CAPILLARY LEAK AND EDEMA AFTER RESUSCITATION: THE POTENTIAL CONTRIBUTION OF REDUCED ENDOTHELIAL SHEAR STRESS CAUSED BY HEMODILUTION.
Journal
Shock (Augusta, Ga.)
ISSN: 1540-0514
Titre abrégé: Shock
Pays: United States
ID NLM: 9421564
Informations de publication
Date de publication:
01 10 2023
01 10 2023
Historique:
medline:
23
10
2023
pubmed:
30
8
2023
entrez:
30
8
2023
Statut:
ppublish
Résumé
Normal shear stress is essential for the normal structure and functions of the microcirculation. Hemorrhagic shock leads to reduced shear stress due to reduced tissue perfusion. Although essential for the urgent restoration of cardiac output and systemic blood pressure, large volume resuscitation with currently available solutions causes hemodilution, further reducing endothelial shear stress. In this narrative review, we consider how the use of currently available resuscitation solutions results in persistent reduction in endothelial shear stress, despite successfully increasing cardiac output and systemic blood pressure. We consider how this reduced shear stress causes (1) a failure to restore normal vasomotor function and normal tissue perfusion thus leading to persistent tissue hypoxia and (2) increased microvascular endothelial permeability resulting in edema formation and impaired organ function. We discuss the need for clinical research into resuscitation strategies and solutions that aim to quickly restore endothelial shear stress in the microcirculation to normal.
Identifiants
pubmed: 37647080
doi: 10.1097/SHK.0000000000002215
pii: 00024382-202310000-00002
doi:
Types de publication
Review
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
487-495Informations de copyright
Copyright © 2023 by the Shock Society.
Références
Tien HC, Spencer F, Tremblay LN, et al. Preventable deaths from hemorrhage at a level I Canadian trauma center. J Trauma . 2007;62(1):142–146.
Sauaia A, Moore FA, Moore EE, et al. Epidemiology of trauma deaths: a reassessment. J Trauma . 1995;38(2):185–193.
Eastridge BJ, Malone D, Holcomb JB. Early predictors of transfusion and mortality after injury: a review of the data-based literature. J Trauma . 2006;60(6 Suppl):S20–S25.
Tachon G, Harrois A, Tanaka S, et al. Microcirculatory alterations in traumatic hemorrhagic shock. Crit Care Med . 2014;42(6):1433–1441.
Massey MJ, Hou PC, Filbin M, et al. Microcirculatory perfusion disturbances in septic shock: results from the ProCESS trial. Crit Care . 2018;22(1):308.
Trzeciak S, McCoy JV, Phillip Dellinger R, et al. Early increases in microcirculatory perfusion during protocol-directed resuscitation are associated with reduced multi-organ failure at 24 h in patients with sepsis. Intensive Care Med . 2008;34(12):2210–2217.
De Backer D, Donadello K, Sakr Y, et al. Microcirculatory alterations in patients with severe sepsis: impact of time of assessment and relationship with outcome. Crit Care Med . 2013;41(3):791–799.
Kerger H, Waschke KF, Ackern KV, et al. Systemic and microcirculatory effects of autologous whole blood resuscitation in severe hemorrhagic shock. Am J Physiol . 1999;276(6):H2035–H2043.
Cryer HM, Gosche J, Harbrecht J, et al. The effect of hypertonic saline resuscitation on responses to severe hemorrhagic shock by the skeletal muscle, intestinal, and renal microcirculation systems: seeing is believing. Am J Surg . 2005;190(2):305–313.
Scalia S, Burton H, Van Wylen D, et al. Persistent arteriolar constriction in microcirculation of the terminal ileum following moderate hemorrhagic hypovolemia and volume restoration. J Trauma . 1990;30(6):713–718.
Chignalia AZ, Yetimakman F, Christiaans SC, et al. The glycocalyx and trauma: a review. Shock . 2016;45(4):338–348.
Wu F, Chipman A, Pati S, et al. Resuscitative strategies to modulate the endotheliopathy of trauma: from cell to patient. Shock . 2020;53(5):575–584.
