Plasma syndecan-1 and heparan sulfate correlate with microvascular glycocalyx degradation in hemorrhaged rats after different resuscitation fluids

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 310, Issue 11, 2016, Pages H1468-H1478

  Torres Filho, Ivo P ^a   Torres, Luciana N ^a   Salgado, Christi ^a   Dubick, Michael A ^a  

^a US ARMY INSTITUTE OF SURGICAL RESEARCH   (United States)

Author keywords

Glycocalyx; Hemorrhage; Microcirculation; Muscle; Resuscitation; Shock; Syndecan

Indexed keywords

BIOLOGICAL MARKER; HEPARAN SULFATE; PROTEOHEPARAN SULFATE; SYNDECAN 1; DEXTRAN; FLUORESCEIN ISOTHIOCYANATE; FLUORESCEIN ISOTHIOCYANATE DEXTRAN; PLASMA SUBSTITUTE; SDC1 PROTEIN, RAT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLEEDING; BLOOD CHEMISTRY; BLOOD FLOW; BLOOD VESSEL PERMEABILITY; BLOOD VOLUME; CONTROLLED STUDY; CREMASTER MUSCLE; DEGRADATION; ERYTHROCYTE; FLUID RESUSCITATION; GLYCOCALYX; INTRAVITAL MICROSCOPY; MALE; NON INVASIVE PROCEDURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; QUANTITATIVE ANALYSIS; RAT; SHEAR RATE; THICKNESS; VENULE; ABDOMINAL WALL MUSCULATURE; ANALOGS AND DERIVATIVES; ANIMAL; BLOOD; CAPILLARY PERMEABILITY; COMPARATIVE STUDY; DISEASE MODEL; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PROCEDURES; PROTEIN DEGRADATION; RESUSCITATION; SHOCK, HEMORRHAGIC; SPRAGUE DAWLEY RAT; VASCULARIZATION;

ABDOMINAL MUSCLES; ANIMALS; BIOMARKERS; CAPILLARY PERMEABILITY; DEXTRANS; DISEASE MODELS, ANIMAL; FLUORESCEIN-5-ISOTHIOCYANATE; GLYCOCALYX; HEPARITIN SULFATE; MALE; PLASMA SUBSTITUTES; PROTEOLYSIS; RATS, SPRAGUE-DAWLEY; RESUSCITATION; SHOCK, HEMORRHAGIC; SYNDECAN-1; VENULES;

EID: 84983801349     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00006.2016     Document Type: Article

References (67)

