Hypervolemia increases release of atrial natriuretic peptide and shedding of the endothelial glycocalyx

Daniel Chappell, Dirk Bruegger, Julia Potzel, Matthias Jacob, Florian Brettner, Michael Vogeser, Peter Conzen, Bernhard F Becker, Markus Rehm, Daniel Chappell, Dirk Bruegger, Julia Potzel, Matthias Jacob, Florian Brettner, Michael Vogeser, Peter Conzen, Bernhard F Becker, Markus Rehm

Abstract

Introduction: Acute normovolemic hemodilution (ANH) and volume loading (VL) are standard blood-sparing procedures. However, VL is associated with hypervolemia, which may cause tissue edema, cardiopulmonary complications and a prolonged hospital stay. The body reacts to hypervolemia with release of atrial natriuretic peptide (ANP) from the heart. ANP has been shown to deteriorate the endothelial glycocalyx, a vital part of the vascular permeability barrier. The aim of the present study was to evaluate and compare ANP release and damage to the glycocalyx during ANH and VL.

Methods: ANH or VL with 6% hydroxyethyl starch 130/0.4 was administered prior to elective surgery in patients of good cardiopulmonary health (n =9 in each group). We measured concentrations of ANP in plasma and of three main constituent parts of the glycocalyx (hyaluronan, heparan sulfate and syndecan 1) in serum before and after ANH or VL. Heparan sulfate and syndecan 1 levels in urine were also determined.

Results: In contrast to ANH, VL (20 ml/kg) induced a significant release of ANP (approximately +100%, P <0.05) and increased the serum concentration of two glycocalyx constituents, hyaluronan and syndecan 1 (both by about 80%, P <0.05). Elevation of syndecan 1 was also detected in the urine of patients undergoing VL, but no increase was found in patients undergoing ANH. Heparan sulfate levels were not influenced by either procedure.

Conclusion: These data suggest that hypervolemia increases the release of ANP and causes enhanced shedding of the endothelial glycocalyx. This perturbation must be expected to impair the vascular barrier, implying that VL may not be as safe as generally assumed and that it should be critically evaluated.

Figures

Figure 1
Figure 1
Atrial natriuretic peptide concentrations. Atrial natriuretic peptide concentrations before (pre) and after (post) volume loading (VL, n =9) or acute normovolemic hemodilution (ANH, n =9) with 6% hydroxyethyl starch 130/0.4. To account for hemodilution, individual atrial natriuretic peptide concentrations were normalized to the individual albumin concentrations. Data are given as mean ± SEM. *P <0.05 (significantly different from pre).
Figure 2
Figure 2
Serum concentrations of glycocalyx components. Serum concentrations of heparan sulfate (a), hyaluronan (b) and syndecan 1 (c) before (pre) and after (post) volume loading (VL, n = 9) or acute normovolemic hemodilution (ANH, n = 9) with 6% hydroxyethyl starch 130/0.4. To account for hemodilution, individual heparan sulfate, hyaluronan and syndecan 1 concentrations were normalized to the individual albumin concentrations. Data are given as mean ± SEM. *P <0.05 (significantly different from pre).
Figure 3
Figure 3
Urinary concentrations of glycocalyx components. Urinary concentrations of heparan sulfate (a) and syndecan 1 (b) before (pre) and after (post) volume loading (VL, n = 9) or acute normovolemic hemodilution (ANH, n = 9) with 6% hydroxyethyl starch 130/0.4. Data are given as mean ± SEM. *P <0.05 (significantly different from pre).