Silversides JA, Fitzgerald E, Manickavasagam US, et al. Deresuscitation of patients with iatrogenic fluid overload is associated with reduced mortality in critical illness. Crit Care Med . 2018;46(10):1600–1607.
Lee JA. Sydney Ringer (1834–1910) and Alexis Hartmann (1898–1964). Anaesthesia . 1981;36(12):1115–1121.
Miller DJ. Sydney Ringer; physiological saline, calcium and the contraction of the heart. J Physiol . 2004;555(Pt 3):585–587.
Vincent JL. Fluid management in the critically ill. Kidney Int . 2019;96(1):52–57.
Finfer S, Myburgh J, Bellomo R. Intravenous fluid therapy in critically ill adults. In: Nature Reviews Nephrology . Nature Publishing Group, 2018:541–557.
Patel A, Laffan MA, Waheed U, et al. Randomised trials of human albumin for adults with sepsis: systematic review and meta-analysis with trial sequential analysis of all-cause mortality. BMJ . 2014;349:g4561.
Myburgh JA. Fluid resuscitation in acute medicine: what is the current situation? J Intern Med . 2015;277(1):58–68.
Secomb TW, Hsu R, Pries AR. Effect of the endothelial surface layer on transmission of fluid shear stress to endothelial cells. Biorheology . 2001;38:143–150.
Tarbell JM, Pahakis MY. Mechanotransduction and the glycocalyx. J Intern Med . 2006;259:339–350.
Curry FE, Adamson RH. Endothelial glycocalyx: permeability barrier and mechanosensor. Ann Biomed Eng . 2012;40:828–839.
Carr JMJR, Hoiland RL, Caldwell HG, et al. Internal carotid and brachial artery shear-dependent vasodilator function in young healthy humans. J Physiol . 2020;598(23):5333–5350.
Iwamoto E, Sakamoto R, Tsuchida W, et al. Effects of menstrual cycle and menopause on internal carotid artery shear-mediated dilation in women. Am J Physiol Heart Circ Physiol . 2021;320(2):H679–h689.
Deng H., Min E, Baeyens N, Activation of Smad2/3 signaling by low fluid shear stress mediates artery inward remodeling. Proc Natl Acad Sci U S A. 2021;118(37): p. e2105339118.
Kostyunina DS, Rowan SC, Pakhomov NV, et al. Shear stress markedly alters the proteomic response to hypoxia in human pulmonary endothelial cells. Am J Respir Cell Mol Biol . 2023;68(5):551–565.
Mehta V, Pang KL, Rozbesky D, et al. The guidance receptor plexin D1 is a mechanosensor in endothelial cells. Nature . 2020;578(7794):290–295.
Siragusa M, Oliveira Justo AF, Malacarne PF, et al. VE-PTP inhibition elicits eNOS phosphorylation to blunt endothelial dysfunction and hypertension in diabetes. Cardiovasc Res . 2021;117(6):1546–1556.
Coon BG, Timalsina S, Astone M, et al. A mitochondrial contribution to anti-inflammatory shear stress signaling in vascular endothelial cells. J Cell Biol . 2022;221(7):e202109144.
Xu J, Mathur J, Vessières E, et al. GPR68 senses flow and is essential for vascular physiology. Cell . 2018;173(3):762–775.e16.
Mack JJ, Mosqueiro TS, Archer BJ, et al. NOTCH1 is a mechanosensor in adult arteries. Nat Commun . 2017;8(1):1620.
Singh S, Adam M, Matkar PN, et al. Endothelial-specific loss of IFT88 promotes endothelial-to-mesenchymal transition and exacerbates bleomycin-induced pulmonary fibrosis. Sci Rep . 2020;10(1):4466.
Fåhræus R, Lindqvist T. The viscosity of the blood in narrow capillary tubes. Am J Physiol-Legacy Content . 1931;96:562–568.
Popel AS, Regirer SA, Usick PI. A continuum model of blood flow. Biorheology . 1974;11:427–437.
Reneman RS, Arts T, Hoeks AP. Wall shear stress—an important determinant of endothelial cell function and structure—in the arterial system in vivo. Discrepancies with theory. J Vasc Res . 2006;43(3):251–269.
