The Endothelial Glycocalyx and Organ Preservation-From Physiology to Possible Clinical Implications for Solid Organ Transplantation

Simon Mathis, Gabriel Putzer, Stefan Schneeberger, Judith Martini, Simon Mathis, Gabriel Putzer, Stefan Schneeberger, Judith Martini

Abstract

The endothelial glycocalyx is a thin layer consisting of proteoglycans, glycoproteins and glycosaminoglycans that lines the luminal side of vascular endothelial cells. It acts as a barrier and contributes to the maintenance of vascular homeostasis and microperfusion. During solid organ transplantation, the endothelial glycocalyx of the graft is damaged as part of Ischemia Reperfusion Injury (IRI), which is associated with impaired organ function. Although several substances are known to mitigate glycocalyx damage, it has not been possible to use these substances during graft storage on ice. Normothermic machine perfusion (NMP) emerges as an alternative technology for organ preservation and allows for organ evaluation, but also offers the possibility to treat and thus improve organ quality during storage. This review highlights the current knowledge on glycocalyx injury during organ transplantation, presents ways to protect the endothelial glycocalyx and discusses potential glycocalyx protection strategies during normothermic machine perfusion.

Keywords: glycocalyx; heparan sulfate; normothermic machine perfusion; solid organ transplantation; static cold storage; syndecan-1.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Real time live confocal visualization of the glycocalyx (in red via wheat germ agglutinin) and endothelial cell nuclei (in blue via HOECHST stain). Porcine blood vessel, 40× water immersion objective.
Figure 2
Figure 2
Glycocalyx-protective mechanisms.

References

    1. Ammirati E., Oliva F., Cannata A., Contri R., Colombo T., Martinelli L., Frigerio M. Current indications for heart transplantation and left ventricular assist device: A practical point of view. Eur. J. Intern. Med. 2014;25:422–429. doi: 10.1016/j.ejim.2014.02.006.
    1. Weill D., Benden C., Corris P.A., Dark J.H., Davis R.D., Keshavjee S., Lederer D.J., Mulligan M.J., Patterson G.A., Singer L.G., et al. A consensus document for the selection of lung transplant candidates: 2014—An update from the Pulmonary Transplantation Council of the International Society for Heart and Lung Transplantation. J. Heart Lung Transplant. 2015;34:1–15. doi: 10.1016/j.healun.2014.06.014.
    1. O’Leary J.G., Lepe R., Davis G.L. Indications for liver transplantation. Gastroenterology. 2008;134:1764–1776. doi: 10.1053/j.gastro.2008.02.028.
    1. Levin A., Hemmelgarn B., Culleton B., Tobe S., McFarlane P., Ruzicka M., Burns K., Manns B., White C., Madore F., et al. Guidelines for the management of chronic kidney disease. CMAJ. 2008;179:1154–1162. doi: 10.1503/cmaj.080351.
    1. Vodkin I., Kuo A. Extended Criteria Donors in Liver Transplantation. Clin. Liver Dis. 2017;21:289–301. doi: 10.1016/j.cld.2016.12.004.
    1. Botha P. Extended donor criteria in lung transplantation. Curr. Opin. Organ. Transplant. 2009;14:206–210. doi: 10.1097/MOT.0b013e328326c834.
    1. Kalogeris T., Baines C.P., Krenz M., Korthuis R.J. Ischemia/Reperfusion. Compr. Physiol. 2016;7:113–170. doi: 10.1002/cphy.c160006.
    1. Stahl J.E., Kreke J.E., Malek F.A., Schaefer A.J., Vacanti J. Consequences of cold-ischemia time on primary nonfunction and patient and graft survival in liver transplantation: A meta-analysis. PLoS ONE. 2008;3:e2468. doi: 10.1371/journal.pone.0002468.
    1. Shah R.J., Diamond J.M. Primary Graft Dysfunction (PGD) Following Lung Transplantation. Semin. Respir. Crit. Care Med. 2018;39:148–154. doi: 10.1055/s-0037-1615797.
    1. Luft J.H. Fine structures of capillary and endocapillary layer as revealed by ruthenium red. Fed. Proc. 1966;25:1773–1783.
    1. Radeva M.Y., Waschke J. Mind the gap: Mechanisms regulating the endothelial barrier. Acta Physiol. 2018;222 doi: 10.1111/apha.12860.
    1. Lipowsky H.H. Role of the Glycocalyx as a Barrier to Leukocyte-Endothelium Adhesion. Adv. Exp. Med. Biol. 2018;1097:51–68. doi: 10.1007/978-3-319-96445-4_3.
    1. Ostrowski S.R., Johansson P.I. Endothelial glycocalyx degradation induces endogenous heparinization in patients with severe injury and early traumatic coagulopathy. J. Trauma Acute Care Surg. 2012;73:60–66. doi: 10.1097/TA.0b013e31825b5c10.
    1. Tarbell J.M., Pahakis M.Y. Mechanotransduction and the glycocalyx. J. Intern. Med. 2006;259:339–350. doi: 10.1111/j.1365-2796.2006.01620.x.
