Myocardial depression in sepsis: From pathogenesis to clinical manifestations and treatment

Journal of Critical Care

Volumn 29, Issue 4, 2014, Pages 500-511

  Antonucci, Elio ^a   Fiaccadori, Enrico ^a   Donadello, Katia ^b   Taccone, Fabio Silvio ^b   Franchi, Federico ^c   Scolletta, Sabino ^c  

^a UNIVERSITY OF PARMA MEDICAL SCHOOL   (Italy)

^b ERASME HOSPITAL   (Belgium)

^c UNIVERSITY OF SIENA   (Italy)

Author keywords

Myocardial depression; Myocardial dysfunction; Septic shock; Severe sepsis

Indexed keywords

ADRENALIN; ANTIBIOTIC AGENT; CALCIUM CHANNEL; CALCIUM CHANNEL L TYPE; CATECHOLAMINE; DOBUTAMINE; DOPAMINE; ENDOTHELIN 1; HYDROCORTISONE; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1; INTERLEUKIN 6; LACTIC ACID; LEVOSIMENDAN; NITRIC OXIDE; NORADRENALIN; REACTIVE OXYGEN METABOLITE; TERLIPRESSIN; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA; VASOPRESSIN; VASOCONSTRICTOR AGENT;

ANTIBIOTIC THERAPY; APOPTOSIS; ARTERIAL PRESSURE; ARTIFICIAL VENTILATION; AUTONOMIC DYSFUNCTION; BLOOD VESSEL TONE; BREATHING RATE; CALCIUM CURRENT; CARDIOMYOPATHY; CELL INFILTRATION; CLINICAL FEATURE; CLINICAL TRIAL (TOPIC); DIAGNOSTIC PROCEDURE; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DRUG DOSE INCREASE; DRUG EFFECT; ECHOCARDIOGRAPHY; FLUID THERAPY; GENETIC ASSOCIATION; GLIA CELL; HEART AFTERLOAD; HEART ARRHYTHMIA; HEART FUNCTION; HEART HEMODYNAMICS; HEART LEFT VENTRICLE FAILURE; HEART MUSCLE CONTRACTILITY; HEART MUSCLE ISCHEMIA; HEART MUSCLE OXYGEN CONSUMPTION; HEART OUTPUT; HEART PRELOAD; HEART RIGHT VENTRICLE FAILURE; HEART VENTRICLE HYPERTROPHY; HUMAN; LACTATE BLOOD LEVEL; MACROPHAGE; MICROANGIOPATHY; MONOCYTE; MYOCARDIAL DEPRESSION; MYOCARDIAL DISEASE; MYOCARDIAL PERFUSION ECHOCARDIOGRAPHY; NERVE CELL NECROSIS; OXIDATIVE STRESS; PATHOGENESIS; POLYMORPHONUCLEAR CELL; POSITIVE END EXPIRATORY PRESSURE; PRACTICE GUIDELINE; PROTEIN EXPRESSION; PULMONARY ARTERY CATHETER; REVIEW; SEPSIS; SEPTIC CARDIOMYOPATHY; SEPTIC SHOCK; SYSTEMIC VASCULAR RESISTANCE; TACHYCARDIA; TIDAL VOLUME; TISSUE DOPPLER IMAGING; TREATMENT DURATION; TREATMENT INDICATION; TREATMENT RESPONSE; VENOUS RETURN; COMPLICATION; DIAGNOSIS; ETIOLOGY; HEART LEFT VENTRICLE FUNCTION; HEART RIGHT VENTRICLE FUNCTION; HEMODYNAMICS; METABOLISM; PULMONARY ARTERY CATHETERIZATION; SHOCK, SEPTIC; THERAPY;

CATHETERIZATION, SWAN-GANZ; ECHOCARDIOGRAPHY; HEMODYNAMICS; HUMANS; MITOCHONDRIAL DISEASES; OXIDATIVE STRESS; SEPSIS; SHOCK, SEPTIC; VASOCONSTRICTOR AGENTS; VENTRICULAR DYSFUNCTION, LEFT; VENTRICULAR DYSFUNCTION, RIGHT;

EID: 84902279045     PISSN: 08839441     EISSN: 15578615     Source Type: Journal    
DOI: 10.1016/j.jcrc.2014.03.028     Document Type: Review

