1995;269:L403-18
31. Shirley HH Jr, Wolfram CG, Wasserman K, Mayerson HS. Capillary permeability to macromolecules: stretched pore phenomenon. Am J Physiol 1957;190:189-93
32. Wasserman K, Loeb L, Mayerson HS. Capillary permeability to macromolecules. Circ Res 1955;3:594-603
33. Curry FR, Noll T. Spotlight on microvascular permeability. Cardiovasc Res 2010;87:195-7
34. Curry FE, Michel CC. A fiber matrix model of capillary permeability. Microvasc Res 1980;20:96-9 (Pubitemid 10087148)
35. Tarbell JM. Shear stress and the endothelial transport barrier. Cardiovasc Res 2010;87:320-30
36. O'Callaghan R, Job KM, Dull RO, Hlady V. Stiffness and heterogeneity of the pulmonary endothelial glycocalyx measured by atomic force microscopy. Am J Physiol Lung Cell Mol Physiol 2011;301:L353-60
37. Gao L, Lipowsky HH. Composition of the endothelial glycocalyx and its relation to its thickness and diffusion of small solutes. Microvasc Res 2010;80:394-401
38. Pries AR, Secomb TW, Gaehtgens P. The endothelial surface layer. Pflugers Arch 2000;440:653-66
39. Jacob M, Bruegger D, Rehm M, Stoeckelhuber M, Welsch U, Conzen P, Becker BF. The endothelial glycocalyx affords compatibility of Starling's principle and high cardiac interstitial albumin levels. Cardiovasc Res 2007;73:575-86 (Pubitemid 46073952)
40. Henry CB, Duling BR. Permeation of the luminal capillary glycocalyx is determined by hyaluronan. Am J Physiol 1999;277:H508-14 (Pubitemid 29415963)
41. Mulivor AW, Lipowsky HH. Role of glycocalyx in leukocyteendothelial cell adhesion. Am J Physiol Heart Circ Physiol 2002;283:H1282-91
42. Shimada K, Kobayashi M, Kimura S, Nishinaga M, Takeuchi K, Ozawa T. Anticoagulant heparin-like glycosaminoglycans on endothelial cell surface. Jpn Circ J 1991;55:1016-21
43. Abrahamsson T, Brandt U, Marklund SL, Sjöqvist PO. Vascular bound recombinant extracellular superoxide dismutase type C protects against the detrimental effects of superoxide radicals on endothelium-dependent arterial relaxation. Circ Res 1992;70:264-71
44. Vink H, Duling BR. Identification of distinct luminal domains for macromolecules, erythrocytes, and leukocytes within mammalian capillaries. Circ Res 1996;79:581-9 (Pubitemid 26276918)
45. van Haaren PM, Van Bavel E, Vink H, Spaan JA. Localization of the permeability barrier to solutes in isolated arteries by confocal microscopy. Am J Physiol Heart Circ Physiol 2003;285:H2848-56 (Pubitemid 37443106)
46. Adamson RH. Permeability of frog mesenteric capillaries after partial pronase digestion of the endothelial glycocalyx. J Physiol 1990;428:1-13 (Pubitemid 20313642)
47. Ueda A, Shimomura M, Ikeda M, Yamaguchi R, Tanishita K. Effect of glycocalyx on shear-dependent albumin uptake in endothelial cells. Am J Physiol Heart Circ Physiol 2004;287:H2287-94 (Pubitemid 39430768)
48. Grichnik KP, D'Amico TA. Acute lung injury and acute respiratory distress syndrome after pulmonary resection. Semin Cardiothorac Vasc Anesth 2004;8:317-34 (Pubitemid 39603177)
49. Maniatis NA, Orfanos SE. The endothelium in acute lung injury/acute respiratory distress syndrome. Curr Opin Crit Care 2008;14:22-30
50. Kuebler WM, Ying X, Bhattacharya J. Pressure-induced endothelial Ca (2+) oscillations in lung capillaries. Am J Physiol Lung Cell Mol Physiol 2002;282:L917-23 (Pubitemid 34654607)
51. Dull RO, Jo H, Sill H, Hollis TM, Tarbell JM. The effect of varying albumin concentration and hydrostatic pressure on hydraulic conductivity and albumin permeability of cultured endothelial monolayers. Microvasc Res 1991;41:390-407
