Fluid resuscitation therapy in endotoxemic hamsters improves survival and attenuates capillary perfusion deficits and inflammatory responses by a mechanism related to nitric oxide

Journal of Translational Medicine

Volumn 12, Issue 1, 2014, Pages

  Villela, Nivaldo Ribeiro ^a   dos Santos, Ana Olimpia Maia Teixeira ^b   de Miranda, Marcos Lopes ^a   Bouskela, Eliete ^a  

^a STATE UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b INSTITUTO OSWALDO CRUZ   (Brazil)

Author keywords

Endotoxemia; Fluid resuscitation; Microcirculation; Nitric oxide; Sepsis

Indexed keywords

ARGININE; BACTERIUM LIPOPOLYSACCHARIDE; BASE; BICARBONATE; GLUCOSE; LACTIC ACID; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; SODIUM CHLORIDE; AUTACOID; LIPOPOLYSACCHARIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERIOLE; ARTERY DIAMETER; ARTICLE; BIOCHEMISTRY; BLOOD PH; CAPILLARY DENSITY; CAPILLARY FLOW; CONTROLLED STUDY; ENZYME INHIBITION; ESCHERICHIA COLI; FLUID RESUSCITATION; HAMSTER; HEMATOCRIT; HEMATOLOGICAL PARAMETERS; HEMODYNAMIC PARAMETERS; INFLAMMATION; INTRAVITAL MICROSCOPY; LEUKOCYTE ADHERENCE; LEUKOCYTE ROLLING; LIPOPOLYSACCHARIDE-INDUCED ENDOTOXEMIA; MALE; MICROSCOPY; NONHUMAN; QUANTITATIVE ANALYSIS; SKINFOLD; SURVIVAL RATE; TREATMENT OUTCOME; VENULE; ANIMAL; CAPILLARY; DISEASE MODEL; DRUG EFFECTS; ENDOTOXEMIA; ESCHERICHIA COLI INFECTIONS; FLUID THERAPY; MESOCRICETUS; METABOLISM; MICROCIRCULATION; MORTALITY; PATHOPHYSIOLOGY; PHYSIOLOGY; PROCEDURES; RESUSCITATION; SHOCK, SEPTIC; SIGNAL TRANSDUCTION;

ANIMALS; CAPILLARIES; CRICETINAE; DISEASE MODELS, ANIMAL; ENDOTOXEMIA; ESCHERICHIA COLI INFECTIONS; FLUID THERAPY; INFLAMMATION MEDIATORS; LIPOPOLYSACCHARIDES; MALE; MESOCRICETUS; MICROCIRCULATION; NITRIC OXIDE; RESUSCITATION; SHOCK, SEPTIC; SIGNAL TRANSDUCTION;

EID: 84906925627     PISSN: None     EISSN: 14795876     Source Type: Journal    
DOI: 10.1186/s12967-014-0232-z     Document Type: Article

References (70)