1. Aird WC. Endothelium as a therapeutic target in sepsis. Curr Drug Targets 8: 501–507, 2007.
2. Aksu U, Bezemer R, Yavuz B, Kandil A, Demirci C, Ince C. Balanced vs. unbalanced crystalloid resuscitation in a near-fatal model of hemor-rhagic shock and the effects on renal oxygenation, oxidative stress, and inflammation. Resuscitation 83: 767–773, 2012.
3. Alam HB, Rhee P. New developments in fluid resuscitation. Surg Clin North Am 87: 55–72, vi, 2007.
4. Annecke T, Chappell D, Chen C, Jacob M, Welsch U, Sommerhoff CP, Rehm M, Conzen PF, Becker BF. Sevoflurane preserves the endo-thelial glycocalyx against ischaemia-reperfusion injury. Br J Anaesth 104: 414–421, 2010.
5. Annecke T, Fischer J, Hartmann H, Tschoep J, Rehm M, Conzen P, Sommerhoff CP, Becker BF. Shedding of the coronary endothelial glycocalyx: effects of hypoxia/reoxygenation vs. ischaemia/reperfusion. Br J Anaesth 107: 679–686, 2011.
6. Ban K, Peng Z, Pati S, Witkov RB, Park PW, Kozar RA. Plasma-mediated gut protection after hemorrhagic shock is lessened in syndecan-1-/-mice. Shock 44: 452–457, 2015.
7. Becker BF, Fischer J, Hartmann H, Chen CC, Sommerhoff CP, Tschoep J, Conzen PC, Annecke T. Inosine, not adenosine, initiates endothelial glycocalyx degradation in cardiac ischemia and hypoxia. Nucleosides Nucleotides Nucleic Acids 30: 1161–1167, 2011.
8. Berg S, Engman A, Hesselvik JF, Laurent TC. Crystalloid infusion increases plasma hyaluronan. Crit Care Med 22: 1563–1567, 1994.
9. Berg S, Golster M, Lisander B. Albumin extravasation and tissue washout of hyaluronan after plasma volume expansion with crystalloid or hypooncotic colloid solutions. Acta Anaesthesiol Scand 46: 166–172, 2002.
10. Bode L, Salvestrini C, Park PW, Li JP, Esko JD, Yamaguchi Y, Murch S, Freeze HH. Heparan sulfate and syndecan-1 are essential in maintaining murine and human intestinal epithelial barrier function. J Clin Invest 118: 229–238, 2008.
11. Borgman MA, Spinella PC, Perkins JG, Grathwohl KW, Repine T, Beekley AC, Sebesta J, Jenkins D, Wade CE, Holcomb JB. The ratio of blood products transfused affects mortality in patients receiving massive transfusions at a combat support hospital. J Trauma 63: 805–813, 2007.
12. Broekhuizen LN, Mooij HL, Kastelein JJ, Stroes ES, Vink H, Nieu-wdorp M. Endothelial glycocalyx as potential diagnostic and therapeutic target in cardiovascular disease. Curr Opin Lipidol 20: 57–62, 2009.
13. Brookes ZL, Brown NJ, Reilly CS. Response of the rat cremaster microcirculation to hemorrhage in vivo: differential effects of intravenous anesthetic agents. Shock 18: 542–548, 2002.
14. Burke-Gaffney A, Evans TW. Lest we forget the endothelial glycocalyx in sepsis. Crit Care 16: 121, 2012.
15. Chappell D, Jacob M, Hofmann-Kiefer K, Bruegger D, Rehm M, Conzen P, Welsch U, Becker BF. Hydrocortisone preserves the vascular barrier by protecting the endothelial glycocalyx. Anesthesiology 107: 776–784, 2007.
16. 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 83: 388–396, 2009.
17. Chiavarelli R, Macchiarelli G, Familiari G, Chiavarelli M, Macchi-arelli A, Del Basso P, Marino B, Motta PM. Ultrastructural changes of coronary artery endothelium induced by cardioplegic solutions. Thorac Cardiovasc Surg 37: 151–157, 1989.
18. Constantinescu AA, Vink H, Spaan JA. Endothelial cell glycocalyx modulates immobilization of leukocytes at the endothelial surface. Arte-rioscler Thromb Vasc Biol 23: 1541–1547, 2003.
19. Curry FE, Adamson RH. Endothelial glycocalyx: permeability barrier and mechanosensor. Ann Biomed Eng 40: 828–839, 2012.
20. Gao L, Lipowsky HH. Composition of the endothelial glycocalyx and its relation to its thickness and diffusion of small solutes. Microvasc Res 80: 394–401, 2010.
21. Grocott MP, Hamilton MA. Resuscitation fluids. Vox Sang 82: 1–8, 2002.
22. Grundmann S, Fink K, Rabadzhieva L, Bourgeois N, Schwab T, Moser M, Bode C, Busch HJ. Perturbation of the endothelial glycocalyx in post cardiac arrest syndrome. Resuscitation 83: 715–720, 2012.
23. Haywood-Watson RJ, Holcomb JB, Gonzalez EA, Peng Z, Pati S, Park PW, Wang W, Zaske AM, Menge T, Kozar RA. Modulation of syndecan-1 shedding after hemorrhagic shock and resuscitation. PLos One 6: e23530, 2011.