References (149)

1. Martin G.S., Mannino D.M., Moss M. The effect of age on the development and outcome of adult sepsis. Crit Care Med 2006, 34:15-21.
2. Dombrovskiy V.Y., Martin A.A., Sunderram J., Paz H.L. Rapid increase in hospitalization and mortality rates for severe sepsis in the United States: a trend analysis from 1993 to 2003. Crit Care Med 2007, 35:1244-1250.
3. Parker M.M., Shelhamer J.H., Bacharach S.L., et al. Profound but reversible myocardial depression in patients with septic shock. Ann Intern Med 1984, 100:483-490.
4. Suffredini A.F., Fromm R.E., Parker M.M., et al. The cardiovascular response of normal humans to the administration of endotoxin. N Engl J Med 1989, 321:280-287.
5. Hochstadt A., Meroz Y., Landesberg G. Myocardial dysfunction in severe sepsis and septic shock: more questions than answers?. J Cardiothorac Vasc Anesth 2011, 25:526-535.
6. Vieillard-Baron A. Septic cardiomyopathy. Ann Intensive Care 2001, 1:6-7.
7. Repessé X., Charron C., Vieillard-Baron A. Evaluation of left ventricular systolic function revisited in septic shock. Crit Care 2013, 17:164-167.
8. McLean A.S. Down but not out: myocardial depression in sepsis. Crit Care 2012, 16:132-133.
9. De Backer D., Scolletta S. Clinical management of the cardiovascular failure in sepsis. Curr Vasc Pharmacol 2013, 11:222-242.
10. dos Santos C.C., Gattas D.J., Tsoporis J.N., et al. Sepsis-induced myocardial depression is associated with transcriptional changes in energy metabolism and contractile related genes: a physiological and gene expression based approach. Crit Care Med 2010, 38:894-902.
11. Lew W.Y., Yasuda S., Yuan T., et al. Endotoxin induced cardiac depression is associated with decreased cardiac dihydropyridine receptors in rabbits. J Mol Cell Cardiol 1996, 28:1367-1371.
12. Zhong J., Hwang T.C., Adams H.R., et al. Reduced L-type calcium current in ventricular myocytes from endotoxemic guinea pigs. Am J Physiol 1997, 273:2312-2324.
13. Stengl M., Bartak F., Sykora R., et al. Reduced L-type calcium current in ventricular myocytes from pigs with hyperdynamic septic shock. Crit Care Med 2010, 38:580-587.
14. Hsu C., Wu G., Yang S.L., et al. Intracellular redistribution of dihydropyridine receptor in the rat heart during the progression of sepsis. J Surg Res 2007, 141:146-152.
15. Wu S.N., Lue S.I., Yang S.L., et al. Electrophysiologic properties of isolated adult cardiomyocytes from septic rats. Circ Shock 1993, 41:239-247.
16. Kirkeboen K.A., Strand O.A. The role of nitric oxide in sepsis: an overview. Acta Anaesthesiol Scand 1999, 43:275-288.
17. Barth E., Radermacher P., Thiemermann C., et al. Role of inducible nitric oxide synthase in the reduced responsiveness of the myocardium to catecholamines in a hyperdynamic, murine model of septic shock. Crit Care Med 2006, 34:307-313.
18. Geoghegan-Morphet N., Burger D., Lu X., et al. Role of neuronal nitric oxide synthase in lipopolysaccharide-induced tumor necrosis factor-alpha expression in neonatal mouse cardiomyocytes. Cardiovasc Res 2007, 75:408-416.
19. Brealey D., Karyampudi S., Jacques T.S., et al. Mitochondrial dysfunction in a long-term rodent model of sepsis and organ failure. Am J Physiol Regul Integr Comp Physiol 2004, 286:491-497.
20. Xu C., Yi C., Wang H., Bruce I.C., et al. Mitochondrial nitric oxide synthase participates in septic shock myocardial depression by nitric oxide overproduction and mitochondrial permeability transition pore opening. Shock 2012, 37:110-115.
21. Fernandes C.J., de Assuncao M.S. Myocardial dysfunction in sepsis: a large, unsolved puzzle. Crit Care Res Pract 2012, 10.1155/2012/896430.
22. Sharma A.C., Motew S.J., Farias S., et al. Sepsis alters myocardial and plasma concentrations of endothelin and nitricoxide in rats. J Mol Cell Cardiol 1997, 29:1469-1477.