52. Dull RO, Dinavahi R, Schwartz L, Humphries DE, Berry D, Sasisekharan R, Garcia JG. Lung endothelial heparan sulfates mediate cationic peptide-induced barrier dysfunction: a new role for the glycocalyx. Am J Physiol Lung Cell Mol Physiol 2003;285:L986-95 (Pubitemid 37310088)
53. Kuebler WM, Uhlig U, Goldmann T, Schael G, Kerem A, Exner K, Martin C, Vollmer E, Uhlig S. Stretch activates nitric oxide production in pulmonary vascular endothelial cells in situ. Am J Respir Crit Care Med 2003;168:1391-8 (Pubitemid 37492903)
54. Florian JA, Kosky JR, Ainslie K, Pang Z, Dull RO, Tarbell JM. Heparan sulfate proteoglycan is a mechanosensor on endothelial cells. Circ Res 2003;93:e136-42
55. Zharikov SI, Sigova AA, Chen S, Bubb MR, Block ER. Cytoskeletal regulation of the L-arginine/NO pathway in pulmonary artery endothelial cells. Am J Physiol Lung Cell Mol Physiol 2001;280:L465-73
56. Bucci M, Roviezzo F, Posadas I, Yu J, Parente L, Sessa WC, Ignarro LJ, Cirino G. Endothelial nitric oxide synthase activation is critical for vascular leakage during acute inflammation in vivo. Proc Natl Acad Sci U S A 2005;102:904-8 (Pubitemid 40282763)
57. Giantsos KM, Kopeckova P, Dull RO. The use of an endotheliumtargeted cationic copolymer to enhance the barrier function of lung capillary endothelial monolayers. Biomaterials 2009;30:5885-91
58. Thi MM, Tarbell JM, Weinbaum S, Spray DC. The role of the glycocalyx in reorganization of the actin cytoskeleton under fluid shear stress: a "bumper-car" model. Proc Natl Acad Sci U S A 2004;101:16483-8 (Pubitemid 39557739)
59. Henry CB, Duling BR. TNF-alpha increases entry of macromolecules into luminal endothelial cell glycocalyx. Am J Physiol Heart Circ Physiol 2000;279:H2815-23 (Pubitemid 32005870)
60. Vink H, Constantinescu AA, Spaan JA. Oxidized lipoproteins degrade the endothelial surface layer: implications for plateletendothelial cell adhesion. Circulation 2000;101:1500-2 (Pubitemid 30180883)
61. Huxley VH, Williams DA. Role of a glycocalyx on coronary arteriole permeability to proteins: evidence from enzyme treatments. Am J Physiol Heart Circ Physiol 2000;278:H1177-85 (Pubitemid 30235494)
62. Van Teeffelen JW, Dekker S, Fokkema DS, Siebes M, Vink H, Spaan JA. Hyaluronidase treatment of coronary glycocalyx increases reactive hyperemia but not adenosine hyperemia in dog hearts. Am J Physiol Heart Circ Physiol 2005;289:H2508-13 (Pubitemid 41698565)
63. van den Berg B, Vink H. Glycocalyx perturbation: cause or consequence of damage to the vasculature? Am J Physiol Heart Circ Physiol 2006;290:H2174-5 (Pubitemid 43846041)
64. Becker BF, Chappell D, Bruegger D, Annecke T, Jacob M. Therapeutic strategies targeting the endothelial glycocalyx: acute deficits, but great potential. Cardiovasc Res 2010;87:300-10
65. Park BJ. Respiratory failure following pulmonary resection. Semin Thorac Cardiovasc Surg 2007;19:374-9 (Pubitemid 351461260)
66. Jordan S, Mitchell JA, Quinlan GJ, Goldstraw P, Evans TW. The pathogenesis of lung injury following pulmonary resection. Eur Respir J 2000;15:790-9 (Pubitemid 30196311)
67. Turnage WS, Lunn JJ. Postpneumonectomy pulmonary edema. A retrospective analysis of associated variables. Chest 1993;103:1646-50 (Pubitemid 23174291)
68. Mathru M, Blakeman B, Dries DJ, Kleinman B, Kumar P. Permeability pulmonary edema following lung resection. Chest 1990;98:1216-8 (Pubitemid 20381291)