    1. Yu H., Kalogeris T., Korthuis R.J. Reactive species-induced microvascular dysfunction in ischemia/reperfusion. Free Radic. Biol. Med. 2019;135:182–197. doi: 10.1016/j.freeradbiomed.2019.02.031.
    1. Mulivor A.W., Lipowsky H.H. Inflammation- and ischemia-induced shedding of venular glycocalyx. Am. J. Physiol. Heart Circ. Physiol. 2004;286:H1672–H1680. doi: 10.1152/ajpheart.00832.2003.
    1. Jackson-Weaver O., Friedman J.K., Rodriguez L.A., Hoof M.A., Drury R.H., Packer J.T., Smith A., Guidry C., Duchesne J.C. Hypoxia/reoxygenation decreases endothelial glycocalyx via reactive oxygen species and calcium signaling in a cellular model for shock. J. Trauma Acute Care Surg. 2019;87:1070–1076. doi: 10.1097/TA.0000000000002427.
    1. Frydland M., Ostrowski S.R., Møller J.E., Hadziselimovic E., Holmvang L., Ravn H.B., Jensen L.O., Pettersson A.S., Kjaergaard J., Lindholm M.G., et al. Plasma Concentration of Biomarkers Reflecting Endothelial Cell- and Glycocalyx Damage are Increased in Patients with Suspected ST-Elevation Myocardial Infarction Complicated by Cardiogenic Shock. Shock. 2018;50:538–544. doi: 10.1097/SHK.0000000000001123.
    1. DellaValle B., Hasseldam H., Johansen F.F., Iversen H.K., Rungby J., Hempel C. Multiple Soluble Components of the Glycocalyx Are Increased in Patient Plasma After Ischemic Stroke. Stroke. 2019;50:2948–2951. doi: 10.1161/STROKEAHA.119.025953.
    1. Rahbar E., Cardenas J.C., Baimukanova G., Usadi B., Bruhn R., Pati S., Ostrowski S.R., Johansson P.I., Holcomb J.B., Wade C.E. Endothelial glycocalyx shedding and vascular permeability in severely injured trauma patients. J. Transl. Med. 2015;13:117. doi: 10.1186/s12967-015-0481-5.
    1. Schiefer J., Lebherz-Eichinger D., Erdoes G., Berlakovich G., Bacher A., Krenn C.G., Faybik P. Alterations of Endothelial Glycocalyx During Orthotopic Liver Transplantation in Patients with End-Stage Liver Disease. Transplantation. 2015;99:2118–2123. doi: 10.1097/TP.0000000000000680.
    1. Becker B.F., Chappell D., Bruegger D., Annecke T., Jacob M. Therapeutic strategies targeting the endothelial glycocalyx: Acute deficits, but great potential. Cardiovasc. Res. 2010;87:300–310. doi: 10.1093/cvr/cvq137.
    1. Song J.W., Zullo J.A., Liveris D., Dragovich M., Zhang X.F., Goligorsky M.S. Therapeutic Restoration of Endothelial Glycocalyx in Sepsis. J. Pharmacol. Exp. Ther. 2017;361:115–121. doi: 10.1124/jpet.116.239509.
    1. Monbaliu D., Brassil J. Machine perfusion of the liver: Past, present and future. Curr. Opin. Organ. Transplant. 2010;15:160–166. doi: 10.1097/MOT.0b013e328337342b.
    1. Danielli J.F. Capillary permeability and oedema in the perfused frog. J. Physiol. 1940;98:109–129. doi: 10.1113/jphysiol.1940.sp003837.
    1. Pries A.R., Secomb T.W., Gaehtgens P. The endothelial surface layer. Pflugers Arch. 2000;440:653–666. doi: 10.1007/s004240000307.
    1. Weinbaum S., Tarbell J.M., Damiano E.R. The structure and function of the endothelial glycocalyx layer. Annu. Rev. Biomed. Eng. 2007;9:121–167. doi: 10.1146/annurev.bioeng.9.060906.151959.
    1. Schnitzer J.E., Carley W.W., Palade G.E. Specific albumin binding to microvascular endothelium in culture. Am. J. Physiol. 1988;254:H425–H437. doi: 10.1152/ajpheart.1988.254.3.H425.
    1. Schnitzer J.E., Pinney E. Quantitation of specific binding of orosomucoid to cultured microvascular endothelium: Role in capillary permeability. Am. J. Physiol. 1992;263:H48–H55. doi: 10.1152/ajpheart.1992.263.1.H48.
    1. Pries A.R., Kuebler W.M. Normal endothelium. Handb. Exp. Pharmacol. 2006:1–40. doi: 10.1007/3-540-32967-6_1.
    1. Rehm M., Bruegger D., Christ F., Conzen P., Thiel M., Jacob M., Chappell D., Stoeckelhuber M., Welsch U., Reichart B., et al. Shedding of the endothelial glycocalyx in patients undergoing major vascular surgery with global and regional ischemia. Circulation. 2007;116:1896–1906. doi: 10.1161/CIRCULATIONAHA.106.684852.