1. Sales-Ju´nior JAL, David CM, Hatum R, Souza PCSP, Japiassu´ A, Pinheiro CTS, Friedman G, Silva OB, Dias MDA, Koterba E, Dias FS, Piras C, Luiz RR. An epidemiological study of sepsis in intensive care units. Sepsis Brazil Study. Rev Bras Ter Intensiva 2006, 18:9-17. 10.1590/S0103-507X2006000100003.
2. Martin GS, Mannino DM, Eaton S, Moss M. The epidemiology of sepsis in the United States from 1979 through 2000. N Engl J Med 2003, 348:1546-1554. 10.1056/NEJMoa022139, 12700374.
3. Carcillo JA, Davis AL, Zaritsky A. Role of early fluid resuscitation in pediatric septic shock. JAMA 1991, 266:1242-1245. 10.1001/jama.1991.03470090076035, 1870250.
4. 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 2001, 345:1368-1377. 10.1056/NEJMoa010307, 11794169.
5. Dellinger RP, Levy MM, Rhodes A, Annane D, Gerlach H, Opal SM, Sevransky JE, Sprung CL, Douglas IS, Jaeschke R, Osborn TM, Nunnally ME, Townsend SR, Reinhart K, Kleinpell RM, Angus DC, Deutschman CS, Machado FR, Rubenfeld GD, Webb SA, Beale RJ, Vincent JL, Moreno R. Surviving sepsis campaign: international guidelines for management of severe sepsis and septic shock: 2012. Crit Care Med 2013, 41:580-637. 10.1097/CCM.0b013e31827e83af, 23353941.
6. Santos AO, Furtado ES, Villela NR, Bouskela E. Microcirculatory effects of fluid therapy and dopamine, associated or not to fluid therapy, in endotoxemic hamsters. Clin Hemorheol Microcirc 2011, 47:1-13. 21321403.
7. Boyd JH, Forbes J, Nakada TA, Walley KR, Russell JA. Fluid resuscitation in septic shock: a positive fluid balance and elevated central venous pressure are associated with increased mortality. Crit Care Med 2011, 39:259-265. 10.1097/CCM.0b013e3181feeb15, 20975548.
8. Maitland K, Kiguli S, Opoka RO, Engoru C, Olupot-Olupot P, Akech SO, Nyeko R, Mtove G, Reyburn H, Lang T, Brent B, Evans JA, Tibenderana JK, Crawley J, Russell EC, Levin M, Babiker AG, Gibb DM. Mortality after fluid bolus in African children with severe infection. N Engl J Med 2011, 364:2483-2495. 10.1056/NEJMoa1101549, 21615299.
9. Ford N, Hargreaves S, Shanks L. Mortality after fluid bolus in children with shock due to sepsis or severe infection: a systematic review and meta-analysis. PLoS One 2012, 7:e43953. 10.1371/journal.pone.0043953, 22952819.
10. Losser MR, Forget AP, Payen D. Nitric oxide involvement in the hemodynamic response to fluid resuscitation in endotoxic shock in rats. Crit Care Med 2006, 34:2426-2431. 10.1097/01.CCM.0000231878.82244.C9, 16791113.
11. Wang W, Ha CH, Jhun BS, Wong C, Jain MK, Jin ZG. Fluid shear stress stimulates phosphorylation-dependent nuclear export of HDAC5 and mediates expression of KLF2 and eNOS. Blood 2010, 115:2971-2979. 10.1182/blood-2009-05-224824, 20042720.
12. Murthy S, Kissoon N. After the FEAST- fluid resuscitation in pediatric sepsis. Indian J Pediatr 2013, 80:151-154. 10.1007/s12098-012-0845-2, 22782787.
13. Ince C. The microcirculation is the motor of sepsis. Crit Care 2005, 9:S13-S19. 10.1186/cc3753, 16168069.
14. Endrich B, Asaishi K, Go¨tz A, Messmer K. Technical report-a new chamber technique for microvascular studies in unanesthetized hamsters. Res Exp Med 1980, 177:125-134. 10.1007/BF01851841.