24. Henrich M, Gruss M, Weigand MA. Sepsis-induced degradation of endothelial glycocalix. Sci World J 10: 917–923, 2010.
25. Henry CB, Duling BR. Permeation of the luminal capillary glycocalyx is determined by hyaluronan. Am J Physiol Heart Circ Physiol 277: H508–H514, 1999.
26. Hofmann-Kiefer KF, Knabl J, Martinoff N, Schiessl B, Conzen P, Rehm M, Becker BF, Chappell D. Increased serum concentrations of circulating glycocalyx components in HELLP syndrome compared with healthy pregnancy: an observational study. Reprod Sci 20: 318–325, 2013.
27. Holcomb JB. A novel and potentially unifying mechanism for shock induced early coagulopathy. Ann Surg 254: 201–202, 2011.
28. Holcomb JB, Wade CE, Michalek JE, Chisholm GB, Zarzabal LA, Schreiber MA, Gonzalez EA, Pomper GJ, Perkins JG, Spinella PC, Williams KL, Park MS. Increased plasma and platelet to red blood cell ratios improves outcome in 466 massively transfused civilian trauma patients. Ann Surg 248: 447–458, 2008.
29. Jacob M, Bruegger D, Rehm M, Stoeckelhuber M, Welsch U, Conzen P, Becker BF. The endothelial glycocalyx affords compatibility of Star-ling’s principle and high cardiac interstitial albumin levels. Cardiovasc Res 73: 575–586, 2007.
30. Johansson PI, Stensballe J, Rasmussen LS, Ostrowski SR. A high admission syndecan-1 level, a marker of endothelial glycocalyx degrada-tion, is associated with inflammation, protein C depletion, fibrinolysis, and increased mortality in trauma patients. Ann Surg 254: 194–200, 2011.
31. Kashuk JL, Moore EE, Johnson JL, Haenel J, Wilson M, Moore JB, Cothren CC, Biffl WL, Banerjee A, Sauaia A. Postinjury life threaten-ing coagulopathy: is 1:1 fresh frozen plasma:packed red blood cells the answer? J Trauma 65: 261–270, 2008.
32. Kozar RA, Peng Z, Zhang R, Holcomb JB, Pati S, Park P, Ko TC, Paredes A. Plasma restoration of endothelial glycocalyx in a rodent model of hemorrhagic shock. Anesth Analg 112: 1289–1295, 2011.
33. Lipowsky HH, Gao L, Lescanic A. Shedding of the endothelial glyco-calyx in arterioles, capillaries, and venules and its effect on capillary hemodynamics during inflammation. Am J Physiol Heart Circ Physiol 301: H2235–H2245, 2011.
34. Marki A, Esko JD, Pries AR, Ley K. Role of the endothelial surface layer in neutrophil recruitment. J Leukoc Biol 98: 503–515, 2015.
35. Mennander AA, Shalaby A, Oksala N, Leppanen T, Hamalainen M, Huovinen S, Zhao F, Moilanen E, Tarkka M. Diazoxide may protect endothelial glycocalyx integrity during coronary artery bypass grafting. Scand Cardiovasc J 46: 339–344, 2012.
36. Mulivor AW, Lipowsky HH. Inflammation-and ischemia-induced shed-ding of venular glycocalyx. Am J Physiol Heart Circ Physiol 286: H1672–H1680, 2004.
37. Mulivor AW, Lipowsky HH. Inhibition of glycan shedding and leuko-cyte-endothelial adhesion in postcapillary venules by suppression of ma-trix metalloprotease activity with doxycycline. Microcirculation 16: 657–666, 2009.
38. Mulivor AW, Lipowsky HH. Role of glycocalyx in leukocyte-endothe-lial cell adhesion. Am J Physiol Heart Circ Physiol 283: H1282–H1291, 2002.
39. Myburgh JA, Mythen MG. Resuscitation fluids. N Engl J Med 369: 2462–2463, 2013.
40. Nieuwdorp M, Meuwese MC, Mooij HL, van Lieshout MH, Hayden A, Levi M, Meijers JC, Ince C, Kastelein JJ, Vink H, Stroes ES. Tumor necrosis factor-α inhibition protects against endotoxin-induced endothelial glycocalyx perturbation. Atherosclerosis 202: 296–303, 2009.
41. Nieuwdorp M, Meuwese MC, Vink H, Hoekstra JB, Kastelein JJ, Stroes ES. The endothelial glycocalyx: a potential barrier between health and vascular disease. Curr Opin Lipidol 16: 507–511, 2005.
42. 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. Loss of endothelial glycocalyx during acute hyperglycemia coincides with endothelial dysfunction and coagulation activation in vivo. Diabetes 55: 480–486, 2006.
43. Pries AR, Kuebler WM. Normal endothelium. Handb Exp Pharmacol 1–40, 2006.
44. Pries AR, Secomb TW, Gaehtgens P. The endothelial surface layer. Pflügers Arch 440: 653–666, 2000.
45. Pries AR, Secomb TW, Sperandio M, Gaehtgens P. Blood flow resistance during hemodilution: effect of plasma composition. Cardiovasc Res 37: 225–235, 1998.