69. Turnage WS, Lunn JJ. Postpneumonectomy pulmonary edema. A retrospective analysis of associated variables. Chest 1993;103:1646-50 (Pubitemid 23174291)
70. van der Werff YD, van der Houwen HK, Heijmans PJ, Duurkens VA, Leusink HA, van Heesewijk HP, de Boer A. Postpneumonectomy pulmonary edema. A retrospective analysis of incidence and possible risk factors. Chest 1997;111:1278-84 (Pubitemid 27200085)
71. Licker M, de Perrot M, Spiliopoulos A, Robert J, Diaper J, Chevalley C, Tschopp JM. Risk factors for acute lung injury after thoracic surgery for lung cancer. Anesth Analg 2003;97:1558-65 (Pubitemid 37475100)
72. Schilling T, Kozian A, Huth C, Bühling F, Kretzschmar M, Welte T, Hachenberg T. The pulmonary immune effects of mechanical ventilation in patients undergoing thoracic surgery. Anesth Analg 2005;101:957-65 (Pubitemid 41383053)
73. Fernandez E, Keegan M, Brown DR. Intraoperative tidal volume as a risk factor for respiratory failure after pneumonectomy [abstract]. Chest 2005;128:129s
74. Wrigge H, Uhlig U, Zinserling J, Behrends-Callsen E, Ottersbach G, Fischer M, Uhlig S, Putensen C. The effects of different ventilatory settings on pulmonary and systemic inflammatory responses during major surgery. Anesth Analg 2004;98:775-81 (Pubitemid 38252675)
75. Parquin F, Marchal M, Mehiri S, Hervé P, Lescot B. Postpneumonectomy pulmonary edema: analysis and risk factors. Eur J Cardiothorac Surg 1996;10:929-32
76. Waller DA, Keavey P, Woodfine L, Dark JH. Pulmonary endothelial permeability changes after major lung resection. Ann Thorac Surg 1996;61:1435-40 (Pubitemid 26150235)
77. Filaire M, Fadel E, Decante B, Seccatore F, Mazmanian GM, Hervé P. Inhaled nitric oxide does not prevent postpneumonectomy pulmonary edema in pigs. J Thorac Cardiovasc Surg 2007;133:770-4
78. Nettelbladt O, Hällgren R. Hyaluronan (hyaluronic acid) in bronchoalveolar lavage fluid during the development of bleomycin-induced alveolitis in the rat. Am Rev Respir Dis 1989;140:1028-32 (Pubitemid 19259508)
79. Liu YY, Lee CH, Dedaj R, Zhao H, Mrabat H, Sheidlin A, Syrkina O, Huang PM, Garg HG, Hales CA, Quinn DA. Highmolecularweight hyaluronan-a possible new treatment for sepsis-induced lung injury: a preclinical study in mechanically ventilated rats. Crit Care 2008;12:R102
80. Singleton PA, Mirzapoiazova T, Guo Y, Sammani S, Mambetsariev N, Lennon FE, Moreno-Vinasco L, Garcia JG. High-molecular-weight hyaluronan is a novel inhibitor of pulmonary vascular leakiness. Am J Physiol Lung Cell Mol Physiol 2010;299:L639-51
81. Wang SF, Yang YS, Wei LX, Lu ZS, Guo MZ, Huang J, Peng LH, Sun G, Ling-Hu EQ, Meng JY. Diagnosis of gastric intraepithelial neoplasia by narrow-band imaging and confocal laser endomicroscopy. World J Gastroenterol 2012;18:4771-80
82. Zeldin RA, Normandin D, Landtwing D, Peters RM. Postpneumonectomy pulmonary edema. J Thorac Cardiovasc Surg 1984;87:359-65 (Pubitemid 14160439)
83. Crouch JD, Lucas CL, Keagy BA, Wilcox BR, Ha B. The acute effects of pneumonectomy on pulmonary vascular impedance in the dog. Ann Thorac Surg 1987;43:613-6 (Pubitemid 17081207)
84. Slinger PD. Postpneumonectomy pulmonary edema: good news, bad news. Anesthesiology 2006;105:2-5 (Pubitemid 44305182)
85. Williams EA, Quinlan GJ, Goldstraw P, Gothard JW, Evans TW. Postoperative lung injury and oxidative damage in patients undergoing pulmonary resection. Eur Respir J 1998;11:1028-34 (Pubitemid 28281018)
