Endotoxin impairs cardiac hemodynamics by affecting loading conditions but not by reducing cardiac inotropism

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 299, Issue 2, 2010, Pages

  Jianhui, Li ^a,b   Rosenblatt Velin, Nathalie ^a   Loukili, Noureddine ^a   Pacher, Pal ^c   Feihl, François ^a   Waeber, Bernard ^a   Liaudet, Lucas ^a  

^a LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^b ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

^c NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM   (United States)

Author keywords

Cardiac function; Contractility; Mice

Indexed keywords

ENDOTOXIN; LIPOPOLYSACCHARIDE;

ACUTE HEART INFARCTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ARTIFICIAL VENTILATION; CONTROLLED STUDY; DIASTOLE; ELASTICITY; HEART AFTERLOAD; HEART EJECTION FRACTION; HEART FUNCTION; HEART HEMODYNAMICS; HEART LEFT VENTRICLE DP-DT; HEART LEFT VENTRICLE PRESSURE; HEART LEFT VENTRICLE VOLUME; HEART MUSCLE CONTRACTILITY; HEART OUTPUT; HEART PRELOAD; HEART STROKE VOLUME; INOTROPISM; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SEPTIC SHOCK; SYSTEMIC VASCULAR RESISTANCE; SYSTOLE;

ANIMALS; ARTERIES; CARDIOMYOPATHIES; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ELASTICITY; ENDOTOXEMIA; ENDOTOXINS; HEART CATHETERIZATION; HEART RATE; INJECTIONS, INTRAPERITONEAL; MALE; MICE; MICE, INBRED BALB C; MODELS, CARDIOVASCULAR; MYOCARDIAL CONTRACTION; STROKE VOLUME; TIME FACTORS; VASCULAR RESISTANCE; VENTRICULAR FUNCTION, LEFT; VENTRICULAR PRESSURE;

EID: 77955459365     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.01135.2009     Document Type: Article

References (58)