46. 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 116: 1896–1906, 2007.
47. Rhee P, Koustova E, Alam HB. Searching for the optimal resuscitation method: recommendations for the initial fluid resuscitation of combat casualties. J Trauma 54: S52–S62, 2003.
48. Rubio-Gayosso I, Platts SH, Duling BR. Reactive oxygen species mediate modification of glycocalyx during ischemia-reperfusion injury. Am J Physiol Heart Circ Physiol 290: H2247–H2256, 2006.
49. Russell DH, Barreto JC, Klemm K, Miller TA. Hemorrhagic shock increases gut macromolecular permeability in the rat. Shock 4: 50–55, 1995.
50. Salmon AH, Ferguson JK, Burford JL, Gevorgyan H, Nakano D, Harper SJ, Bates DO, Peti-Peterdi J. Loss of the endothelial glycocalyx links albumin-uria and vascular dysfunction. J Am Soc Nephrol 23: 1339–1350, 2012.
51. Savery MD, Jiang JX, Park PW, Damiano ER. The endothelial glyco-calyx in syndecan-1 deficient mice. Microvasc Res 87: 83–91, 2013.
52. Sillesen M, Rasmussen LS, Jin G, Jepsen CH, Imam A, Hwabejire JO, Halaweish I, DeMoya M, Velmahos G, Johansson PI, Alam HB. Assessment of coagulopathy, endothelial injury, and inflammation after traumatic brain injury and hemorrhage in a porcine model. J Trauma Acute Care Surg 76: 12–20, 2014.
53. Snoeijs MG, Vink H, Voesten N, Christiaans MH, Daemen JW, Peppelenbosch AG, Tordoir JH, Peutz-Kootstra CJ, Buurman WA, Schurink GW, van Heurn LW. Acute ischemic injury to the renal microvasculature in human kidney transplantation. Am J Physiol Renal Physiol 299: F1134–F1140, 2010.
54. Torres Filho I, Torres LN, Sondeen JL, Polykratis IA, Dubick MA. In vivo evaluation of venular glycocalyx during hemorrhagic shock in rats using intravital microscopy. Microvasc Res 85: 128–133, 2013.
55. Torres Filho IP, Contaifer D Jr, Garcia S, Torres LN. Effects of hypertonic saline solution on mesenteric microcirculation. Shock 15: 353–359, 2001.
56. Torres Filho IP, Torres LN, Pittman RN. Early physiologic responses to hemorrhagic hypotension. Transl Res 155: 78–88, 2010.
57. Torres Filho IP, Vink H, Torres LN, Pittman RN. Reduction in endothelial glycocalyx thickness after hemorrhage. FASEB J 23: 950, 2009.
58. Torres LN, Pittman RN, Torres Filho IP. Microvascular blood flow and oxygenation during hemorrhagic hypotension. Microvasc Res 75: 217–226, 2008.
59. Torres LN, Sondeen JL, Dubick MA, Filho IT. Systemic and micro-vascular effects of resuscitation with blood products after severe hemor-rhage in rats. J Trauma Acute Care Surg 77: 716–723, 2014.
60. Torres LN, Sondeen JL, Ji L, Dubick MA, Torres Filho I. Evaluation of resuscitation fluids on endothelial glycocalyx, venular blood flow, and coagulation function after hemorrhagic shock in rats. J Trauma Acute Care Surg 75: 759–766, 2013.
61. Vajda K, Szabo A, Boros M. Heterogeneous microcirculation in the rat small intestine during hemorrhagic shock: quantification of the effects of hypertonic-hyperoncotic resuscitation. Eur Surg Res 36: 338–344, 2004.
62. van Golen RF, van Gulik TM, Heger M. Mechanistic overview of reactive species-induced degradation of the endothelial glycocalyx during hepatic ischemia/reperfusion injury. Free Radic Biol Med 52: 1382–1402, 2012.
63. Villela NR, Tsai AG, Cabrales P, Intaglietta M. Improved resuscitation from hemorrhagic shock with Ringer’s lactate with increased viscosity in the hamster window chamber model. J Trauma 71: 418–424, 2011.
64. Ward BJ, Donnelly JL. Hypoxia induced disruption of the cardiac endothelial glycocalyx: implications for capillary permeability. Cardio-vasc Res 27: 384–389, 1993.
65. Weinbaum S, Tarbell JM, Damiano ER. The structure and function of the endothelial glycocalyx layer. Annu Rev Biomed Eng 9: 121–167, 2007.
66. Woodcock TE, Woodcock TM. Revised Starling equation and the glycocalyx model of transvascular fluid exchange: an improved para-digm for prescribing intravenous fluid therapy. Br J Anaesth 108: 384–394, 2012.
67. Zeng Y, Adamson RH, Curry FR, Tarbell JM. Sphingosine-1-phos-phate protects endothelial glycocalyx by inhibiting syndecan-1 shedding. Am J Physiol Heart Circ Physiol 306: H363–H372, 2014.