15. Klyscz T, Ju¨nger M, Jung F, Zeintl H. Cap image-a new kind of computer-assisted video image analysis system for dynamic capillary microscopy. Biomed Tech 1997, 42:168-175. 10.1515/bmte.1997.42.6.168.
16. Dubin A, Pozo MO, Ferrara G, Murias G, Martins E, Canulla´n C, Canales HS, Kanoore Edul VS, Estenssoro E, Ince C. Systemic and microcirculatory responses to progressive hemorrhage. Intensive Care Med 2009, 35:556-564. 10.1007/s00134-008-1385-0, 19127356.
17. Hoffmann JN, Vollmar B, Inthorn D, Schildberg FW, Menger MD. A chronic model for intravital microscopic study of microcirculatory disorders and leukocyte/endothelial cell interaction during normotensive endotoxemia. Shock 1999, 12:355-364. 10.1097/00024382-199911000-00005, 10565610.
18. Rittirsch D, Hoesel LM, Ward PA. The disconnect between animal models of sepsis and human sepsis. J Leukoc Biol 2007, 81:137-143. 10.1189/jlb.0806542, 17020929.
19. Fink MP, Heard SO. Laboratory models of sepsis and septic shock. J Surg Res 1990, 49:186-196. 10.1016/0022-4804(90)90260-9, 2199735.
20. Wettstein R, Tsai AG, Erni D, Winslow RM, Intaglietta M. Resuscitation with polyethylene glycol-modified human hemoglobin improves microcirculatory blood flow and tissue oxygenation after hemorrhagic shock in awake hamsters. Crit Care Med 2003, 31:1824-1830. 10.1097/01.CCM.0000069340.16319.F2, 12794426.
21. Tsai TG, Cabrales P, Winslow RM, Intaglietta M. Microvascular oxygen distribution in awake hamster window chamber model during hyperoxia. Am J Physiol Heart Circ Physiol 2003, 285:H1537-H1545. 12805029.
22. Hoffmann JN, Vollmar B, Laschke MW, Inthorn D, Fertmann J, Schildberg FW, Menger MD. Microhemodynamic and cellular mechanisms of activated protein C action during endotoxemia. Crit Care Med 2004, 32:1011-1017. 10.1097/01.CCM.0000120058.88975.42, 15071394.
23. Cabrales P, Tsai AG, Winslow RM, Intaglietta M. Effects of extreme hemodilution with hemoglobin-based O2 carriers on microvascular pressure. Am J Physiol Heart Circ Physiol 2005, 288:H2146-H2153. 10.1152/ajpheart.00749.2004, 15637119.
24. Hoffmann JN, Vollmar B, Laschke MW, Fertmann JM, Jauch KW, Menger MD. Microcirculatory alterations in ischemia-reperfusion injury and sepsis: effects of activated protein C and thrombin inhibition. Crit Care 2005, 9(Suppl 4):S33-S37. 10.1186/cc3758, 16168073.
25. Hangai-Hoger N, Tsai AG, Cabrales P, Suematsu M, Intaglietta M. Microvascular and systemic effects following top load administration of saturated carbon monoxide-saline solution. Crit Care Med 2007, 35:1123-1132. 10.1097/01.CCM.0000259533.84180.C7, 17334240.
26. Vi´tecˇek J, Lojek A, Valacchi G, Kubala L. Arginine-based inhibitors of nitric oxide synthase: therapeutic potential and challenges. Mediators of Inflammation 2012, 2012:1-22. 10.1155/2012/318087.
27. Kilbourn RG, Szabo´ C, Traber DL. Beneficial versus detrimental effects of nitric oxide synthase inhibitors in circulatory shock: lessons learned from experimental and clinical studies. Shock 1997, 7:235-246. 10.1097/00024382-199704000-00001, 9110408.