Long DS, Smith ML, Pries AR, et al. Microviscometry reveals reduced blood viscosity and altered shear rate and shear stress profiles in microvessels after hemodilution. Proc Natl Acad Sci U S A . 2004;101:10060–10065.
Savery MD, Damiano ER. The endothelial glycocalyx is hydrodynamically relevant in arterioles throughout the cardiac cycle. Biophys J . 2008;95(3):1439–1447.
Gates PE, Gurung A, Mazzaro L, et al. Measurement of wall shear stress exerted by flowing blood in the human carotid artery: ultrasound Doppler velocimetry and echo particle image velocimetry. Ultrasound Med Biol . 2018;44(7):1392–1401.
Sriram K, Intaglietta M, Tartakovsky DM. Non-Newtonian flow of blood in arterioles: consequences for wall shear stress measurements. Microcirculation . 2014;21(7):628–639.
van Haaren PM, VanBavel E, Vink H, et al. Localization of the permeability barrier to solutes in isolated arteries by confocal microscopy. Am J Physiol Heart Circ Physiol . 2003;285(6):H2848–H2856.
Pries AR, Secomb TW, Gaehtgens P. The endothelial surface layer. Pflugers Arch . 2000;440(5):653–666.
Reitsma S, Slaaf DW, Vink H, et al. The endothelial glycocalyx: composition, functions, and visualization. Pflugers Arch . 2007;454(3):345–359.
Tarbell JM, Simon SI, Curry FR. Mechanosensing at the vascular interface. Annu Rev Biomed Eng . 2014;16:505–532.
Weinbaum S, Zhang X, Han Y, et al. Mechanotransduction and flow across the endothelial glycocalyx. Proc Natl Acad Sci . 2003;100:7988–7995.
Adapala RK, Katari V, Teegala LR, et al. TRPV4 Mechanotransduction in fibrosis. Cells . 2021;10(11):3053.
Ranade SS, Qiu Z, Woo SH, et al. Piezo1, a mechanically activated ion channel, is required for vascular development in mice. Proc Natl Acad Sci U S A . 2014;111(28):10347–10352.
Martel MJ. No. 115-hemorrhagic shock. J Obstet Gynaecol Can . 2018;40(12):e874–e882.
Kaur P, Basu S, Kaur G, et al. Transfusion protocol in trauma. J Emerg Trauma Shock . 2011;4(1):103–108.
Spahn DR, Bouillon B, Cerny V, et al. The European guideline on management of major bleeding and coagulopathy following trauma: fifth edition. Crit Care . 2019;23(1):98.
Pacheco LD, Saade GR, Costantine MM, et al. An update on the use of massive transfusion protocols in obstetrics. Am J Obstet Gynecol . 2016;214(3):340–344.
Meneses E, Boneva D, McKenney M, et al. Massive transfusion protocol in adult trauma population. Am J Emerg Med . 2020;38(12):2661–2666.
Holcomb JB, Jenkins D, Rhee P, et al. Damage control resuscitation: directly addressing the early coagulopathy of trauma. J Trauma . 2007;62(2):307–310.
Stainsby D, MacLennan S, Thomas D, et alBritish Committee for Standards in Haematology. Guidelines on the management of massive blood loss. Br J Haematol . 2006;135(5):634–641.
Holcomb JB, Tilley BC, Baraniuk S, et al. Transfusion of plasma, platelets, and red blood cells in a 1:1:1 vs a 1:1:2 ratio and mortality in patients with severe trauma: the PROPPR randomized clinical trial. JAMA . 2015;313:471–482.
Rahouma M, Kamel M, Jodeh D, et al. Does a balanced transfusion ratio of plasma to packed red blood cells improve outcomes in both trauma and surgical patients? A meta-analysis of randomized controlled trials and observational studies. Am J Surg . 2018;216(2):342–350.
McQuilten ZK, Crighton G, Brunskill S, et al. Optimal dose, timing and ratio of blood products in massive transfusion: results from a systematic review. Transfus Med Rev . 2018;32(1):6–15.