23. Chopra M., Sharma A.C. Distinct cardiodynamic and molecular characteristics during early and late stages of sepsis induced myocardial dysfunction. Life Sci 2007, 81:306-316.
24. Vincent J.L., Bakker J., Marécaux G., et al. Administration of anti-TNF antibody improves left ventricular function in septic shock patients. Results of a pilot study. Chest 1992, 101:810-815.
25. Abraham E., Wunderink R., Silverman H., et al. Efficacy and safety of monoclonal antibody to human tumor necrosis factor α in patients with sepsis syndrome: a randomized, controlled, double-blind, multicenter clinical trial. J Am Med Assoc 1995, 273:934-941.
26. Bujak M., Frangogiannis N.G. The role of IL-1 in the pathogenesis of heart disease. Arch Immunol Ther Exp 2009, 57:165-176.
27. Pathan N., Franklin J.L., Eleftherohorinou H., et al. Myocardial depressant effects of interleukin 6 in meningococcal sepsis are regulated by p38 mitogen-activated protein kinase. Crit Care Med 2011, 39:1692-1711.
28. Kimmoun A., Levy B. Treatment of myocardial dysfunction in sepsis: the toll-like receptor antagonist approach. Shock 2011, 36:633-634.
29. Gao M., Ha T., Zhang X., et al. Toll-like receptor 3 plays a central role in cardiac dysfunction during polymicrobial sepsis. Crit Care Med 2012, 40:1-10.
30. Cunnion R.E., Schaer G.L., Parker M.M., et al. The coronary circulation in human septic shock. Circulation 1986, 73:637-644.
31. Groeneveld A.B., van Lambalgen A.A., van den Bos G.C., et al. Maldistribution of heterogeneous coronary blood flow during canine endotoxin shock. Cardiovasc Res 1991, 25:80-88.
32. Levy R.J., Vijayasarathy C., Raj N.R., et al. Competitive and noncompetitive inhibition of myocardial cytochrome C oxidase in sepsis. Shock 2004, 21:110-114.
33. Scolletta S., Biagioli B. Energetic myocardial metabolism and oxidative stress: let's make them our friends in the fight against heart failure. Biomed Pharmacother 2010, 64:203-207.
34. Wang F., Pan W., Wang H., et al. Relationship between thyroid function and ICU mortality: a prospective observation study. Crit Care 2012, 16:R11-R19.
35. Calvano S.E., Xiao W., Richards D.R., et al. A network-based analysis of systemic inflammation in humans. Nature 2005, 437:1032-1037.
36. Carré J.E., Orban J.C., Re L., et al. Survival in critical illness is associated with early activation of mitochondrial biogenesis. Am J Respir Crit Care Med 2010, 182:745-751.
37. Galley F.H. Oxidative stress and mitochondrial dysfunction in sepsis. Br J Anaesth 2011, 107:57-64.
38. Singer M. The role of mitochondrial dysfunction in sepsis-induced multi-organ failure. Virulence 2013, 1:66-72.
39. Beurskens C.J.P., Aslami H., Kuipers M.T., et al. Induced hypothermia is protective in a rat model of pneumococcal pneumonia associated with increased adenosine triphosphate availability and turnover. Crit Care Med 2012, 40:919-926.
40. MacGarvey N.C., Suliman H.B., Bartz R.R., et al. Finally, activation of mitochondrial biogenesis by heme oxygenase-1-mediated NF-E2-related factor-2 induction rescues mice from lethal Staphylococcus aureus sepsis. Am J Respir Crit Care Med 2012, 185:851-861.
41. Sharshar T., Annane D., de la Grandmaison G.L., et al. The neuropathology of septic shock. Brain Pathol 2004, 14:21-33.
42. Sharshar T., Gray F., Lorin de la Grandmaison G., et al. Apoptosis of neurons in cardiovascular autonomic centres triggered by inducible nitric oxide synthase after death from septic shock. Lancet 2003, 362:1799-1805.
43. Cariou A., Pinsky M.R., Monchi M., et al. Is myocardial adrenergic responsiveness depressed in human septic shock?. Intensive Care Med 2008, 34:917-922.
44. Smeding L., Plötz F.B., Groeneveld A.B., et al. Structural changes of the heart during severe sepsis or septic shock. Shock 2012, 37:449-456.
45. Schouten M., Wiersinga W.J., Levi M., et al. Inflammation, endothelium, and coagulation in sepsis. J Leukoc Biol 2008, 83:536-545.
46. Buerke U., Carter J.M., Schlitt A., et al. Apoptosis contributes to septic cardiomyopathy and is improved by simvastatin therapy. Shock 2008, 29:497-503.
47. Celes M.R., Torres-Dueñas D., Malvestio L.M., et al. Disruption of sarcolemmal dystrophin and beta-dystroglycan may be a potential mechanism for myocardial dysfunction in severe sepsis. Lab Invest 2010, 90:531-542.
48. Rabuel C., Mebazaa A. Septic shock: a heart story since the1960s. Intensive Care Med 2006, 32:799-807.
49. Brandt S., Regueira T., Bracht H., et al. Effect of fluid resuscitation on mortality and organ function in experimental sepsis models. Crit Care 2009, 13:R186-R197.
50. O'Dwyer S.T., Michie H.R., Ziegler T.R., et al. A single dose of endotoxin increases intestinal permeability in healthy humans. Arch Surg 1988, 123:1459-1464.
51. Fink M.P., Antonsson J.B., Wang H., et al. Increased intestinal permeability in endotoxic pigs. Arch Surg 1991, 126:211-218.
52. Pinsky M.R., Matuschak G.M. Cardiovascular determinants of the hemodynamic response to acute endotoxemia in the dog. J Crit Care 1986, 1:18-31.
53. Brienza N., Ayuse T., Revelly J.P., et al. Effects of endotoxin on isolated porcine liver: pressure-flow analysis. J Appl Physiol 1995, 78:784-792.
54. Stephan F., Novara A., Tournier B., et al. Determination of total effective vascular compliance in patients with sepsis syndrome. Am J Respir Crit Care Med 1998, 157:50-56.
55. Annane D., Bellissant E., Sebille V., et al. Impaired pressor sensitivity to noradrenaline in septic shock patients with and without impaired adrenal function reserve. Br J Clin Pharmacol 1998, 46:589-597.
56. Umans J.G., Wylam M.E., Samsel R.W., et al. Effects of endotoxin in vivo on endothelial and smooth-muscle function in rabbit and rat aorta. Am Rev Respir Dis 1993, 148:1638-1645.
57. Levy B., Collin S., Sennoun N., et al. Vascular hyporesponsiveness to vasopressors in septic shock: from bench to bedside. Intensive Care Med 2010, 36:2019-2029.
58. Bucher M., Hobbhahn J., Taeger K., et al. Cytokine-mediated downregulation of vasopressin V(1A) receptors during acute endotoxemia in rats. Am J Physiol Regul Integr Comp Physiol 2002, 282:979-984.
59. Hamu Y., Kanmura Y., Tsuneyoshi I., et al. The effects of vasopressin on endotoxin-induced attenuation of contractile responses in human gastroepiploic arteries in vitro. Anesth Analg 1999, 88:542-548.
60. Julou-Schaeffer G., Gray G.A., Fleming I., et al. Loss of vascular responsiveness induced by endotoxin involves l-arginine pathway. Am J Physiol 1990, 259:1038-1043.
61. Boyle W.A., Parvathaneni L.S., Bourlier V., et al. iNOS gene expression modulates microvascular responsiveness in endotoxin-challenged mice. Circ Res 2000, 87:18-24.
62. Kooy N.W., Royall J.A. Agonist-induced peroxynitrite production from endothelial cells. Arch Biochem Biophys 1994, 310:352-359.
63. Salvemini D., Wang Z.Q., Zweier J.L., et al. A nonpeptidyl mimic of superoxide dismutase with therapeutic activity in rats. Science 1999, 286:304-306.
64. Hocherl K., Schmidt C., Kurt B., et al. Activation of the PGI(2)/IP system contributes to the development of circulatory failure in a rat model of endotoxic shock. Hypertension 2008, 52:330-335.
65. Landry D.W., Oliver J.A. The ATP-sensitive K+ channel mediates hypotension in endotoxemia and hypoxic lactic acidosis in dog. J Clin Invest 1992, 89:2071-2074.
66. Croner R.S., Hoerer E., Kulu Y., et al. Hepatic platelet and leukocyte adherence during endotoxemia. Crit Care 2006, 10:R15-R21.