1. Baan J, van der Velde ET, de Bruin HG, Smeenk GJ, Koops J, van Dijk AD, Temmerman D, Senden J, Buis B. Continuous measurement of left ventricular volume in animals and humans by conductance catheter. Circulation 70: 812-823, 1984. (Pubitemid 15205446)
2. Barraud D, Faivre V, Damy T, Welschbillig S, Gayat E, Heymes C, Payen D, Shah AM, Mebazaa A. Levosimendan restores both systolic and diastolic cardiac performance in lipopolysaccharide-treated rabbits: comparison with dobutamine and milrinone. Crit Care Med 35: 1376-1382, 2007.
3. Batkai S, Pacher P, Jarai Z, Wagner JA, Kunos G. Cannabinoid antagonist SR-141716 inhibits endotoxic hypotension by a cardiac mechanism not involving CB1 or CB2 receptors. Am J Physiol Heart Circ Physiol 287: H595-H600, 2004.
4. Boltwood CM Jr, Appleyard RF, Glantz SA. Left ventricular volume measurement by conductance catheter in intact dogs. Parallel conductance volume depends on left ventricular size. Circulation 80: 1360-1377, 1989.
5. Boyd JH, Kan B, Roberts H, Wang Y, Walley KR. S100A8 and S100A9 mediate endotoxin-induced cardiomyocyte dysfunction via the receptor for advanced glycation end products. Circ Res 102: 1239-1246, 2008.
6. Buys ES, Cauwels A, Raher MJ, Passeri JJ, Hobai I, Cawley SM, Rauwerdink KM, Thibault H, Sips PY, Thoonen R, Scherrer-Crosbie M, Ichinose F, Brouckaert P, Bloch KD. sGCα1β1 attenuates cardiac dysfunction and mortality in murine inflammatory shock models. Am J Physiol Heart Circ Physiol 297: H654-H663, 2009.
7. Chirinos JA, Rietzschel ER, De Buyzere ML, De Bacquer D, Gillebert TC, Gupta AK, Segers P. Arterial load and ventricular-arterial coupling: physiologic relations with body size and effect of obesity. Hypertension 54: 558-566, 2009.
8. Cholley BP, Lang RM, Berger DS, Korcarz C, Payen D, Shroff SG. Alterations in systemic arterial mechanical properties during septic shock: role of fluid resuscitation. Am J Physiol Heart Circ Physiol 269: H375-H384, 1995.
9. Claessens TE, Georgakopoulos D, Afanasyeva M, Vermeersch SJ, Millar HD, Stergiopulos N, Westerhof N, Verdonck PR, Segers P. Nonlinear isochrones in murine left ventricular pressure-volume loops: how well does the time-varying elastance concept hold? Am J Physiol Heart Circ Physiol 290: H1474-H1483, 2006.
10. Constable PD. Acute endotoxemia increases left ventricular contractility and diastolic stiffness in calves. Shock 12: 391-401, 1999.
11. Davani EY, Boyd JH, Dorscheid DR, Wang Y, Meredith A, Chau E, Singhera GK, Walley KR. Cardiac ICAM-1 mediates leukocyte-dependent decreased ventricular contractility in endotoxemic mice. Cardiovasc Res 72: 134-142, 2006.
12. Fishman D, Liaudet L, Lazor R, Perret CH, Feihl F. L-canavanine, an inhibitor of inducible nitric oxide synthase, improves venous return in endotoxemic rats. Crit Care Med 25: 469-475, 1997.
13. Freeman GL, Little WC, O'Rourke RA. Influence of heart rate on left ventricular performance in conscious dogs. Circ Res 61: 455-464, 1987.
14. Hollenberg SM. Mouse models of resuscitated shock. Shock 24, Suppl 1: 58-63, 2005.
15. Hunter JD, Doddi M. Sepsis and the heart. Br J Anaesth 104: 3-11, 2010.
16. Ichinose F, Buys ES, Neilan TG, Furutani EM, Morgan JG, Jassal DS, Graveline AR, Searles RJ, Lim CC, Kaneki M, Picard MH, Scherrer- Crosbie M, Janssens S, Liao R, Bloch KD. Cardiomyocyte-specific overexpression of nitric oxide synthase 3 prevents myocardial dysfunction in murine models of septic shock. Circ Res 100: 130-139, 2007.
17. Kass DA, Maughan WL, Guo ZM, Kono A, Sunagawa K, Sagawa K. Comparative influence of load versus inotropic states on indexes of ventricular contractility: experimental and theoretical analysis based on pressure-volume relationships. Circulation 76: 1422-1436, 1987.
18. Knuefermann P, Nemoto S, Misra A, Nozaki N, Defreitas G, Goyert SM, Carabello BA, Mann DL, Vallejo JG. CD14-deficient mice are protected against lipopolysaccharide-induced cardiac inflammation and left ventricular dysfunction. Circulation 106: 2608-2615, 2002.
19. Kober PM, Thomas JX Jr, Raymond RM. Increased myocardial contractility during endotoxin shock in dogs. Am J Physiol Heart Circ Physiol 249: H715-H722, 1985.
20. Kumar A, Bunnell E, Lynn M, Anel R, Habet K, Neumann A, Parrillo JE. Experimental human endotoxemia is associated with depression of load-independent contractility indices: prevention by the lipid a analogue E5531. Chest 126: 860-867, 2004.
21. Lancel S, Petillot P, Favory R, Stebach N, Lahorte C, Danze PM, Vallet B, Marchetti P, Neviere R. Expression of apoptosis regulatory factors during myocardial dysfunction in endotoxemic rats. Crit Care Med 33: 492-496, 2005.
22. Landry DW, Oliver JA. The pathogenesis of vasodilatory shock. N Engl J Med 345: 588-595, 2001.
23. Lanoye L, Segers P, Tchana-Sato V, Rolin S, Dogne JM, Ghuysen A, Lambermont B, Hanson J, Desaive T, Verdonck P, D'Orio V, Kolh P. Cardiovascular haemodynamics and ventriculo-arterial coupling in an acute pig model of coronary ischaemia-reperfusion. Exp Physiol 92: 127-137, 2007.
24. Liaudet L, Feihl F, Rosselet A, Markert M, Hurni JM, Perret C. Beneficial effects of L-canavanine, a selective inhibitor of inducible nitric oxide synthase, during rodent endotoxaemia. Clin Sci (Lond) 90: 369-377, 1996.
25. Losser MR, Forget AP, Payen D. Nitric oxide involvement in the hemodynamic response to fluid resuscitation in endotoxic shock in rats. Crit Care Med 34: 2426-2431, 2006.
26. Magder S, Vanelli G. Circuit factors in the high cardiac output of sepsis. J Crit Care 11: 155-166, 1996.
27. Mahieu T, Park JM, Revets H, Pasche B, Lengeling A, Staelens J, Wullaert A, Vanlaere I, Hochepied T, van Roy F, Karin M, Libert C. The wild-derived inbred mouse strain SPRET/Ei is resistant to LPS and defective in IFN-beta production. Proc Natl Acad Sci U S A 103: 2292-2297, 2006.
28. Mathru M, Pollard V, He G, Varma TK, Ahmad M, Prough DS. Left ventricular diastolic filling characteristics are not impaired but systolic performance was augmented in the early hours of experimental endotoxemia in humans. Shock 25: 338-343, 2006.
29. Maughan WL, Sunagawa K, Burkhoff D, Graves WL Jr, Hunter WC, Sagawa K. Effect of heart rate on the canine end-systolic pressure-volume relationship. Circulation 72: 654-659, 1985.
30. Merx MW, Weber C. Sepsis and the heart. Circulation 116: 793-802, 2007.
31. Mulder MF, van Lambalgen AA, van den Bos GC, Thijs LG. The fall of cardiac output in endotoxemic rats cannot explain all changes in organ blood flow: a comparison between endotoxin and low venous return shock. Shock 5: 135-140, 1996.
32. Natanson C, Fink MP, Ballantyne HK, MacVittie TJ, Conklin JJ, Parrillo JE. Gram-negative bacteremia produces both severe systolic and diastolic cardiac dysfunction in a canine model that simulates human septic shock. J Clin Invest 78: 259-270, 1986.
33. Nemoto S, DeFreitas G, Mann DL, Carabello BA. Effects of changes in left ventricular contractility on indexes of contractility in mice. Am J Physiol Heart Circ Physiol 283: H2504-H2510, 2002.
34. Nemoto S, Vallejo JG, Knuefermann P, Misra A, Defreitas G, Carabello BA, Mann DL. Escherichia coli LPS-induced LV dysfunction: role of toll-like receptor-4 in the adult heart. Am J Physiol Heart Circ Physiol 282: H2316-H2323, 2002.
35. Nicholson SC, Hahn RT, Grobmyer SR, Brause JE, Hafner A, Potter S, Devereux RB, Nathan CF. Echocardiographic and survival studies in mice undergoing endotoxic shock: effects of genetic ablation of inducible nitric oxide synthase and pharmacologic antagonism of platelet-activating factor. J Surg Res 86: 198-205, 1999.
36. Nielsen JM, Kristiansen SB, Ringgaard S, Nielsen TT, Flyvbjerg A, Redington AN, Botker HE. Left ventricular volume measurement in mice by conductance catheter: evaluation and optimization of calibration. Am J Physiol Heart Circ Physiol 293: H534-H540, 2007.
37. Pacher P, Liaudet L, Bai P, Mabley JG, Kaminski PM, Virag L, Deb A, Szabo E, Ungvari Z, Wolin MS, Groves JT, Szabo C. Potent metalloporphyrin peroxynitrite decomposition catalyst protects against the development of doxorubicin-induced cardiac dysfunction. Circulation 107: 896-904, 2003.
38. Pacher P, Nagayama T, Mukhopadhyay P, Batkai S, Kass DA. Measurement of cardiac function using pressure-volume conductance catheter technique in mice and rats. Nat Protoc 3: 1422-1434, 2008.