    1. Jung C., Fuernau G., Muench P., Desch S., Eitel I., Schuler G., Adams V., Figulla H.R., Thiele H. Impairment of the endothelial glycocalyx in cardiogenic shock and its prognostic relevance. Shock. 2015;43:450–455. doi: 10.1097/SHK.0000000000000329.
    1. Vink H., Duling B.R. Identification of distinct luminal domains for macromolecules, erythrocytes, and leukocytes within mammalian capillaries. Circ. Res. 1996;79:581–589. doi: 10.1161/01.RES.79.3.581.
    1. Klitzman B., Duling B.R. Microvascular hematocrit and red cell flow in resting and contracting striated muscle. Am. J. Physiol. 1979;237:H481–H490. doi: 10.1152/ajpheart.1979.237.4.H481.
    1. Pries A.R., Secomb T.W., Gessner T., Sperandio M.B., Gross J.F., Gaehtgens P. Resistance to blood flow in microvessels in vivo. Circ. Res. 1994;75:904–915. doi: 10.1161/01.RES.75.5.904.
    1. Fåhraeus R. The suspension stability of the blood. Physiol. Rev. 1929;9:241–274. doi: 10.1152/physrev.1929.9.2.241.
    1. Desjardins C., Duling B.R. Heparinase treatment suggests a role for the endothelial cell glycocalyx in regulation of capillary hematocrit. Am. J. Physiol. 1990;258:H647–H654. doi: 10.1152/ajpheart.1990.258.3.H647.
    1. Adamson R.H., Lenz J.F., Zhang X., Adamson G.N., Weinbaum S., Curry F.E. Oncotic pressures opposing filtration across non-fenestrated rat microvessels. J. Physiol. 2004;557:889–907. doi: 10.1113/jphysiol.2003.058255.
    1. Adamson R.H. Permeability of frog mesenteric capillaries after partial pronase digestion of the endothelial glycocalyx. J. Physiol. 1990;428:1–13. doi: 10.1113/jphysiol.1990.sp018197.
    1. Jeansson M., Haraldsson B. Morphological and functional evidence for an important role of the endothelial cell glycocalyx in the glomerular barrier. Am. J. Physiol. Renal Physiol. 2006;290:F111–F116. doi: 10.1152/ajprenal.00173.2005.
    1. Van den Berg B.M., Vink H., Spaan J.A. The endothelial glycocalyx protects against myocardial edema. Circ. Res. 2003;92:592–594. doi: 10.1161/01.RES.0000065917.53950.75.
    1. Vink H., Constantinescu A.A., Spaan J.A. Oxidized lipoproteins degrade the endothelial surface layer: Implications for platelet-endothelial cell adhesion. Circulation. 2000;101:1500–1502. doi: 10.1161/01.CIR.101.13.1500.
    1. Lipowsky H.H., Sah R., Lescanic A. Relative roles of doxycycline and cation chelation in endothelial glycan shedding and adhesion of leukocytes. Am. J. Physiol. Heart Circ. Physiol. 2011;300:H415–H422. doi: 10.1152/ajpheart.00923.2010.
    1. Lee D.H., Dane M.J., van den Berg B.M., Boels M.G., van Teeffelen J.W., de Mutsert R., den Heijer M., Rosendaal F.R., van der Vlag J., van Zonneveld A.J., et al. Deeper penetration of erythrocytes into the endothelial glycocalyx is associated with impaired microvascular perfusion. PLoS ONE. 2014;9:e96477. doi: 10.1371/journal.pone.0096477.
    1. Rubanyi G.M., Romero J.C., Vanhoutte P.M. Flow-induced release of endothelium-derived relaxing factor. Am. J. Physiol. 1986;250:H1145–H1149. doi: 10.1152/ajpheart.1986.250.6.H1145.
    1. Weinbaum S., Zhang X., Han Y., Vink H., Cowin S.C. Mechanotransduction and flow across the endothelial glycocalyx. Proc. Natl. Acad. Sci. USA. 2003;100:7988–7995. doi: 10.1073/pnas.1332808100.
    1. Florian J.A., Kosky J.R., Ainslie K., Pang Z., Dull R.O., Tarbell J.M. Heparan sulfate proteoglycan is a mechanosensor on endothelial cells. Circ. Res. 2003;93:e136–e142. doi: 10.1161/01.RES.0000101744.47866.D5.
    1. Mochizuki S., Vink H., Hiramatsu O., Kajita T., Shigeto F., Spaan J.A., Kajiya F. Role of hyaluronic acid glycosaminoglycans in shear-induced endothelium-derived nitric oxide release. Am. J. Physiol. Heart Circ. Physiol. 2003;285:H722–H726. doi: 10.1152/ajpheart.00691.2002.
    1. Gandhi N.S., Mancera R.L. The structure of glycosaminoglycans and their interactions with proteins. Chem. Biol. Drug Des. 2008;72:455–482. doi: 10.1111/j.1747-0285.2008.00741.x.
    1. Fromm J.R., Hileman R.E., Weiler J.M., Linhardt R.J. Interaction of fibroblast growth factor-1 and related peptides with heparan sulfate and its oligosaccharides. Arch. Biochem. Biophys. 1997;346:252–262. doi: 10.1006/abbi.1997.0299.
    1. Shimada K., Kobayashi M., Kimura S., Nishinaga M., Takeuchi K., Ozawa T. Anticoagulant heparin-like glycosaminoglycans on endothelial cell surface. Jpn. Circ. J. 1991;55:1016–1021. doi: 10.1253/jcj.55.1016.
    1. Ikeda M., Matsumoto H., Ogura H., Hirose T., Shimizu K., Yamamoto K., Maruyama I., Shimazu T. Circulating syndecan-1 predicts the development of disseminated intravascular coagulation in patients with sepsis. J. Crit. Care. 2018;43:48–53. doi: 10.1016/j.jcrc.2017.07.049.
    1. Wada H., Thachil J., Di Nisio M., Mathew P., Kurosawa S., Gando S., Kim H.K., Nielsen J.D., Dempfle C.E., Levi M., et al. Guidance for diagnosis and treatment of DIC from harmonization of the recommendations from three guidelines. J. Thromb. Haemost. 2013 doi: 10.1111/jth.12155.
    1. Kettner S.C., Gonano C., Seebach F., Sitzwohl C., Acimovic S., Stark J., Schellongowski A., Blaicher A., Felfernig M., Zimpfer M. Endogenous heparin-like substances significantly impair coagulation in patients undergoing orthotopic liver transplantation. Anesth. Analg. 1998;86:691–695. doi: 10.1213/00000539-199804000-00002.
    1. Senzolo M., Cholongitas E., Thalheimer U., Riddell A., Agarwal S., Mallett S., Ferronato C., Burroughs A.K. Heparin-like effect in liver disease and liver transplantation. Clin. Liver Dis. 2009;13:43–53. doi: 10.1016/j.cld.2008.09.004.
    1. Liu G., Zhang H., Hao F., Hao J., Pan L., Zhao Q., Wo J. Clusterin Reduces Cold Ischemia-Reperfusion Injury in Heart Transplantation Through Regulation of NF-kB Signaling and Bax/Bcl-xL Expression. Cell Physiol. Biochem. 2018;45:1003–1012. doi: 10.1159/000487295.
    1. Saidi R.F., Kenari S.K. Liver ischemia/reperfusion injury: An overview. J. Investig. Surg. 2014;27:366–379. doi: 10.3109/08941939.2014.932473.
    1. Nieuwenhuijs-Moeke G.J., Pischke S.E., Berger S.P., Sanders J.S.F., Pol R.A., Struys M.M.R.F., Ploeg R.J., Leuvenink H.G.D. Ischemia and Reperfusion Injury in Kidney Transplantation: Relevant Mechanisms in Injury and Repair. J. Clin. Med. 2020;9:253. doi: 10.3390/jcm9010253.
    1. Chen F., Date H. Update on ischemia-reperfusion injury in lung transplantation. Curr. Opin. Organ. Transplant. 2015;20:515–520. doi: 10.1097/MOT.0000000000000234.
    1. Passov A., Schramko A., Mäkisalo H., Nordin A., Andersson S., Pesonen E., Ilmakunnas M. Graft glycocalyx degradation in human liver transplantation. PLoS ONE. 2019;14:e0221010. doi: 10.1371/journal.pone.0221010.
    1. Sladden T.M., Yerkovich S., Grant M., Zhang F., Liu X., Trotter M., Hopkins P., Linhardt R.J., Chambers D.C. Endothelial Glycocalyx Shedding Predicts Donor Organ Acceptability and Is Associated with Primary Graft Dysfunction in Lung Transplant Recipients. Transplantation. 2019;103:1277–1285. doi: 10.1097/TP.0000000000002539.
    1. Schiefer J., Faybik P., Koch S., Tudor B., Kollmann D., Kuessel L., Krenn C.G., Berlakovich G., Baron D.M., Baron-Stefaniak J. Glycocalyx Damage Within Human Liver Grafts Correlates with Graft Injury and Postoperative Graft Function After Orthotopic Liver Transplantation. Transplantation. 2020;104:72–78. doi: 10.1097/TP.0000000000002838.
    1. Snoeijs M.G., Vink H., Voesten N., Christiaans M.H., Daemen J.W., Peppelenbosch A.G., Tordoir J.H., Peutz-Kootstra C.J., Buurman W.A., Schurink G.W., et al. Acute ischemic injury to the renal microvasculature in human kidney transplantation. Am. J. Physiol. Renal Physiol. 2010;299:F1134–F1140. doi: 10.1152/ajprenal.00158.2010.
    1. Brettner F., Chappell D., Nebelsiek T., Hauer D., Schelling G., Becker B.F., Rehm M., Weis F. Preinterventional hydrocortisone sustains the endothelial glycocalyx in cardiac surgery. Clin. Hemorheol. Microcirc. 2019;71:59–70. doi: 10.3233/CH-180384.
    1. Belavić M., Sotošek Tokmadžić V., Fišić E., Brozović Krijan A., Strikić N., Lončarić Katušin M., Žunić J. The effect of various doses of infusion solutions on the endothelial glycocalyx layer in laparoscopic cholecystectomy patients. Minerva Anestesiol. 2018;84:1032–1043. doi: 10.23736/S0375-9393.18.12150-X.
    1. Berg S., Engman A., Hesselvik J.F., Laurent T.C. Crystalloid infusion increases plasma hyaluronan. Crit. Care Med. 1994;22:1563–1567. doi: 10.1097/00003246-199410000-00010.
    1. Chappell D., Bruegger D., Potzel J., Jacob M., Brettner F., Vogeser M., Conzen P., Becker B.F., Rehm M. Hypervolemia increases release of atrial natriuretic peptide and shedding of the endothelial glycocalyx. Crit. Care. 2014;18:538. doi: 10.1186/s13054-014-0538-5.
    1. Potter L.R., Yoder A.R., Flora D.R., Antos L.K., Dickey D.M. Natriuretic peptides: Their structures, receptors, physiologic functions and therapeutic applications. Handb. Exp. Pharmacol. 2009:341–366. doi: 10.1007/978-3-540-68964-5_15.
    1. Bruegger D., Jacob M., Rehm M., Loetsch M., Welsch U., Conzen P., Becker B.F. 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. doi: 10.1152/ajpheart.00218.2005.
    1. Knotzer H., Hasibeder W.R. In search of the optimal perfusion pressure--does the microcirculation give us the answer? Crit. Care Med. 2009;37:2120–2121. doi: 10.1097/CCM.0b013e3181a5c2b8.
    1. Brunkhorst F.M., Engel C., Bloos F., Meier-Hellmann A., Ragaller M., Weiler N., Moerer O., Gruendling M., Oppert M., Grond S., et al. Intensive insulin therapy and pentastarch resuscitation in severe sepsis. N. Engl. J. Med. 2008;358:125–139. doi: 10.1056/NEJMoa070716.
    1. Guidet B., Martinet O., Boulain T., Philippart F., Poussel J.F., Maizel J., Forceville X., Feissel M., Hasselmann M., Heininger A., 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. doi: 10.1186/11358.
    1. Patel A., Pieper K., Myburgh J.A., Perkovic V., Finfer S., Yang Q., Li Q., Billot L. Reanalysis of the Crystalloid versus Hydroxyethyl Starch Trial (CHEST) N. Engl. J. Med. 2017;377:298–300. doi: 10.1056/NEJMc1703337.
    1. Roberts I., Shakur H., Bellomo R., Bion J., Finfer S., Hunt B., Myburgh J., Perner A., Reinhart K. Hydroxyethyl starch solutions and patient harm. Lancet. 2018;391:736. doi: 10.1016/S0140-6736(18)30255-1.
    1. Raghunathan K., Murray P.T., Beattie W.S., Lobo D.N., Myburgh J., Sladen R., Kellum J.A., Mythen M.G., Shaw A.D., Group A.X.I. Choice of fluid in acute illness: What should be given? An international consensus. Br. J. Anaesth. 2014;113:772–783. doi: 10.1093/bja/aeu301.
    1. Perner A., Haase N., Guttormsen A.B., Tenhunen J., Klemenzson G., Åneman A., Madsen K.R., Møller M.H., Elkjær J.M., Poulsen L.M., et al. Hydroxyethyl starch 130/0.42 versus Ringer’s acetate in severe sepsis. N. Engl. J. Med. 2012;367:124–134. doi: 10.1056/NEJMoa1204242.
    1. Torres Filho I.P., Torres L.N., Salgado C., Dubick M.A. 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. doi: 10.1152/ajpheart.00006.2016.
    1. Jacob M., Bruegger D., Rehm M., Welsch U., Conzen P., Becker B.F. Contrasting effects of colloid and crystalloid resuscitation fluids on cardiac vascular permeability. Anesthesiology. 2006;104:1223–1231. doi: 10.1097/00000542-200606000-00018.
    1. Han S., Sangwook Ko J., Jin S.M., Man Kim J., Choi S.J., Joh J.W., Hoon Chung Y., Lee S.K., Gwak M.S., Kim G. Glycemic responses to intermittent hepatic inflow occlusion in living liver donors. Liver Transpl. 2015;21:180–186. doi: 10.1002/lt.24029.
    1. Fliser D., Pacini G., Engelleiter R., Kautzky-Willer A., Prager R., Franek E., Ritz E. Insulin resistance and hyperinsulinemia are already present in patients with incipient renal disease. Kidney Int. 1998;53:1343–1347. doi: 10.1046/j.1523-1755.1998.00898.x.
    1. Kwon S., Hermayer K.L., Hermayer K. Glucocorticoid-induced hyperglycemia. Am. J. Med. Sci. 2013;345:274–277. doi: 10.1097/MAJ.0b013e31828a6a01.
    1. Barth E., Albuszies G., Baumgart K., Matejovic M., Wachter U., Vogt J., Radermacher P., Calzia E. Glucose metabolism and catecholamines. Crit. Care Med. 2007;35:S508–S518. doi: 10.1097/01.CCM.0000278047.06965.20.
    1. Dungan K.M., Braithwaite S.S., Preiser J.C. Stress hyperglycaemia. Lancet. 2009;373:1798–1807. doi: 10.1016/S0140-6736(09)60553-5.
    1. Pillinger N.L., Kam P. Endothelial glycocalyx: Basic science and clinical implications. Anaesth. Intensive Care. 2017;45:295–307. doi: 10.1177/0310057X1704500305.
    1. Nieuwdorp M., van Haeften T.W., Gouverneur M.C., Mooij H.L., van Lieshout M.H., Levi M., Meijers J.C., Holleman F., Hoekstra J.B., Vink H., et al. Loss of endothelial glycocalyx during acute hyperglycemia coincides with endothelial dysfunction and coagulation activation in vivo. Diabetes. 2006;55:480–486. doi: 10.2337/diabetes.55.02.06.db05-1103.
    1. Lopez-Quintero S.V., Cancel L.M., Pierides A., Antonetti D., Spray D.C., Tarbell J.M. High glucose attenuates shear-induced changes in endothelial hydraulic conductivity by degrading the glycocalyx. PLoS ONE. 2013;8:e78954. doi: 10.1371/journal.pone.0078954.
    1. Singh A., Fridén V., Dasgupta I., Foster R.R., Welsh G.I., Tooke J.E., Haraldsson B., Mathieson P.W., Satchell S.C. High glucose causes dysfunction of the human glomerular endothelial glycocalyx. Am. J. Physiol. Renal Physiol. 2011;300:F40–F48. doi: 10.1152/ajprenal.00103.2010.
    1. Zuurbier C.J., 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. 2005;99:1471–1476. doi: 10.1152/japplphysiol.00436.2005.
    1. Astapenko D., Pouska J., Benes J., Skulec R., Lehmann C., Vink H., Cerny V. Neuraxial anesthesia is less harmful to the endothelial glycocalyx during elective joint surgery compared to general anesthesia. Clin. Hemorheol. Microcirc. 2019;72:11–21. doi: 10.3233/CH-180428.
    1. Li J., Yuan T., Zhao X., Lv G.Y., Liu H.Q. Protective effects of sevoflurane in hepatic ischemia-reperfusion injury. Int. J. Immunopathol. Pharmacol. 2016;29:300–307. doi: 10.1177/0394632016638346.
    1. Casanova J., Simon C., Vara E., Sanchez G., Rancan L., Abubakra S., Calvo A., Gonzalez F.J., Garutti I. Sevoflurane anesthetic preconditioning protects the lung endothelial glycocalyx from ischemia reperfusion injury in an experimental lung autotransplant model. J. Anesth. 2016;30:755–762. doi: 10.1007/s00540-016-2195-0.
    1. Annecke T., Chappell D., Chen C., Jacob M., Welsch U., Sommerhoff C.P., Rehm M., Conzen P.F., Becker B.F. Sevoflurane preserves the endothelial glycocalyx against ischaemia-reperfusion injury. Br. J. Anaesth. 2010;104:414–421. doi: 10.1093/bja/aeq019.
    1. Chen C., Chappell D., Annecke T., Conzen P., Jacob M., Welsch U., Zwissler B., Becker B.F. Sevoflurane mitigates shedding of hyaluronan from the coronary endothelium, also during ischemia/reperfusion: An ex vivo animal study. Hypoxia. 2016;4:81–90. doi: 10.2147/HP.S98660.
    1. Kim H.J., Kim E., Baek S.H., Kim H.Y., Kim J.Y., Park J., Choi E.J. Sevoflurane did not show better protective effect on endothelial glycocalyx layer compared to propofol during lung resection surgery with one lung ventilation. J. Thorac. Dis. 2018;10:1468–1475. doi: 10.21037/jtd.2018.03.44.
    1. McAnulty J.F. Hypothermic organ preservation by static storage methods: Current status and a view to the future. Cryobiology. 2010;60:S13–S19. doi: 10.1016/j.cryobiol.2009.06.004.
    1. Southard J.H., Belzer F.O. Organ preservation. Annu. Rev. Med. 1995;46:235–247. doi: 10.1146/annurev.med.46.1.235.
    1. Ardehali A., Esmailian F., Deng M., Soltesz E., Hsich E., Naka Y., Mancini D., Camacho M., Zucker M., Leprince P., et al. Ex-vivo perfusion of donor hearts for human heart transplantation (PROCEED II): A prospective, open-label, multicentre, randomised non-inferiority trial. Lancet. 2015;385:2577–2584. doi: 10.1016/S0140-6736(15)60261-6.
    1. Sanchez P.G., Mackowick K.M., Kon Z.N. Current state of ex-vivo lung perfusion. Curr. Opin. Organ. Transplant. 2016;21:258–266. doi: 10.1097/MOT.0000000000000310.
    1. Ravikumar R., Jassem W., Mergental H., Heaton N., Mirza D., Perera M.T., Quaglia A., Holroyd D., Vogel T., Coussios C.C., et al. Liver Transplantation After Ex Vivo Normothermic Machine Preservation: A Phase 1 (First-in-Man) Clinical Trial. Am. J. Transplant. 2016;16:1779–1787. doi: 10.1111/ajt.13708.
    1. Hosgood S.A., Nicholson M.L. First in man renal transplantation after ex vivo normothermic perfusion. Transplantation. 2011;92:735–738. doi: 10.1097/TP.0b013e31822d4e04.
    1. Weissenbacher A., Hunter J. Normothermic machine perfusion of the kidney. Curr. Opin. Organ. Transplant. 2017;22:571–576. doi: 10.1097/MOT.0000000000000470.
    1. Nasralla D., Coussios C.C., Mergental H., Akhtar M.Z., Butler A.J., Ceresa C.D.L., Chiocchia V., Dutton S.J., García-Valdecasas J.C., Heaton N., et al. A randomized trial of normothermic preservation in liver transplantation. Nature. 2018;557:50–56. doi: 10.1038/s41586-018-0047-9.
    1. Cardini B., Oberhuber R., Fodor M., Hautz T., Margreiter C., Resch T., Scheidl S., Maglione M., Bösmüller C., Mair H., et al. Clinical Implementation of Prolonged Liver Preservation and Monitoring Through Normothermic Machine Perfusion in Liver Transplantation. Transplantation. 2020;104:1917–1928. doi: 10.1097/TP.0000000000003296.
    1. Watson C.J.E., Jochmans I. From “Gut Feeling” to Objectivity: Machine Preservation of the Liver as a Tool to Assess Organ Viability. Curr. Transplant. Rep. 2018;5:72–81. doi: 10.1007/s40472-018-0178-9.
    1. Dengu F., Abbas S.H., Ebeling G., Nasralla D. Normothermic Machine Perfusion (NMP) of the Liver as a Platform for Therapeutic Interventions during Ex-Vivo Liver Preservation: A Review. J. Clin. Med. 2020;9:1046. doi: 10.3390/jcm9041046.
    1. Li X., Zhang J.F., Lu M.Q., Yang Y., Xu C., Li H., Wang G.S., Cai C.J., Chen G.H. Alleviation of ischemia-reperfusion injury in rat liver transplantation by induction of small interference RNA targeting Fas. Langenbecks Arch. Surg. 2007;392:345–351. doi: 10.1007/s00423-006-0142-5.
    1. Rigo F., De Stefano N., Navarro-Tableros V., David E., Rizza G., Catalano G., Gilbo N., Maione F., Gonella F., Roggio D., et al. Extracellular Vesicles from Human Liver Stem Cells Reduce Injury in an Ex Vivo Normothermic Hypoxic Rat Liver Perfusion Model. Transplantation. 2018;102:e205–e210. doi: 10.1097/TP.0000000000002123.
    1. Goldaracena N., Spetzler V.N., Echeverri J., Kaths J.M., Cherepanov V., Persson R., Hodges M.R., Janssen H.L., Selzner N., Grant D.R., et al. Inducing Hepatitis C Virus Resistance After Pig Liver Transplantation-A Proof of Concept of Liver Graft Modification Using Warm Ex Vivo Perfusion. Am. J. Transplant. 2017;17:970–978. doi: 10.1111/ajt.14100.
    1. Chappell D., Hofmann-Kiefer K., Jacob M., Rehm M., Briegel J., Welsch U., Conzen P., Becker B.F. TNF-alpha induced shedding of the endothelial glycocalyx is prevented by hydrocortisone and antithrombin. Basic Res. Cardiol. 2009;104:78–89. doi: 10.1007/s00395-008-0749-5.
    1. Jacob M., Paul O., Mehringer L., Chappell D., Rehm M., Welsch U., Kaczmarek I., Conzen P., Becker B.F. Albumin augmentation improves condition of guinea pig hearts after 4 hr of cold ischemia. Transplantation. 2009;87:956–965. doi: 10.1097/TP.0b013e31819c83b5.
    1. Talha S., Charloux A., Piquard F., Geny B. Brain natriuretic peptide and right heart dysfunction after heart transplantation. Clin. Transplant. 2017;31 doi: 10.1111/ctr.12969.
    1. Xu J., Kim G.M., Ahmed S.H., Yan P., Xu X.M., Hsu C.Y. Glucocorticoid receptor-mediated suppression of activator protein-1 activation and matrix metalloproteinase expression after spinal cord injury. J. Neurosci. 2001;21:92–97. doi: 10.1523/JNEUROSCI.21-01-00092.2001.
    1. Chappell D., Jacob M., Hofmann-Kiefer K., Rehm M., Welsch U., Conzen P., Becker B.F. Antithrombin reduces shedding of the endothelial glycocalyx following ischaemia/reperfusion. Cardiovasc. Res. 2009;83:388–396. doi: 10.1093/cvr/cvp097.