67. De Backer D., Creteur J., Preiser J.C., et al. Microvascular blood flow is altered in patients with sepsis. Am J Respir Crit Care Med 2002, 166:98-104.
68. Marechal X., Favory R., Joulin O., et al. Endothelial glycocalyx damage during endotoxemia coincides with microcirculatory dysfunction and vascular oxidative stress. Shock 2008, 29:572-576.
69. Piagnerelli M., Boudjeltia K.Z., Vanhaeverbeek M., et al. Red blood cell rheology in sepsis. Intensive Care Med 2003, 29:1052-1061.
70. Taccone F.S., Su F., Pierrakos C., et al. Cerebral microcirculation is impaired during sepsis: an experimental study. Crit Care 2010, 14:R40-R150.
71. Trzeciak S. 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, 34:2210-2217.
72. Vincent J.L., De Backer D. Oxygen transport-the oxygen delivery controversy. Intensive Care Med 1990-1996, 2004:30.
73. Budinger G.R.S., Chandel N., Shao Z.H., et al. Cellular energy utilization and supply during hypoxia in embryonic cardiac myocytes. Am J Physiol 1996, 270:44-53.
74. Nichol A.D., Egi M., Pettila V., et al. Relative hyperlactatemia and hospital mortality in critically ill patients: a retrospective multi-centre study. Crit Care 2010, 14:R25-R34.
75. Bakker J., Gris P., Coffernils M., et al. Serial blood lactate levels can predict the development of multiple organ failure following septic shock. Am J Surg 1996, 171:221-226.
76. Luecke T., Pelosi P. Clinical review: positive end-expiratory pressure and cardiac output. Crit Care 2005, 9:607-621.
77. Fougères E., Teboul J.L., Richard C., et al. Hemodynamic impact of a positive end-expiratory pressure setting in acute respiratory distress syndrome: importance of volume status. Crit Care Med 2010, 38:802-807.
78. Dellinger R.P., Levy M.M., Rhodes A., et al. Surviving Sepsis Campaign: international guidelines for management of severe sepsis and septic shock: 2012. Crit Care Med 2013, 41:580-637.
79. Pinsky M.R. Cardiovascular issues in respiratory care. Chest 2005, 128:592-597.
80. Roosens C.D., Ama R., Leather H.A., et al. Hemodynamic effects of different lung-protective ventilation strategies in closed-chest pigs with normal lungs. Crit Care Med 2006, 34:2990-2996.
81. Boissier F., Katsahian S., Razazi K., et al. Prevalence and prognosis of cor pulmonale during protective ventilation for acute respiratory distress syndrome. Intensive Care Med 2013, 39:1725-1733.
82. Etchecopar-Chevreuil C., Franĉois B., Clavel M., et al. Cardiac morphological and functional changes during early septic shock: a transesophageal echocardiographic study. Intensive Care Med 2008, 34:250-256.
83. Jardin F., Brun-Ney D., Auvert B., et al. Sepsis-related cardiogenic shock. Crit Care Med 1990, 18:1055-1060.
84. Vieillard-Baron A., Caille V., Charron C., et al. Actual incidence of global left ventricular hypokinesia in adult septic shock. Crit Care Med 2008, 36:1701-1706.
85. Vieillard-Baron A., Schmitt J.M., Beauchet A., et al. Early preload adaptation in septic shock? A transesophageal echocardiographic study. Anesthesiology 2001, 94:400-406.
86. Chantler P.D., Lakatta E.G., Najjar S.S. Arterial-ventricular coupling: mechanistic insights into cardiovascular performance at rest and during exercise. J Appl Physiol 2008, 105:1342-1351.
87. Guarracino F., Baldassarri R., Pinsky M.R. Ventriculo-arterial decoupling in acutely altered hemodynamic states. Crit Care 2013, 17:213-220.
88. Chen C.H., Fetics B., Nevo E., et al. Noninvasive single-beat determination of left ventricular end-systolic elastance in humans. J Am Coll Cardiol 2001, 38:2028-2034.
89. Guarracino F., Cariello C., Danella A., et al. Effect of levosimendan on ventriculo-arterial coupling in patients with ischemic cardiomyopathy. Acta Anaesthesiol Scand 2007, 51:1217-1224.