28. Yeo TW, Lampah DA, Gitawati R, Tjitra E, Kenangalem E, McNeil YR, Darcy CJ, Granger DL, Weinberg JB, Lopansri BK, Price RN, Duffull SB, Celermajer DS, Anstey NM. Impaired nitric oxide bioavailability and L-arginine reversible endothelial dysfunction in adults with falciparum malaria. J Exp Med 2007, 204:2693-2704. 10.1084/jem.20070819, 17954570.
29. Kalil AC, Sevransky JE, Myers DE, Esposito C, Vandivier RW, Eichacker P, Susla GM, Solomon SB, Csako G, Costello R, Sittler KJ, Banks S, Natanson C, Danner RL. Preclinical trial of L-arginine monotherapy alone or with N-acetylcysteine in septic shock. Crit Care Med 2006, 34:2719-2728. 10.1097/01.CCM.0000242757.26245.03, 16971848.
30. Sun D, Messina EJ, Koller A, Wolin MS, Kaley G. Endothelium-dependent dilation to L-arginine in isolated rat skeletal muscle arterioles. Am J Physiol 1992, 262:H1211-H1216. 1566902.
31. Bode-Bo¨ger SM, Bo¨ger RH, Galland A, Tsikas D, Fro¨lich JC. L-arginine-induced vasodilation in healthy humans: pharmacokinetic-pharmacodynamic relationship. Br J Clin Pharmacol 1998, 46:489-497. 10.1046/j.1365-2125.1998.00803.x, 9833603.
32. McGown CC, Brookes ZLS. Beneficial effects of statins on the microcirculation during sepsis: the role of nitric oxide. Br J Anaesth 2007, 98:163-175. 10.1093/bja/ael358, 17251210.
33. Hossain M, Qadri SM, Liu L. Inhibition of nitric oxide synthesis enhances leukocyte rolling and adhesion in human microvasculature. J Inflamm 2012, 9:28. 10.1186/1476-9255-9-28.
34. Chandra A, Enkhbaatar P, Nakano Y, Traber LD, Traber DL. Sepsis: emerging role of nitric oxide and selectins. Clinics 2006, 61:71-76. 10.1590/S1807-59322006000100012, 16532228.
35. Li X, Klintman D, Weitz-Schmidt G, Schramm R, Thorlacius H. Lymphocyte function antigen-1 mediates leukocyte adhesion and subsequent liver damage in endotoxemic mice. Br J Pharmacol 2004, 141:709-716. 10.1038/sj.bjp.0705634, 14744817.
36. Murohara T, Parkinson SJ, Waldman SA, Lefer AM. Inhibition of nitric oxide biosynthesis promotes P-selectin expression in platelets: role of protein kinase C. Arterioscler Thromb Vasc Biol 1995, 15:2068-2075. 10.1161/01.ATV.15.11.2068, 7583591.
37. Davenpeck KL, Gauthier TW, Lefer AM. Inhibition of endothelial-derived nitric oxide promotes P-selectin expression and actions in the rat microcirculation. Gastroenterology 1994, 107:1050-1058. 7523213.
38. Zhang J, Friedman MH. Adaptive response of vascular endothelial cells to an acute increase in shear stress magnitude. Am J Physiol Heart Circ Physiol 2012, 302:H983-H991. 10.1152/ajpheart.00168.2011, 22140046.
39. Zhang J, Friedman MH. Adaptive response of vascular endothelial cells to an acute increase in shear stress frequency. Am J Physiol Heart Circ Physiol 2013, 305:H894-H902. 10.1152/ajpheart.00174.2013, 23851277.
40. Laughlin MH, Roseguini B. Mechanisms for exercise training-induced increases in skeletal muscle blood flow capacity: differences with interval sprint training versus aerobic endurance training. J Physiol Pharmacol 2008, 59(Suppl 7):71-88. 19258658.
41. Yeh YC, Sun WZ, Ko WJ, Chan WS, Fan SZ, Tsai JC, Lin TY. Dexmedetomidine prevents alterations of intestinal microcirculation that are induced by surgical stress and pain in a novel rat model. Anesth Analg 2012, 115:46-53. 10.1213/ANE.0b013e318253631c, 22504209.