References

    1. Pries AR, Kuebler WM. Normal endothelium. Handb Exp Pharmacol. 2006;176:1–40. doi: 10.1007/3-540-32967-6_1.
    1. Curry FE, Adamson RH. Endothelial glycocalyx: permeability barrier and mechanosensor. Ann Biomed Eng. 2012;40:828–839. doi: 10.1007/s10439-011-0429-8.
    1. Pries AR, Secomb TW, Gaehtgens P. The endothelial surface layer. Pflugers Arch. 2000;440:653–666. doi: 10.1007/s004240000307.
    1. Weinbaum S, Tarbell JM, Damiano ER. 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. Curry FR, Adamson RH. Vascular permeability modulation at the cell, microvessel, or whole organ level: towards closing gaps in our knowledge. Cardiovasc Res. 2010;87:218–229. doi: 10.1093/cvr/cvq115.
    1. Burke-Gaffney A, Evans TW. Lest we forget the endothelial glycocalyx in sepsis. Crit Care. 2012;16:121. doi: 10.1186/cc11239.
    1. Nelson A, Berkestedt I, Schmidtchen A, Ljunggren L, Bodelsson M. Increased levels of glycosaminoglycans during septic shock: relation to mortality and the antibacterial actions of plasma. Shock. 2008;30:623–627. doi: 10.1097/SHK.0b013e3181777da3.
    1. 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. doi: 10.1097/SLA.0b013e318226113d.
    1. Lobo DN, Bostock KA, Neal KR, Perkins AC, Rowlands BJ, Allison SP. Effect of salt and water balance on recovery of gastrointestinal function after elective colonic resection: a randomised controlled trial. Lancet. 2002;359:1812–1818. doi: 10.1016/S0140-6736(02)08711-1.
    1. Nisanevich V, Felsenstein I, Almogy G, Weissman C, Einav S, Matot I. Effect of intraoperative fluid management on outcome after intraabdominal surgery. Anesthesiology. 2005;103:25–32. doi: 10.1097/00000542-200507000-00008.
    1. Brandstrup B, Tønnesen H, Beier-Holgersen R, Hjortsø E, Ørding 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. Effects of intravenous fluid restriction on postoperative complications: comparison of two perioperative fluid regimens: a randomized assessor-blinded multicenter trial. Ann Surg. 2003;238:641–648. doi: 10.1097/01.sla.0000094387.50865.23.
    1. Curry FR. Atrial natriuretic peptide: an essential physiological regulator of transvascular fluid, protein transport, and plasma volume. J Clin Invest. 2005;115:1458–1461. doi: 10.1172/JCI25417.
    1. Bruegger D, Jacob M, Rehm M, Loetsch M, Welsch U, Conzen P, Becker BF. 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. Bruegger D, Schwartz L, Chappell D, Jacob M, Rehm M, Vogeser M, Christ F, Reichart B, Becker BF. Release of atrial natriuretic peptide precedes shedding of the endothelial glycocalyx equally in patients undergoing on- and off-pump coronary artery bypass surgery. Basic Res Cardiol. 2011;106:1111–1121. doi: 10.1007/s00395-011-0203-y.
    1. Rehm M, Haller M, Orth V, Kreimeier U, Jacob M, Dressel H, Mayer S, Brechtelsbauer H, Finsterer U. Changes in blood volume and hematocrit during acute preoperative volume loading with 5% albumin or 6% hetastarch solutions in patients before radical hysterectomy. Anesthesiology. 2001;95:849–856. doi: 10.1097/00000542-200110000-00011.
    1. Rehm M, Orth V, Kreimeier U, Thiel M, Haller M, Brechtelsbauer H, Finsterer U. Changes in intravascular volume during acute normovolemic hemodilution and intraoperative retransfusion in patients with radical hysterectomy. Anesthesiology. 2000;92:657–664. doi: 10.1097/00000542-200003000-00008.
    1. Perner A, Haase N, Guttormsen AB, Tenhunen J, Klemenzson G, Åneman A, Madsen KR, Møller MH, Elkjær JM, Poulsen LM, Bendtsen A, Winding R, Steensen M, Berezowicz P, Søe-Jensen P, Bestle M, Strand K, Wiis J, White JO, Thornberg KJ, Quist L, Nielsen J, Andersen LH, Holst LB, Thormar K, Kjældgaard AL, Fabritius ML, Mondrup F, Pott FC, Møller TP, Winkel P, Wetterslev J, for the 6S Trial Group and Scandinavian Critical Care Trials Group 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. Myburgh JA, Finfer S, Bellomo R, Billot L, Cass A, Gattas D, Glass P, Lipman J, Liu B, McArthur C, McGuinness S, Rajbhandari D, Taylor CB, Webb SAR, for the CHEST Investigators and the Australian and New Zealand Intensive Care Society Clinical Trials Group Hydroxyethyl starch or saline for fluid resuscitation in intensive care. N Engl J Med. 2012;367:1901–1911. doi: 10.1056/NEJMoa1209759.