90. Scolletta S., Bodson L., Donadello K., et al. Assessment of left ventricular function by pulse wave analysis in critically ill patients. Intensive Care Med 2013, 39:1025-1033.
91. Poelaert J., Declerck C., Vogelaers D., et al. Left ventricular systolic and diastolic function in septic shock. Intensive Care Med 1997, 23:553-560.
92. Munt B., Jue J., Gin K., et al. Diastolic filling in human severe sepsis: an echocardiographic study. Crit Care Med 1829-1833, 1998:26.
93. Bouhemad B., Nicolas-Robin A., Arbelot C., et al. Isolated and reversible impairment of ventricular relaxation in patients with septic shock. Crit Care Med 2008, 36:766-777.
94. Marthu M., Pollard V., He G., et al. Left ventricular diastolic filling characteristics are not impaired but systolic performance was augmented in the early hours of experimental endotoxemia in humans. Shock 2006, 25:338-343.
95. Landesberg G., Gilon D., Meroz Y., et al. Diastolic dysfunction and mortality in severe sepsis and septic shock. Eur Heart J 2012, 33:895-903.
96. Hoffman M.J., Lazar J.G., Sugerman H.F., et al. Unsuspected right ventricular dysfunction in shock and sepsis. Ann Surg 1983, 198:307-318.
97. Schneider A.J., Teule G.J., Groeneveld A.B., et al. Biventricular performance during volume loading in patients with early septic shock, with emphasis on the right ventricle: a combined hemodynamic and radionuclide study. Am Heart J 1988, 116:103-112.
98. Parker M.M., McCArthy K.E., Ognibene F.P., et al. Right ventricular dysfunction and dilatation, similar to left ventricular changes, characterize the cardiac depression of septic shock in humans. Chest 1990, 97:126-131.
99. Vincent J.L., Reuse C., Frank N., et al. Right ventricular dysfunction in septic shock: assessment by measurements using the thermodilution technique. Acta Anaesthesiol Scand 1989, 33:34-38.
100. Furian T., Aguiar C., Prado K., et al. Ventricular dysfunction and dilation in severe sepsis and septic shock: relation to endothelial function and mortality. J Crit Care 2011, 27:319-325.
101. Sanz J., García-Alvarez A., Fernández-Friera L., et al. Right ventriculo-arterial coupling in pulmonary hypertension: a magnetic resonance study. Heart 2012, 98:238-243.
102. Rajaram S.S., Desai N.K., Kalra A., et al. Pulmonary artery catheters for adult patients in intensive care. Cochrane Database Syst Rev 2013, 2:1-59.
103. Vincent J.L., Rhodes A., Perel A., et al. Clinical review: update on hemodynamic monitoring-a consensus of 16. Crit Care 2011, 15:229-237.
104. Ho C.Y., Solomon S.D. A clinician's guide to tissue Doppler imaging. Circulation 2006, 113:396-398.
105. Dokainish H., Zoghbi W.A., Lakkis N.M., et al. Incremental predictive power of B-type natriuretic peptide and tissue Doppler echocardiography in the prognosis of patients with congestive heart failure. J Am Coll Cardiol 2005, 45:1223-1226.
106. Nikitin N.P., Loh P.H., Silva R., et al. Prognostic value of systolic mitral annular velocity measured with Doppler tissue imaging in patients with chronic heart failure caused by left ventricular systolic dysfunction. Heart 2006, 92:775-779.
107. Abdel-Hady H.E., Matter M.K., El-Arman M.M. Myocardial dysfunction in neonatal sepsis: a tissue Doppler imaging study. Pediatr Crit Care Med 2012, 13:318-323.
108. Weng L., Liu Y.T., Du B., Zhou J.F., Guo X.X., et al. The prognostic value of left ventricular systolic function measured by tissue Doppler imaging in septic shock. Crit Care 2012, 16:R71-R79.
109. A'roch R., Gustafsson U., Johansson G., et al. Left ventricular strain and peak systolic velocity: responses to controlled changes in load and contractility, explored in a porcine model. Cardiovasc Ultrasound 2012, 10:22-31.
110. Sado D., Greaves K. Myocardial perfusion echocardiography: a novel use in the diagnosis of sepsis-induced left ventricular systolic impairment on the intensive care unit. Eur J Echocardiogr 2011, 12:81-84.
111. Varpula M., Tallgren M., Saukkonen K., et al. Hemodynamic variables related to outcome in septic shock. Intensive Care Med 2005, 31:1066-1071.
112. Rivers E., Nguyen B., Havstad S., et al. Early goal-directed therapy in the treatment of severe sepsis and septic shock. N Engl J Med 2001, 345:1368-1377.
113. Pinsky M.R., Vincent J.L. Let us use the pulmonary artery catheter correctly and only when we need it. Crit Care Med 2005, 33:1119-1122.
114. Velissaris D., Pierrakos C., Scolletta S., et al. High mixed venous oxygen saturation levels do not exclude fluid responsiveness in critically ill septic patients. Crit Care 2011, 15:R177-R183.
115. 2 Collaborative Group. N Engl J Med 1995, 333:1025-1032.
116. Heyland D.K., Cook D.J., King D., et al. Maximizing oxygen delivery in critically ill patients: a methodologic appraisal of the evidence. Crit Care Med 1996, 24:517-524.
117. Hogue B., Chagnon F., Lesur O. Resuscitation fluids and endotoxin-induced myocardial dysfunction: is selection a load-independent differential issue?. Shock 2012, 38:307-313.
118. Hayes M.A., Timmins A.C., Yau E.H., et al. Elevation of systemic oxygen delivery in the treatment of critically ill patients. N Engl J Med 1994, 330:1717-1722.
119. De Backer D., Creteur J., Dubois M.J., et al. The effects of dobutamine on microcirculatory alterations in patients with septic shock are independent of its systemic effects. Crit Care Med 2006, 34:403-408.
120. Enrico C., Kanoore Edul V.S., Vazquez A.R., et al. Systemic and microcirculatory effects of dobutamine in patients with septic shock. J Crit Care 2012, 27:630-638.
121. Joly L.M., Monchi M., Cariou A., et al. Effects of dobutamine on gastric mucosal perfusion and hepatic metabolism in patients with septic shock. Am J Respir Crit Care Med 1999, 160:1983-1986.
122. Levy B., Bollaert P.E., Lucchelli J.P., et al. Dobutamine improves the adequacy of gastric mucosal perfusion in epinephrine-treated septic shock. Crit Care Med 1997, 25:1649-1654.
123. Silverman H.J., Tuma P. Gastric tonometry in patients with sepsis. Effects of dobutamine infusions and packed red blood cell transfusions. Chest 1992, 102:184-188.
124. Lebuffe G., Levy B., Neviere R., et al. Dobutamine and gastric-to-arterial carbon dioxide gap in severe sepsis without shock. Intensive Care Med 2002, 28:265-271.
125. Morelli A., De Castro S., Teboul J.L., et al. Effects of levosimendan on systemic and regional hemodynamics in septic myocardial depression. Intensive Care Med 2005, 31:638-644.
126. Kumar A., Roberts D., Wood K.E., et al. Duration of hypotension prior to initiation of effective antimicrobial therapy is the critical determinant of survival in human septic shock. Crit Care Med 2006, 34:1589-1596.
127. Hartemink K.J., Groeneveld A.B. Vasopressors and inotropes in the treatment of human septic shock: effect on innate immunity?. Inflammation 2012, 35:206-213.
128. Chew M.S., Hawthorne W.J., Bendall J., et al. No beneficial effects of levosimendan in acute porcine endotoxaemia. Acta Anaesthesiol Scand 2011, 55:851-861.
129. Parissis J.T., Andreadou I., Bistola V., et al. Novel biologic mechanisms of levosimendan and its effect on the failing heart. Expert Opin Investig Drugs 2008, 17:1143-1150.
130. Hasslacher J., Bijuklic K., Bertocchi C., et al. Levosimendan inhibits release of reactive oxygen species in polymorphonuclear leukocytes in vitro and in patients with acute heart failure and septic shock: a prospective observational study. Crit Care 2011, 15:R166-R176.
131. Barraud D., Faivre V., Damy T., et al. Levosimendan restores doth systolic and diastolic cardiac performance in lipopolysaccharide-treated rabbits: comparison with dobutamine and milrinone. Crit Care Med 2007, 35:1376-1382.
132. Fries M., Ince C., Rossaint R., et al. Levosimendan but not norepinephrine improves microvascular oxygenation during experimental septic shock. Crit Care Med 1886-1891, 2008:36.
133. Morelli A., Donati A., Ertmer C., et al. Levosimendan for resuscitating the microcirculation in patients with septic shock: a randomized controlled study. Crit Care 2010, 14:R232.
134. Avgeropoulou C., Andreadou I., Markantonis-Kyroudis S., et al. The Ca-sensitizer levosimendan improves oxidative damage, BNP and pro-inflammatory cytokine levels in patients with advanced decompensated heart failure in comparison to dobutamine. Eur J Heart Fail 2005, 7:882-887.
135. Annane D., Vignon P., Renault A., et al. Norepinephrine plus dobutamine versus epinephrine alone for management of septic shock: a randomised trial. Lancet 2007, 370:676-684.
136. Myburgh J.A., Higgins A., Jovanovska A., et al. A comparison of epinephrine and norepinephrine in critically ill patients. Intensive Care Med 2008, 34:2226-2234.
137. Levy B., Perez P., Perny J., et al. Comparison of norepinephrine-dobutamine to epinephrine for hemodynamics, lactate metabolism, and organ function variables in cardiogenic shock. A prospective, randomized pilot study. Crit Care Med 2011, 39:450-455.
138. Sakr Y., Reinhart K., Vincent J.L., et al. Does dopamine administration in shock influence outcome? Results of the Sepsis Occurrence in Acutely Ill Patients (SOAP) study. Crit Care Med 2006, 34:589-597.
139. Vasu T.S., Cavallazzi R., Hirani A., et al. Norepinephrine or dopamine for septic shock: a systematic review of randomized clinical trials. J Intensive Care Med 2011, 27:172-178.
140. De Backer D., Biston P., Devriendt J., et al. Comparison of dopamine and norepinephrine in the treatment of shock. N Engl J Med 2010, 362:779-789.
141. De Backer D., Aldecoa C., Njimi H., et al. Dopamine versus norepinephrine in the treatment of septic shock: a meta-analysis. Crit Care Med 2012, 40:725-730.
142. Patel B.M., Chittock D.R., Russell J.A., et al. Beneficial effects of short-term vasopressin infusion during severe septic shock. Anesthesiology 2002, 96:576-582.
143. Klinzing S., Simon M., Reinhart K., et al. High-dose vasopressin is not superior to norepinephrine in septic shock. Crit Care Med 2003, 31:2646-2650.
144. Dunser M.W., Mayr A.J., Ulmer H., et al. The effects of vasopressin on systemic hemodynamics in catecholamine-resistant septic and postcardiotomy shock: a retrospective analysis. Anesth Analg 2001, 93:7-13.
145. Serpa Neto A., Nassar A.P., Cardoso S.O., et al. Vasopressin and terlipressin in adult vasodilatory shock: a systematic review and meta-analysis of nine randomized controlled trials. Crit Care 2012, 16:R154-R164.
146. Tenover F.C. Rapid detection and identification of bacterial pathogens using novel molecular technologies: infection control and beyond. Clin Infect Dis 2007, 44:418-423.
147. Bellissant E., Annane D. Effect of hydrocortisone on phenylephrine-mean arterial pressure dose-response relationship in septic shock. Clin Pharmacol Ther 2000, 68:293-303.
148. Boonen E., Vervenne H., Meersseman P., et al. Reduced cortisol metabolism during critical illness. N Engl J Med 2013, 368:1477-1488.
149. Morelli A., Ertmer C., Westphal M., et al. Effect of heart rate control with esmolol on hemodynamic and clinical outcomes in patients with septic shock: a randomized clinical trial. JAMA 2013, 310:1683-1691.