Torres CM, Kent A, Scantling D, et al. Association of whole blood with survival among patients presenting with severe hemorrhage in US and Canadian adult civilian trauma centers. JAMA Surg . 2023;158(5):532–540.
Spinella PC, Pidcoke HF, Strandenes G, et al. Whole blood for hemostatic resuscitation of major bleeding. Transfusion . 2016;56(suppl 2):S190–S202.
Gurney J, Staudt A, Cap A, et al. Improved survival in critically injured combat casualties treated with fresh whole blood by forward surgical teams in Afghanistan. Transfusion . 2020;60(suppl 3):S180–S188.
Williams J, Gustafson M, Bai Y, et al. Limitations of available blood products for massive transfusion during mass casualty events at US level 1 trauma centers. Shock . 2021;56(1S):62–69.
Morgan JM, Calleja P. Emergency trauma care in rural and remote settings: challenges and patient outcomes. Int Emerg Nurs . 2020;51:100880.
Whedon JM, von Recklinghausen FM. An exploratory analysis of transfer times in a rural trauma system. J Emerg Trauma Shock . 2013;6(4):259–263.
ATLS Subcommittee; American College of Surgeons’ Committee on Trauma; International ATLS working group. Advanced Trauma Life Support (ATLS®): The Ninth Edition. J Trauma Acute Care Surg . 2013;74(5):1363–1366.
Kanani AN, Hartshorn S. NICE clinical guideline NG39: major trauma: assessment and initial management. Arch Dis Child Educ Pract Ed . 2017;102(1):20–23.
Zampieri FG, Machado FR, Biondi RS, et al. Effect of intravenous fluid treatment with a balanced solution vs 0.9% saline solution on mortality in critically ill patients: the BaSICS randomized clinical trial. JAMA . 2021;326(9):1–12.
Finfer S, Micallef S, Hammond N, et al. Balanced multielectrolyte solution versus saline in critically ill adults. N Engl J Med . 2022;386(9):815–826.
Gomez H, Priyanka P, Bataineh A, et al. Effects of 5% albumin plus saline versus saline alone on outcomes from large-volume resuscitation in critically ill patients. Crit Care Med . 2021;49(1):79–90.
Vaya A, Simo M, Santaolaria M, Carrasco P, Corella D. Plasma viscosity and related cardiovascular risk factors in a Spanish Mediterranean population. Thromb Res . 2007;120(4):489–495.
Hammond NE, Taylor C, Saxena M, et al. Resuscitation fluid use in Australian and New Zealand intensive care units between 2007 and 2013. Intensive Care Med . 2015;41(9):1611–1619.
Harreby M, Danneskiold-Samsøe B, Kjer J, et al. Viscosity of plasma in patients with rheumatoid arthritis. Ann Rheum Dis . 1987;46(8):601–604.
Hayakawa M. Pathophysiology of trauma-induced coagulopathy: disseminated intravascular coagulation with the fibrinolytic phenotype. J Intensive Care . 2017;5:14.
Savery MD, Jiang JX, Park PW, et al. The endothelial glycocalyx in syndecan-1 deficient mice. Microvasc Res . 2013;87:83–91.
Muller JM, Davis MJ, Chilian WM. Integrated regulation of pressure and flow in the coronary microcirculation. Cardiovasc Res . 1996;32(4):668–678.
Koller A, Sun D, Kaley G. Role of shear stress and endothelial prostaglandins in flow- and viscosity-induced dilation of arterioles in vitro. Circ Res . 1993;72(6):1276–1284.
Koller A, Sun D, Huang A, et al. Corelease of nitric oxide and prostaglandins mediates flow-dependent dilation of rat gracilis muscle arterioles. Am J Physiol . 1994;267(1 Pt 2):H326–H332.
Buga GM, Gold ME, Fukuto JM, et al. Shear stress-induced release of nitric oxide from endothelial cells grown on beads. Hypertension . 1991;17(2):187–193.
Lakshmikanthan S, Zheng X, Nishijima Y, et al. Rap1 promotes endothelial mechanosensing complex formation, NO release and normal endothelial function. EMBO Rep . 2015;16(5):628–637.