    1. Sanner B.M., Meder U., Zidek W., Tepel M. Effects of glucocorticoids on generation of reactive oxygen species in platelets. Steroids. 2002;67:715–719. doi: 10.1016/S0039-128X(02)00024-7.
    1. Ramnath R., Foster R.R., Qiu Y., Cope G., Butler M.J., Salmon A.H., Mathieson P.W., Coward R.J., Welsh G.I., Satchell S.C. Matrix metalloproteinase 9-mediated shedding of syndecan 4 in response to tumor necrosis factor α: A contributor to endothelial cell glycocalyx dysfunction. FASEB J. 2014;28:4686–4699. doi: 10.1096/fj.14-252221.
    1. Cui N., Wang H., Long Y., Su L., Liu D. Dexamethasone Suppressed LPS-Induced Matrix Metalloproteinase and Its Effect on Endothelial Glycocalyx Shedding. Mediat. Inflamm. 2015;2015:912726. doi: 10.1155/2015/912726.
    1. Chappell D., Jacob M., Hofmann-Kiefer K., Bruegger D., Rehm M., Conzen P., Welsch U., Becker B.F. Hydrocortisone preserves the vascular barrier by protecting the endothelial glycocalyx. Anesthesiology. 2007;107:776–784. doi: 10.1097/01.anes.0000286984.39328.96.
    1. Masola V., Zaza G., Onisto M., Lupo A., Gambaro G. Glycosaminoglycans, proteoglycans and sulodexide and the endothelium: Biological roles and pharmacological effects. Int. Angiol. 2014;33:243–254.
    1. Veraldi N., Guerrini M., Urso E., Risi G., Bertini S., Bensi D., Bisio A. Fine structural characterization of sulodexide. J. Pharm. Biomed. Anal. 2018;156:67–79. doi: 10.1016/j.jpba.2018.04.012.
    1. Carroll B.J., Piazza G., Goldhaber S.Z. Sulodexide in venous disease. J. Thromb. Haemost. 2019;17:31–38. doi: 10.1111/jth.14324.
    1. Cosmi B., Cini M., Legnani C., Pancani C., Calanni F., Coccheri S. Additive thrombin inhibition by fast moving heparin and dermatan sulfate explains the anticoagulant effect of sulodexide, a natural mixture of glycosaminoglycans. Thromb. Res. 2003;109:333–339. doi: 10.1016/S0049-3848(03)00246-9.
    1. Coccheri S., Mannello F. Development and use of sulodexide in vascular diseases: Implications for treatment. Drug Des. Dev. Ther. 2013;8:49–65. doi: 10.2147/DDDT.S6762.
    1. Masola V., Onisto M., Zaza G., Lupo A., Gambaro G. A new mechanism of action of sulodexide in diabetic nephropathy: Inhibits heparanase-1 and prevents FGF-2-induced renal epithelial-mesenchymal transition. J. Transl. Med. 2012;10:213. doi: 10.1186/1479-5876-10-213.
    1. Lauver D.A., Booth E.A., White A.J., Poradosu E., Lucchesi B.R. Sulodexide attenuates myocardial ischemia/reperfusion injury and the deposition of C-reactive protein in areas of infarction without affecting hemostasis. J. Pharmacol. Exp. Ther. 2005;312:794–800. doi: 10.1124/jpet.104.075283.
    1. Schmid R.A., Yamashita M., Ando K., Tanaka Y., Cooper J.D., Patterson G.A. Lidocaine reduces reperfusion injury and neutrophil migration in canine lung allografts. Ann. Thorac. Surg. 1996;61:949–955. doi: 10.1016/0003-4975(95)01182-X.
    1. Yanagi H., Sankawa H., Saito H., Iikura Y. Effect of lidocaine on histamine release and Ca2+ mobilization from mast cells and basophils. Acta Anaesthesiol. Scand. 1996;40:1138–1144. doi: 10.1111/j.1399-6576.1996.tb05577.x.
    1. Rancan L., Simón C., Sánchez Pedrosa G., Aymonnier K., Shahani P.M., Casanova J., Muñoz C., Garutti I., Vara E. Glycocalyx Degradation after Pulmonary Transplantation Surgery. Eur. Surg. Res. 2018;59:115–125. doi: 10.1159/000489492.
    1. Rubio-Gayosso I., Platts S.H., Duling B.R. Reactive oxygen species mediate modification of glycocalyx during ischemia-reperfusion injury. Am. J. Physiol. Heart Circ. Physiol. 2006;290:H2247–H2256. doi: 10.1152/ajpheart.00796.2005.
    1. Mensah S.A., Cheng M.J., Homayoni H., Plouffe B.D., Coury A.J., Ebong E.E. Regeneration of glycocalyx by heparan sulfate and sphingosine 1-phosphate restores inter-endothelial communication. PLoS ONE. 2017;12:e0186116. doi: 10.1371/journal.pone.0186116.

Source: PubMed

Sponsorzy i współpracownicy

Warunki medyczne

Interwencje lekowe

3
Subskrybuj