39. Parker MM, Shelhamer JH, Bacharach SL, Green MV, Natanson C, Frederick TM, Damske BA, Parrillo JE. Profound but reversible myocardial depression in patients with septic shock. Ann Intern Med 100: 483-490, 1984.
40. Pinsky MR, Rico P. Cardiac contractility is not depressed in early canine endotoxic shock. Am J Respir Crit Care Med 161: 1087-1093, 2000.
41. Porterfield JE, Kottam AT, Raghavan K, Escobedo D, Jenkins JT, Larson ER, Trevino RJ, Valvano JW, Pearce JA, Feldman MD. Dynamic correction for parallel conductance, GP, and gain factor, α, in invasive murine left ventricular volume measurements. J Appl Physiol 107: 1693-1703, 2009.
42. Ricard-Hibon A, Losser MR, Kong R, Beloucif S, Teisseire B, Payen D. Systemic pressure-flow reactivity to norepinephrine in rabbits: impact of endotoxin and fluid loading. Intensive Care Med 24: 959-966, 1998.
43. Rivers E, Nguyen B, Havstad S, Ressler J, Muzzin A, Knoblich B, Peterson E, Tomlanovich M. Early goal-directed therapy in the treatment of severe sepsis and septic shock. N Engl J Med 345: 1368-1377, 2001.
44. Rosselet A, Feihl F, Markert M, Gnaegi A, Perret C, Liaudet L. Selective iNOS inhibition is superior to norepinephrine in the treatment of rat endotoxic shock. Am J Respir Crit Care Med 157: 162-170, 1998.
45. Rudiger A, Singer M. Mechanisms of sepsis-induced cardiac dysfunction. Crit Care Med 35: 1599-1608, 2007.
46. Sennoun N, Meziani F, Dessebe O, Cattan V, Collin S, Montemont C, Gibot S, Asfar P, Ramaroson A, Regnault V, Slama M, Lecompte T, Lacolley P, Levy B. Activated protein C improves lipopolysaccharide-induced cardiovascular dysfunction by decreasing tissular inflammation and oxidative stress. Crit Care Med 37: 246-255, 2009.
47. Senzaki H, Chen CH, Kass DA. Single-beat estimation of end-systolic pressure-volume relation in humans. A new method with the potential for noninvasive application. Circulation 94: 2497-2506, 1996.
48. Sodums MT, Badke FR, Starling MR, Little WC, O'Rourke RA. Evaluation of left ventricular contractile performance utilizing end-systolic pressure- volume relationships in conscious dogs. Circ Res 54: 731-739, 1984.
49. Suga H, Sagawa K. Instantaneous pressure-volume relationships and their ratio in the excised, supported canine left ventricle. Circ Res 35: 117-126, 1974.
50. Suga H, Sagawa K, Shoukas AA. Load independence of the instantaneous pressure-volume ratio of the canine left ventricle and effects of epinephrine and heart rate on the ratio. Circ Res 32: 314-322, 1973.
51. Szabo C, Mitchell JA, Thiemermann C, Vane JR. Nitric oxide-mediated hyporeactivity to noradrenaline precedes the induction of nitric oxide synthase in endotoxin shock. Br J Pharmacol 108: 786-792, 1993. (Pubitemid 23067954)
52. Tokunaga C, Bateman RM, Boyd J, Wang Y, Russell JA, Walley KR. Albumin resuscitation improves ventricular contractility and myocardial tissue oxygenation in rat endotoxemia. Crit Care Med 35: 1341-1347, 2007.
53. Ullrich R, Scherrer-Crosbie M, Bloch KD, Ichinose F, Nakajima H, Picard MH, Zapol WM, Quezado ZM. Congenital deficiency of nitric oxide synthase 2 protects against endotoxin-induced myocardial dysfunction in mice. Circulation 102: 1440-1446, 2000.
54. Wang X, Zingarelli B, O'Connor M, Zhang P, Adeyemo A, Kranias EG, Wang Y, Fan GC. Overexpression of Hsp20 prevents endotoxin-induced myocardial dysfunction and apoptosis via inhibition of NF-kappaB activation. J Mol Cell Cardiol 47: 382-390, 2009.
55. Wei CL, Valvano JW, Feldman MD, Nahrendorf M, Peshock R, Pearce JA. Volume catheter parallel conductance varies between endsystole and end-diastole. IEEE Trans Biomed Eng 54: 1480-1489, 2007.
56. Wei CL, Valvano JW, Feldman MD, Pearce JA. Nonlinear conductance- volume relationship for murine conductance catheter measurement system. IEEE Trans Biomed Eng 52: 1654-1661, 2005.
57. Witzenbichler B, Westermann D, Knueppel S, Schultheiss HP, Tschope C. Protective role of angiopoietin-1 in endotoxic shock. Circulation 111: 97-105, 2005.
58. You W, Min X, Zhang X, Qian B, Pang S, Ding Z, Li C, Gao X, Di R, Cheng Y, Liu L. Cardiac-specific expression of heat shock protein 27 attenuated endotoxin-induced cardiac dysfunction and mortality in mice through a PI3K/Akt-dependent mechanism. Shock 32: 108-117, 2009.