Frangos JA, Eskin SG, McIntire LV, et al. Flow effects on prostacyclin production by cultured human endothelial cells. Science . 1985;227(4693):1477–1479.
Furchgott RF, Vanhoutte PM. Endothelium-derived relaxing and contracting factors. FASEB J . 1989;3(9):2007–2018.
Pohl U, Herlan K, Huang A, et al. EDRF-mediated shear-induced dilation opposes myogenic vasoconstriction in small rabbit arteries. Am J Physiol . 1991;261(6 Pt 2):H2016–H2023.
Melkumyants AM, Balashov SA, Khayutin VM. Endothelium dependent control of arterial diameter by blood viscosity. Cardiovasc Res . 1989;23(9):741–747.
Sakai H, Sato T, Maekawa Y, et al. Capillary blood flow during severe hemodilution observed by a noninvasive transcutaneous technique using flash epi-illumination. Microvasc Res . 2002;64(1):120–126.
Tsai AG, Friesenecker B, McCarthy M, et al. Plasma viscosity regulates capillary perfusion during extreme hemodilution in hamster skinfold model. Am J Physiol . 1998;275(6):H2170–H2180.
Cabrales P, Martini J, Intaglietta M, et al. Blood viscosity maintains microvascular conditions during normovolemic anemia independent of blood oxygen-carrying capacity. Am J Physiol Heart Circ Physiol . 2006;291(2):H581–H590.
Belcher DA, Williams AT, Palmer AF, et al. Polymerized albumin restores impaired hemodynamics in endotoxemia and polymicrobial sepsis. Sci Rep . 2021;11(1):10834.
Cabrales P, Intaglietta M, Tsai AG. Increase plasma viscosity sustains microcirculation after resuscitation from hemorrhagic shock and continuous bleeding. Shock . 2005;23(6):549–555.
Villela NR, Tsai AG, Cabrales P, et al. Improved resuscitation from hemorrhagic shock with Ringer's lactate with increased viscosity in the hamster window chamber model. J Trauma . 2011.71(2):418–424.
Cabrales P, Tsai AG, Intaglietta M. Is resuscitation from hemorrhagic shock limited by blood oxygen-carrying capacity or blood viscosity? Shock . 2007;27(4):380–389.
Dekker RJ, van Soest S, Fontijn RD, et al. Prolonged fluid shear stress induces a distinct set of endothelial cell genes, most specifically lung Krüppel-like factor (KLF2). Blood . 2002;100:1689–1698.
Walsh TG, Murphy RP, Fitzpatrick P, et al. Stabilization of brain microvascular endothelial barrier function by shear stress involves VE-cadherin signaling leading to modulation of pTyr-occludin levels. J Cell Physiol . 2011;226(11):3053–3063.
Seebach J, Dieterich P, Luo F, et al. Endothelial barrier function under laminar fluid shear stress. Lab Invest . 2000;80(12):1819–1831.
Siddharthan V, Kim YV, Liu S, et al. Human astrocytes/astrocyte-conditioned medium and shear stress enhance the barrier properties of human brain microvascular endothelial cells. Brain Res . 2007;1147:39–50.
Ando J, Yamamoto K. Vascular mechanobiology: endothelial cell responses to fluid shear stress. Circ J . 2009;73(11):1983–1992.
Moon JJ, Matsumoto M, Patel S, et al. Role of cell surface heparan sulfate proteoglycans in endothelial cell migration and mechanotransduction. J Cell Physiol . 2005;203(1):166–176.
Colgan OC, Ferguson G, Collins NT, et al. Regulation of bovine brain microvascular endothelial tight junction assembly and barrier function by laminar shear stress. Am J Physiol Heart Circ Physiol . 2007;292(6):H3190–H3197.
Zeng Y, Tarbell JM. The adaptive remodeling of endothelial glycocalyx in response to fluid shear stress. PloS One . 2014;9:e86249.
Wang G, Kostidis S, Tiemeier GL, et al. Shear stress regulation of endothelial glycocalyx structure is determined by glucobiosynthesis. Arterioscler Thromb Vasc Biol . 2020;40:350–364.