    1. 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;138:1445–1447. doi: 10.1016/j.jtcvs.2008.07.063.
    1. Zausig YA, Chappell D, Becker BF, Potschka D, Busse H, Nixdorf K, Bitzinger D, Jacob B, Jacob M. The impact of crystalloidal and colloidal infusion preparations on coronary vascular integrity, interstitial oedema and cardiac performance in isolated hearts. Crit Care. 2013;17:R203. doi: 10.1186/cc12898.
    1. 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. doi: 10.1186/cc6913.
    1. 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;116:1896–1906. doi: 10.1161/CIRCULATIONAHA.106.684852.
    1. 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. 2007;107:776–784. doi: 10.1097/01.anes.0000286984.39328.96.
    1. Fraser JR, Laurent TC, Pertoft H, Baxter E. Plasma clearance, tissue distribution and metabolism of hyaluronic acid injected intravenously in the rabbit. Biochem J. 1981;200:415–424.
    1. Lebel L. Clearance of hyaluronan from the circulation. Adv Drug Deliv Rev. 1991;7:221–235. doi: 10.1016/0169-409X(91)90003-U.
    1. Pouta AM, Karinen J, Vuolteenaho OJ, Laatikainen TJ. Effect of intravenous fluid preload on vasoactive peptide secretion during Caesarean section under spinal anaesthesia. Anaesthesia. 1996;51:128–132. doi: 10.1111/j.1365-2044.1996.tb07698.x.
    1. Kumar R, Chakraborty I, Sehgal R. A prospective randomized study comparing two techniques of perioperative blood conservation: isovolemic hemodilution and hypervolemic hemodilution. Anesth Analg. 2002;95:1154–1161. doi: 10.1097/00000539-200211000-00005.
    1. Schreier B, Börner S, Völker K, Gambaryan S, Schäfer SC, Kuhlencordt P, Gassner B, Kuhn M. The heart communicates with the endothelium through the guanylyl cyclase-A receptor: acute handling of intravascular volume in response to volume expansion. Endocrinology. 2008;149:4193–4199. doi: 10.1210/en.2008-0212.
    1. Chappell D, Jacob M, Hofmann-Kiefer K, Conzen P, Rehm M. A rational approach to perioperative fluid management. Anesthesiology. 2008;109:723–740. doi: 10.1097/ALN.0b013e3181863117.
    1. Bayer O, Reinhart K, Kohl M, Kabisch B, Marshall J, Sakr Y, Bauer M, Hartog C, Schwarzkopf D, Riedemann N. Effects of fluid resuscitation with synthetic colloids or crystalloids alone on shock reversal, fluid balance, and patient outcomes in patients with severe sepsis: a prospective sequential analysis. Crit Care Med. 2012;40:2543–2551. doi: 10.1097/CCM.0b013e318258fee7.
    1. Guidet B, Martinet O, Boulain T, Philippart F, Poussel J, Maizel J, Forceville X, Feissel M, Hasselmann M, Heininger A, Van Aken H. 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/cc11358.
    1. Annane D, Siami S, Jaber S, Martin C, Elatrous S, Declère AD, Preiser JC, Outin H, Troché G, Charpentier C, Trouillet JL, Kimmoun A, Forceville X, Darmon M, Lesur O, Reignier J, Abroug F, Berger P, Clec’h C, Cousson J, Thibault L, Chevret S, for the CRISTAL Investigators Effects of fluid resuscitation with colloids vs crystalloids on mortality in critically ill patients presenting with hypovolemic shock: the CRISTAL randomized trial. JAMA. 2013;310:1809–1817. doi: 10.1001/jama.2013.280502.
    1. Caironi P, Tognoni G, Masson S, Fumagalli R, Pesenti A, Romero M, Fanizza C, Caspani L, Faenza S, Grasselli G, Iapichino G, Antonelli M, Parrini V, Fiore G, Latini R, Gattinoni L, for the ALBIOS Study Investigators Albumin replacement in patients with severe sepsis or septic shock. N Engl J Med. 2014;370:1412–1421. doi: 10.1056/NEJMoa1305727.
    1. Jacob M, Bruegger D, Rehm M, Welsch U, Conzen P, Becker BF. Contrasting effects of colloid and crystalloid resuscitation fluids on cardiac vascular permeability. Anesthesiology. 2006;104:1223–1231. doi: 10.1097/00000542-200606000-00018.
    1. Drummer C, Heer M, Baisch F, Blomqvist CG, Lang RE, Maass H, Gerzer R. Diuresis and natriuresis following isotonic saline infusion in healthy young volunteers before, during, and after HDT. Acta Physiol Scand. 1992;604:101–111.
    1. Becker BF, Chappell D, Jacob M. Endothelial glycocalyx and coronary vascular permeability: the fringe benefit. Basic Res Cardiol. 2010;105:687–701. doi: 10.1007/s00395-010-0118-z.

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