42. Turek Z, Sykora R, Matejovic M, Cerny V. Anesthesia and the microcirculation. Semin Cardiothorac Vasc Anesth 2009, 13:249-258. 10.1177/1089253209353134, 19959497.
43. Cepinskas G, Wilson JX. Inflammatory response in microvascular endothelium in sepsis: role of oxidants. J Clin Biochem Nutr 2008, 42:175-184. 10.3164/jcbn.2008026, 18545638.
44. Bode-Bo¨ger SM, Bo¨ger RH, Creutzig A, Tsikas D, Gutzki FM, Alexander K, Fro¨lich JC. L-arginine infusion decreases peripheral arterial resistance and inhibits platelet aggregation in healthy subjects. Clin Sci 1994, 87:303-310. 7955906.
45. Tsao PS, Theilmeier G, Singer AH, Leung LL, Cooke JP. L-arginine attenuates platelet reactivity in hypercholesterolemic rabbits. Arterioscler Thromb 1994, 14:1529-1533. 10.1161/01.ATV.14.10.1529, 7918301.
46. Gunnerson KJ, Saul M, He S, Kellum JA. Lactate versus non-lactate metabolic acidosis: a retrospective outcome evaluation of critically ill patients. Crit Care 2006, 10:R22. 10.1186/cc3987, 16507145.
47. Bakker J, Nijsten MW, Jansen TC. Clinical use of lactate monitoring in critically ill patients. Ann Intensive Care 2013, 3:12. 10.1186/2110-5820-3-12, 23663301.
48. Hangai-Hoger N, Nacharaju P, Manjula BN, Cabrales P, Tsai AG, Acharya SA, Intaglietta M. Microvascular effects following treatment with polyethylene glycol-albumin in lipopolysaccharide-induced endotoxemia. Crit Care Med 2006, 34:108-117. 10.1097/01.CCM.0000190623.97200.82, 16374164.
49. Yeo TW, Lampah DA, Gitawati R, Tjitra E, Kenangalem E, Granger DL, Weinberg JB, Lopansri BK, Price RN, Celermajer DS, Duffull SB, Anstey NM. Safety profile of L-arginine infusion in moderately severe falciparum malaria. PLoS One 2008, 3:e2347. 10.1371/journal.pone.0002347, 18545693.
50. Jutkowitz LA. Reproductive emergencies. Vet Clin North Am Small Anim Pract 2005, 35:397-420. 10.1016/j.cvsm.2004.10.006, 15698917.
51. Uemura K, Tamagawa T, Chen Y, Maeda N, Yoshioka S, Itoh K, Miura H, Iguchi A, Hotta N. NG-methyl-L-arginine, an inhibitor of nitric oxide synthase, affects the central nervous system to produce peripheral hyperglycemia in conscious rats. Neuroendocrinology 1997, 66:136-144. 10.1159/000127231, 9263211.
52. Wu G, Bazer FW, Cudd TA, Jobgen WS, Kim SW, Lassala A, Li P, Matis JH, Meininger CJ, Spencer TE. Pharmacokinetics and safety of arginine supplementation in animals. J Nutr 2007, 137:1673S-1680S. 17513446.
53. Avontuur JA, Buijk SL, Bruining HA. Distribution and metabolism of N(G)-nitro-L-arginine methyl ester in patients with septic shock. Eur J Clin Pharmacol 1998, 54:627-631. 10.1007/s002280050525, 9860150.
54. Sordi R, Fernandes D, Heckert BT, Assreuy J. Early potassium channel blockade improves sepsis-induced organ damage and cardiovascular dysfunction. Br J Pharmacol 2011, 163:1289-1301. 10.1111/j.1476-5381.2011.01324.x, 21410460.
55. Matejovic M, Radermacher P, Tugtekin I, Stehr A, Theisen M, Vogt J, Wachter U, Ploner F, Georgieff M, Tra¨ger K. Effects of selective iNOS inhibition on gut and liver O2-exchange and energy metabolism during hyperdynamic porcine endotoxemia. Shock 2001, 16:203-210. 10.1097/00024382-200116030-00006, 11531022.