Rowan SC, Rochfort KD, Piouceau L, et al. Pulmonary endothelial permeability and tissue fluid balance depend on the viscosity of the perfusion solution. Am J Physiol Lung Cell Mol Physiol . 2018;315:L476–L484.
Torres Filho I, Torres LN, Sondeen JL, et al. In vivo evaluation of venular glycocalyx during hemorrhagic shock in rats using intravital microscopy. Microvasc Res . 201385:128–133.
Torres Filho IP, Torres LN, Salgado C, et al. 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(11):H1468–H1478.
Kozar RA, Peng Z, Zhang R, et al. Plasma restoration of endothelial glycocalyx in a rodent model of hemorrhagic shock. Anesth Analg . 2011;112(6):1289–1295.
Torres LN, Chung KK, Salgado CL, et al. Low-volume resuscitation with normal saline is associated with microvascular endothelial dysfunction after hemorrhage in rats, compared to colloids and balanced crystalloids. Crit Care . 2017;21(1):160.
Peng Z, Pati S, Potter D, et al. Fresh frozen plasma lessens pulmonary endothelial inflammation and hyperpermeability after hemorrhagic shock and is associated with loss of syndecan 1. Shock . 2013;40(3):195–202.
Naumann DN, Beaven A, Dretzke J, et al. Searching for the optimal fluid to restore microcirculatory flow dynamics after haemorrhagic shock: a systematic review of preclinical studies. Shock . 2016;46(6):609–622.
Walsh D. VEGFR2-dependent restoration of pulmonary endothelial barrier function by perfusion with optimal physiological viscosity solution following ischemia-reperfusion injury. Am Thorac Soc Ann Meeting . 2022.
Ponschab M, Schöchl H, Gabriel C, et al. Haemostatic profile of reconstituted blood in a proposed 1:1:1 ratio of packed red blood cells, platelet concentrate and four different plasma preparations. Anaesthesia . 2015;70(5):528–536.
Brummel-Ziedins K, Whelihan MF, Ziedins EG, et al. The resuscitative fluid you choose may potentiate bleeding. J Trauma . 2006;61(6):1350–1358.
Brazil EV, Coats TJ. Sonoclot coagulation analysis of in-vitro haemodilution with resuscitation solutions. J R Soc Med . 2000;93(10):507–510.
Coats TJ, Brazil E, Heron M, et al. Impairment of coagulation by commonly used resuscitation fluids in human volunteers. Emerg Med J . 2006;23(11):846–849.
Smith CA, Gosselin RC, Utter GH, et al. Does saline resuscitation affect mechanisms of coagulopathy in critically ill trauma patients? An exploratory analysis. Blood Coagul Fibrinolysis . 2015;26(3):250–254.
Myburgh JA, Mythen MG. Resuscitation fluids. N Engl J Med . 2013;369:1243–1251.
Hartmann AF, Senn MJ. Studies in the metabolism of sodium r-lactate. I. response of normal human subjects to the intravenous injection of sodium r-lactate. J Clin Invest . 1932;11(2):327–335.
Kellum JA. Abnormal saline and the history of intravenous fluids. Nat Rev Nephrol . 2018;14(6):358–360.
Weinkove R, Rangarajan S. Fibrinogen concentrate for acquired hypofibrinogenaemic states. Transfus Med . 2008;18(3):151–157.
Weiss G, Lison S, Glaser M, et al. Observational study of fibrinogen concentrate in massive hemorrhage: evaluation of a multicenter register. Blood Coagul Fibrinolysis . 2011;22(8):727–734.
Spahn DR, Cerny V, Coats TJ, et al. Management of bleeding following major trauma: a European guideline. Crit Care . 2007;11(1):R17.
Stinger HK, Spinella PC, Perkins JG, et al. The ratio of fibrinogen to red cells transfused affects survival in casualties receiving massive transfusions at an army combat support hospital. J Trauma . 2008;64(2 suppl):S79–S85.
Fenger-Eriksen C, Ingerslev J, Sørensen B. Fibrinogen concentrate–a potential universal hemostatic agent. Expert Opin Biol Ther . 2009;9(10):1325–1333.