86. Broccard AF, Hotchkiss JR, Kuwayama N, Olson DA, Jamal S, Wangensteen DO, Marini JJ. Consequences of vascular flow on lung injury induced by mechanical ventilation. Am J Respir Crit Care Med 1998;157:1935-42
87. Briot R, Bayat S, Anglade D, Martiel JL, Grimbert F. Increased cardiac index due to terbutaline treatment aggravates capillaryalveolar macromolecular leakage in oleic acid lung injury in dogs. Crit Care 2009;13:R166
88. Broccard AF, Vannay C, Feihl F, Schaller MD. Impact of low pulmonary vascular pressure on ventilator-induced lung injury. Crit Care Med 2002;30:2183-90 (Pubitemid 35191565)
89. Hotchkiss JR Jr, Blanch L, Murias G, Adams AB, Olson DA, Wangensteen OD, Leo PH, Marini JJ. Effects of decreased respiratory frequency on ventilator-induced lung injury. Am J Respir Crit Care Med 2000;161:463-8 (Pubitemid 30129453)
90. Hotchkiss JR Jr, Blanch L, Naveira A, Adams AB, Carter C, Olson DA, Leo PH, Marini JJ. Relative roles of vascular and airspace pressures in ventilator-induced lung injury. Crit Care Med 2001;29:1593-8 (Pubitemid 32762342)
91. Anglade D, Corboz M, Menaouar A, Parker JC, Sanou S, Bayat S, Benchetrit G, Grimbert FA. Blood flow vs. venous pressure effects on filtration coefficient in oleic acid-injured lung. J Appl Physiol 1998;84:1011-23 (Pubitemid 28110633)
92. Ohkuda K, Nakahara K, Weidner WJ, Binder A, Staub NC. Lung fluid exchange after uneven pulmonary artery obstruction in sheep. Circ Res 1978;43:152-61 (Pubitemid 9004277)
93. Landolt CC, Matthay MA, Albertine KH, Roos PJ, Wiener-Kronish JP, Staub NC. Overperfusion, hypoxia, and increased pressure cause only hydrostatic pulmonary edema in anesthetized sheep. Circ Res 1983;52:335-41 (Pubitemid 13158749)
94. García-Delgado M, Colmenero-Ruiz M, Fernández- Sacristán MA, Rus-Mansilla C, Fernández-Mondéjar E. Effect of a catecholamineinduced increase in cardiac output on extravascular lung water. Crit Care Med 2001;29:931-5 (Pubitemid 32424340)
95. Townsley MI, Parker JC, Korthuis RJ, Taylor AE. Alterations in hemodynamics and Kf, c during lung mass resection. J Appl Physiol 1987;63:2460-6 (Pubitemid 18024871)
96. Licker M, de Perrot M, Spiliopoulos A, Robert J, Diaper J, Chevalley C, Tschopp JM. Risk factors for acute lung injury after thoracic surgery for lung cancer. Anesth Analg 2003;97:1558-65 (Pubitemid 37475100)
97. Schreiber T, Hueter L, Gaser E, Schmidt B, Schwarzkopf K, Rek H, Karzai W. PEEP has beneficial effects on inflammation in the injured and no deleterious effects on the noninjured lung after unilateral lung acid instillation. Intensive Care Med 2006;32:740-9
98. Motosugi H, Quinlan WM, Bree M, Doerschuk CM. Role of CD11b in focal acid-induced pneumonia and contralateral lung injury in rats. Am J Respir Crit Care Med 1998;157:192-8 (Pubitemid 28071282)
99. Schreiber T, Hueter L, Gaser E, Schmidt B, Schwarzkopf K, Karzai W. Effects of a catecholamine-induced increase in cardiac output on lung injury after experimental unilateral pulmonary acid instillation. Crit Care Med 2007;35:1741-8 (Pubitemid 46985879)
100. Lopez-Quintero SV, Amaya R, Pahakis M, Tarbell JM. The endothelial glycocalyx mediates shear-induced changes in hydraulic conductivity. Am J Physiol Heart Circ Physiol 2009;296:H1451-6
101. Czarnowska E, Karwatowska-Prokopczuk E. Role of oxygen free radicals in cardiocyte injury in the reperfused rat heart. Folia Histochem Cytobiol 1996;34 Suppl 1:25-6 (Pubitemid 26270531)
102. Nogae C, Makino N, Hata T, Nogae I, Takahashi S, Suzuki K, Taniguchi N, Yanaga T. Interleukin 1 alpha-induced expression of manganous superoxide dismutase reduces myocardial reperfusion injury in the rat. J Mol Cell Cardiol 1995;27:2091-9
103. Chen EP, Bittner HB, Davis RD, Folz RJ, Van Trigt P. Extracellular superoxide dismutase transgene overexpression preserves postischemic myocardial function in isolated murine hearts. Circulation 1996;94: II412-7 (Pubitemid 26363427)
104. Rubio-Gayosso I, Platts SH, Duling BR. Reactive oxygen species mediate modification of glycocalyx during ischemiareperfusion injury. Am J Physiol Heart Circ Physiol 2006;290:H2247-56 (Pubitemid 43846051)
105. Kurzelewski M, Czarnowska E, Beresewicz A. Superoxideand nitric oxide-derived species mediate endothelial dysfunction, endothelial glycocalyx disruption, and enhanced neutrophil adhesion in the post-ischemic guinea-pig heart. J Physiol Pharmacol 2005;56:163-78 (Pubitemid 40911085)
106. Bruegger D, Rehm M, Jacob M, Chappell D, Stoeckelhuber M, Welsch U, Conzen P, Becker BF. Exogenous nitric oxide requires an endothelial glycocalyx to prevent postischemic coronary vascular leak in guinea pig hearts. Crit Care 2008;12:R73
107. Rehm M, Bruegger D, Christ F, Conzen P, Thiel M, Jacob M, Chappell D, Stoeckelhuber M, Welsch U, Reichart B, Peter K, Becker BF. Shedding of the endothelial glycocalyx in patients undergoing major vascular surgery with global and regional ischemia. Circulation 2007;116:1896-906 (Pubitemid 350287085)
108. Bruegger D, Rehm M, Abicht J, Paul JO, Stoeckelhuber M, Pfirrmann M, Reichart B, Becker BF, Christ F. Shedding of the endothelial glycocalyx during cardiac surgery: on-pump versus off-pump coronary artery bypass graft surgery. J Thorac Cardiovasc Surg 2009;138:1445-7
109. Chappell D, Jacob M, Hofmann-Kiefer K, Rehm M, Welsch U, Conzen P, Becker BF. Antithrombin reduces shedding of the endothelial glycocalyx following ischaemia/reperfusion. Cardiovasc Res 2009;83:388-96
110. Nieuwdorp M, Meuwese MC, Mooij HL, Ince C, Broekhuizen LN, Kastelein JJ, Stroes ES, Vink H. Measuring endothelial glycocalyx dimensions in humans: a potential novel tool to monitor vascular vulnerability. J Appl Physiol 2008;104:845-52 (Pubitemid 351468815)
111. The ARDS Definition Task Force. Acute respiratory distress syndrome: the Berlin Definition. JAMA 2012;307:2526-33
112. Williams EA, Quinlan GJ, Anning PB, Goldstraw P, Evans TW. Lung injury following pulmonary resection in the isolated, blood-perfused rat lung. Eur Respir J 1999;14:745-50 (Pubitemid 29519331)
113. Ley K. The role of selectins in inflammation and disease. Trends Mol Med 2003;9:263-8 (Pubitemid 36841686)
114. Kaslovsky RA, Horgan MJ, Lum H, McCandless BK, Gilboa N, Wright SD, Malik AB. Pulmonary edema induced by phagocytosing neutrophils. Protective effect of monoclonal antibody against phagocyte CD18 integrin. Circ Res 1990;67:795-802 (Pubitemid 20315011)
115. Chappell D, Hofmann-Kiefer K, Jacob M, Rehm M, Briegel J, Welsch U, Conzen P, Becker BF. TNF-alpha induced shedding of the endothelial glycocalyx is prevented by hydrocortisone and antithrombin. Basic Res Cardiol 2009;104:78-89
116. Giantsos-Adams K, Lopez-Quintero V, Kopeckova P, Kopecek J, Tarbell JM, Dull R. Study of the therapeutic benefit of cationic copolymer administration to vascular endothelium under mechanical stress. Biomaterials 2011;32:288-94