56. Matejovic M, Krouzecky A, Martinkova V, Rokyta R, Kralova H, Treska V, Radermacher P, Novak I. Selective inducible nitric oxide synthase inhibition during long-term hyperdynamic porcine bacteremia. Shock 2004, 21:458-465. 10.1097/00024382-200405000-00010, 15087823.
57. Siegemund M, van Bommel J, Schwarte LA, Studer W, Girard T, Marsch S, Radermacher P, Ince C. Inducible nitric oxide synthase inhibition improves intestinal microcirculatory oxygenation and CO2 balance during endotoxemia in pigs. Intensive Care Med 2005, 31:985-992. 10.1007/s00134-005-2664-7, 15959764.
58. Gimeno G, Carpentier PH, Desquand-Billiald S, Hanf R, Finet M. L-arginine and NG-nitro-L-arginine methyl ester cause macromolecule extravasation in the microcirculation of awake hamsters. Eur J Pharmacol 1998, 346:275-282. 10.1016/S0014-2999(98)00045-4, 9652370.
59. London NR, Zhu W, Bozza FA, Smith MC, Greif DM, Sorensen LK, Chen L, Kaminoh Y, Chan AC, Passi SF, Day CW, Barnard DL, Zimmerman GA, Krasnow MA, Li DY. Targeting Robo4-dependent Slit signaling to survive the cytokine storm in sepsis and influenza. Sci Transl Med 2010, 2:23ra19. 10.1126/scitranslmed.3000678, 20375003.
60. Lee WL, Slutsky AS. Sepsis and endothelial permeability. N Engl J Med 2010, 363:689-691. 10.1056/NEJMcibr1007320, 20818861.
61. Kalil AC, Danner RL. L-Arginine supplementation in sepsis: beneficial or harmful?. Curr Opin Crit Care 2006, 12:303-308. 10.1097/01.ccx.0000235206.92697.bf, 16810039.
62. Lei HY, Yeh TM, Liu HS, Lin YS, Chen SH, Liu CC. Immunopathogenesis of dengue virus infection. J Biomed Sci 2001, 8:377-388. 10.1007/BF02255946, 11549879.
63. Caixeta DM, Fialho FM, Azevedo ZM, Collett-Solberg PF, Villela NR, Bouskela E. Evaluation of sublingual microcirculation in children with dengue shock. Clinics 2013, 68:1061-1064. 10.6061/clinics/2013(07)26, 23917674.
64. Kellum JA. Fluid resuscitation and hyperchloremic acidosis in experimental sepsis: improved short-term survival and acid-base balance with Hextend compared with saline. Crit Care Med 2002, 30:300-305. 10.1097/00003246-200202000-00006, 11889298.
65. Gheorghe C, Dadu R, Blot C, Barrantes F, Vazquez R, Berianu F, Feng Y, Feintzig I, Amoateng-Adjepong Y, Manthous CA. Hyperchloremic metabolic acidosis following resuscitation of shock. Chest 2010, 138:1521-1522. 10.1378/chest.10-1458, 21138891.
66. Go¨decke A, Decking UK, Ding Z, Hirchenhain J, Bidmon HJ, Go¨decke S, Schrader J. Coronary hemodynamics in endothelial NO synthase knockout mice. Circ Res 1998, 82:186-194. 10.1161/01.RES.82.2.186, 9468189.
67. Huang A, Sun D, Koller A, Kaley G. Gender difference in flow-induced dilation and regulation of shear stress: role of estrogen and nitric oxide. Am J Physiol 1998, 275:R1571-R1577. 9791075.
68. Sun D, Huang A, Smith CJ, Stackpole CJ, Connetta JA, Shesely EG, Koller A, Kaley G. Enhanced release of prostaglandins contributes to flow-induced arteriolar dilation in eNOS knockout mice. Circ Res 1999, 85:288-293. 10.1161/01.RES.85.3.288, 10436172.
69. Wu Y, Huang A, Sun D, Falck JR, Koller A, Kaley G. Gender-specific compensation for the lack of NO in the mediation of flow-induced arteriolar dilation. Am J Physiol Heart Circ Physiol 2001, 280:H2456-H2461. 11356598.
70. Huang A, Sun D, