Glycocalyx and sepsis-induced alterations in vascular permeability

Critical Care

Volumn 19, Issue 1, 2015, Pages

  Chelazzi, Cosimo ^a   Villa, Gianluca ^a   Mancinelli, Paola ^a   De Gaudio, A Raffaele ^a   Adembri, Chiara ^a  

^a UNIVERSITY OF FLORENCE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOCALYX PROTEIN; GLYCOPROTEIN; UNCLASSIFIED DRUG; BIOLOGICAL MARKER;

BIOCHEMICAL COMPOSITION; BLOOD VESSEL PERMEABILITY; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; HUMAN; INFLAMMATION; MEMBRANE STRUCTURE; MOLECULAR IMAGING; MOLECULAR PATHOLOGY; OXIDATIVE STRESS; PERMEABILITY BARRIER; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW; SEPSIS; TRANSMISSION ELECTRON MICROSCOPY; TREATMENT PLANNING; CAPILLARY PERMEABILITY; COMPLICATION; FLUID SHIFT; GLYCOCALYX; METABOLISM; MORTALITY; PATHOLOGY; PHYSIOLOGY;

BIOMARKERS; CAPILLARY PERMEABILITY; ENDOTHELIAL CELLS; FLUID SHIFTS; GLYCOCALYX; HUMANS; SEPSIS;

EID: 84939202132     PISSN: 13648535     EISSN: 1466609X     Source Type: Journal    
DOI: 10.1186/s13054-015-0741-z     Document Type: Review

References (74)

1. Dellinger RP, Levy MM, Carlet JM, Bion J, Parker MM, Jaeschke R, et al. Surviving Sepsis Campaign: international guidelines for management of severe sepsis and septic shock: 2008. Intensive Care Med. 2008;34:17-60.
2. Christaki E, Opal SM. Is the mortality rate for septic shock really decreasing? Curr Opin Crit Care. 2008;14:580-6.
3. De Backer D, Orbegozo Cortes D, Donadello K, Vincent JL. Pathophysiology of microcirculatory dysfunction and the pathogenesis of septic shock. Virulence. 2014;5:73-9.
4. Paulus P, Jennewein C, Zacharowski K. Biomarkers of endothelial dysfunction: can they help us deciphering systemic inflammation and sepsis? Biomarkers. 2011;16 Suppl 1:S11-21.
5. De Backer D, Creteur J, Preiser JC, Dubois MJ, Vincent JL. Microvascular blood flow is altered in patients with sepsis. Am J Respir Crit Care Med. 2002;166:98-104.
6. 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.
7. Donati A, Domizi R, Damiani E, Adrario E, Pelaia P, Ince C. From macrohemodynamic to the microcirculation. Crit Care Res Pract. 2013;2013:892710.
8. Salmon AH, Satchell SC. Endothelial glycocalyx dysfunction in disease: albuminuria and increased microvascular permeability. J Pathol. 2012;226:562-74.
9. De Gaudio AR, Adembri C, Grechi S, Novelli GP. Microalbuminuria as an early index of impairment of glomerular permeability in postoperative septic patients. Intensive Care Med. 2000;26:1364-8.
10. Karamysheva AF. Mechanisms of angiogenesis. Biochemistry (Mosc). 2008;73:751-62.
11. Levick JR, Smaje LH. An analysis of the permeability of a fenestra. Microvasc Res. 1987;33:233-56.
12. 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.
13. Li L, Ly M, Linhardt RJ. Proteoglycan sequence. Mol Biosyst. 2012;8:1613-25.
14. Luft HJ. Fine structure of capillary and endocapillary layer as revealed by ruthenium red. Fed Proc. 1966;25:1773-83.
15. Kolářová H, Ambrůzová B, Svihálková Šindlerová L, Klinke A, Kubala L. Modulation of endothelial glycocalyx structure under inflammatory conditions. Mediators Inflamm. 2014;2014:694312.
16. Pries AR, Secomb TW, Gaehtgens P. The endothelial surface layer. Pflugers Arch. 2000;440:653-66.
17. Megens RT, Reitsma S, Schiffers PH, Hilgers RH, De Mey JG, 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.
18. Copley AL, Staple PH. Haemorheological studies on the plasmatic zone in the microcirculation of the cheek pouch of Chinese and Syrian hamsters. Biorheology. 1962;1:3-14.
19. Lekakis J, Abraham P, Balbarini A, Blann A, Boulanger CM, Cockcroft J, 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;18:775-89.
20. 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;108:384-94.
21. Frati-Munari AC. Medical significance of endothelial glycocalyx. Arch Cardiol Mex. 2013;83:303-12.
22. Yuan S, Rigor R. Structure and function of exchange microvessels. In Regulation of Endothelial Barrier Function. Edited by Granger DN and Granger JP. San Rafael: Morgan & Claypool Life Sciences; 2010:1-13. [Granger DN and Granger JP (Series Editors): Integrated Systems Physiology:From Molecule to Function to Disease].
23. Serpa Neto A, Veelo DP, Peireira VG, de Assunção MS, Manetta JA, Espósito DC, et al. Fluid resuscitation with hydroxyethyl starches in patients with sepsis is associated with an increased incidence of acute kidney injury and use of renal replacement therapy: a systematic review and meta-analysis of the literature. J Crit Care. 2014;29:185.e1-7.
24. Caironi P, Tognoni G, Masson S, Fumagalli R, Pesenti A, Romero M, et al. Albumin replacement in patients with severe sepsis or septic shock. N Engl J Med. 2014;370:1412-21.
25. Bark BP, Persson J, Grände PO. Importance of the infusion rate for the plasma expanding effect of 5% albumin, 6% HES 130/0.4, 4% gelatin, and 0.9% NaCl in the septic rat. Crit Care Med. 2013;41:857-66.
26. Donati A, Damiani E, Domizi R, Romano R, Adrario E, Pelaia P, et al. Alteration of the sublingual microvascular glycocalyx in critically ill patients. Microvasc Res. 2013;90:86-9.
27. Schmidt EP, Yang Y, Janssen WJ, Gandjeva A, Perez MJ, Barthel L, et al. The pulmonary endothelial glycocalyx regulates neutrophil adhesion and lung injury during experimental sepsis. Nat Med. 2012;18:1217-23.
28. Singh A, Ramnath RD, Foster RR, Wylie EC, Fridén V, Dasgupta I, et al. Reactive oxygen species modulate the barrier function of the human glomerular endothelial glycocalyx. PLoS One. 2013;8:e55852.
29. Stehouwer CD, Smulders YM. Microalbuminuria and risk for cardiovascular disease: analysis of potential mechanisms. J Am Soc Nephrol. 2006;17:2106-11.
30. Forbes JM, Coughlan MT, Cooper ME. Oxidative stress as a major culprit in kidney disease in diabetes. Diabetes. 2008;57:1446-54.
31. Adachi T, Fukushima T, Usami Y, Hirano K. Binding of human xanthine oxidase to sulphated glycosaminoglycans on the endothelial-cell surface. Biochem J. 1993;289:523-7.
32. Becker M, Menger MD, Lehr HA. Heparin-released superoxide dismutase inhibits postischemic leukocyte adhesion to venular endothelium. Am J Physiol. 1994;267:H925-930.
33. Myburgh JA, Mythen MG. Resuscitation fluids. N Engl J Med. 2013;369:1243-51.
34. Henrich M, Gruss M, Weigand MA. Sepsis-induced degradation of endothelial glycocalix. Sci World J. 2010;10:917-23.
35. Wiesinger A, Peters W, Chappell D, Kentrup D, Reuter S, Pavenstädt H, et al. Nanomechanics of the endothelial glycocalyx in experimental sepsis. PLoS One. 2013;8:e80905.
36. Sakr Y, Dubois MJ, De Backer D, Creteur J, Vincent JL. Persistent microcirculatory alterations are associated with organ failure and death in patients with septic shock. Crit Care Med. 2004;32:1825-31.
37. Chelazzi C, Villa G, De Gaudio AR. Cardiorenal syndromes and sepsis. Int J Nephrol. 2011;2011:652967.
38. Steppan J, Hofer S, Funke B, Brenner T, Henrich M, Martin E, et al. Sepsis and major abdominal surgery lead to flaking of the endothelial glycocalix. J Surg Res. 2011;165:136-41.
39. Gunst J, Derese I, Aertgeerts A, Ververs EJ, Wauters A, Van den Berghe G, et al. Insufficient autophagy contributes to mitochondrial dysfunction, organ failure, and adverse outcome in an animal model of critical illness. Crit Care Med. 2013;41:182-94.
40. Adembri C, Sgambati E, Vitali L, Selmi V, Margheri M, Tani A, et al. Sepsis induces albuminuria and alterations in the glomerular filtration barrier: a morphofunctional study in the rat. Crit Care. 2011;15:R277.
41. Pierrakos C, Vincent JL. Sepsis biomarkers: a review. Crit Care. 2010;14:R15.
42. Nakamura T, Ushiyama C, Suzuki Y, Shoji H, Shimada N, Koide H. Hemoperfusion with polymyxin B immobilized fibers for urinary albumin excretion in septic patients with trauma. ASAIO J. 2002;48:244-8.
43. Hippenstiel S, Krüll M, Ikemann A, Risau W, Clauss M, Suttorp N. VEGF induces hyperpermeability by a direct action on endothelial cells. Am J Physiol. 1998;274:L678-84.
44. Rinaldi S, Adembri C, Grechi S, De Gaudio AR. Low-dose hydrocortisone during severe sepsis: effects on microalbuminuria. Crit Care Med. 2006;34:2334-9.
45. Abid O, Sun Q, Sugimoto K, Mercan D, Vincent JL. Predictive value of microalbuminuria in medical ICU patients: results of a pilot study. Chest. 2001;120:1984-8.
46. Herrera R, Almaguer M, Chipi J, Martínez O, Bacallao J, Rodríguez N, et al. Albuminuria as a marker of kidney and cardio-cerebral vascular damage. Isle of Youth Study (ISYS), Cuba. MEDICC Rev. 2010;12:20-6.
47. Koike K, Aiboshi J, Shinozawa Y, Sekine K, Endo T, Yamamoto Y. Correlation of glomerular permeability, endothelial injury, and postoperative multiple organ dysfunction. Surg Today. 2004;34:811-6.
48. Chappell D, Hofmann-Kiefer K, Jacob M, Rehm M, Briegel J, Welsch U, et al. TNF-alpha induced shedding of the endothelial glycocalyx is prevented by hydrocortisone and antithrombin. Basic Res Cardiol. 2009;104:78-89.
49. Moseley R, Waddington RJ, Embery G. Degradation of glycosaminoglycans by reactive oxygen species derived from stimulated polymorphonuclear leukocytes. Biochim Biophys Acta. 1997;1362:221-31.
50. Constantinescu A, Spaan JA, Arkenbout EK, Vink H, Vanteeffelen JW. Degradation of the endothelial glycocalyx is associated with chylomicron leakage in mouse cremaster muscle microcirculation. Thromb Haemost. 2011;105:790-801.
51. Iantorno M, Campia U, Di Daniele N, Nistico S, Forleo GB, Cardillo C, et al. Obesity, inflammation and endothelial dysfunction. J Biol Regul Homeost Agents. 2014;28:169-76.
52. van den Berg BM, Spaan JA, Rolf TM, Vink H. Atherogenic region and diet diminish glycocalyx dimension and increase intima-to-media ratios at murine carotid artery bifurcation. Am J Physiol Heart Circ Physiol. 2006;290:H915-20.
53. Meuwese MC, Mooij HL, Nieuwdorp M, van Lith B, Marck R, Vink H, et al. Partial recovery of the endothelial glycocalyx upon rosuvastatin therapy in patients with heterozygous familial hypercholesterolemia. J Lipid Res. 2009;50:148-53.
54. Zuurbier CJ, Demirci C, Koeman A, Vink H, Ince C. Short-term hyperglycemia increases endothelial glycocalyx permeability and acutely decreases lineal density of capillaries with flowing red blood cells. J Appl Physiol (1985). 2005;99:1471-6.
55. Broekhuizen LN, Lemkes BA, Mooij HL, Meuwese MC, Verberne H, Holleman F, et al. Effect of sulodexide on endothelial glycocalyx and vascular permeability in patients with type 2 diabetes mellitus. Diabetologia. 2010;53:2646-55.
56. Haywood-Watson RJ, Holcomb JB, Gonzalez EA, Peng Z, Pati S, Park PW, et al. Modulation of syndecan-1 shedding after hemorrhagic shock and resuscitation. PLoS One. 2011;6:e23530.
57. 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.
58. Lehr HA, Bittinger F, Kirkpatrick CJ. Microcirculatory dysfunction in sepsis: a pathogenetic basis for therapy? J Pathol. 2000;190:373-86.
59. Sarrazin S, Lyon M, Deakin JA, Guerrini M, Lassalle P, Delehedde M, et al. Characterization and binding activity of the chondroitin/dermatan sulfate chain from Endocan, a soluble endothelial proteoglycan. Glycobiology. 2010;20:1380-8.
60. Mikkelsen ME, Shah CV, Scherpereel A, Lanken PN, Lassalle P, Bellamy SL, et al. Lower serum endocan levels are associated with the development of acute lung injury after major trauma. J Crit Care. 2012;27:522.e11-7.
61. Sarti A, De Gaudio AR, Messineo A, Cuttini M, Ventura A. Glomerular permeability after surgical trauma in children: relationship between microalbuminuria and surgical stress score. Crit Care Med. 2001;29:1626-9.
62. Pallister I, Dent C, Wise CC, Alpar EK, Gosling P. Early post-traumatic acute respiratory distress syndrome and albumin excretion rate: a prospective evaluation of a 'point-of care' predictive test. Injury. 2001;32:177-81.
63. Gosling P, Brudney S, McGrath L, Riseboro S, Manji M. Mortality prediction at admission to intensive care: a comparison of microalbuminuria with acute physiology scores after 24 hours. Crit Care Med. 2003;31:98-103.
64. Thorevska N, Sabahi R, Upadya A, Manthous C, Amoateng-Adjepong Y. Microalbuminuria in critically ill medical patients: prevalence, predictors, and prognostic significance. Crit Care Med. 2003;31:1075-81.
65. Honarmand A, Safavi M, Baghery K, Momayezi A. The association of microalbuminuria and duration of mechanical ventilation in critically ill trauma patients. Ulus Travma Acil Cerrahi Derg. 2009;15:12-8.
66. Basu S, Bhattacharya M, Chatterjee TK, Chaudhuri S, Todi SK, Majumdar A. Microalbuminuria: a novel biomarker of sepsis. Indian J Crit Care Med. 2010;14:22-8.
67. Kranidioti H, Orfanos SE, Vaki I, Kotanidou A, Raftogiannis M, Dimopoulou I, et al. Angiopoietin-2 is increased in septic shock: evidence for the existence of a circulating factor stimulating its release from human monocytes. Immunol Lett. 2009;125:65-71.
68. Xing K, Murthy S, Liles WC, Singh JM. Clinical utility of biomarkers of endothelial activation in sepsis - a systematic review. Crit Care. 2012;16:R7.
69. Siner JM, Bhandari V, Engle KM, Elias JA, Siegel MD. Elevated serum angiopoietin 2 levels are associated with increased mortality in sepsis. Shock. 2009;31:348-53.
70. Annane D. Corticosteroids for severe sepsis: an evidence-based guide for physicians. Ann Intensive Care. 2011;1:7.
71. Moran JL, Graham PL, RockliffS, Bersten AD. Updating the evidence for the role of corticosteroids in severe sepsis and septic shock: a Bayesian meta-analytic perspective. Crit Care. 2010;14:R134.
72. Marechal X, Favory R, Joulin O, Montaigne D, Hassoun S, Decoster B, et al. Endothelial glycocalyx damage during endotoxemia coincides with microcirculatory dysfunction and vascular oxidative stress. Shock. 2008;29:572-6.
73. Nieuwdorp M, van Haeften TW, Gouverneur MC, Mooij HL, van Lieshout MH, Levi M, et al. Loss of endothelial glycocalyx during acute hyperglycemia coincides with endothelial dysfunction and coagulation activation in vivo. Diabetes. 2006;55:480-6.
74. Eskens BJ, Zuurbier CJ, van Haare J, Vink H, van Teeffelen JW. Effects of two weeks of metformin treatment on whole-body glycocalyx barrier properties in db/db mice. Cardiovasc Diabetol. 2013;12:175.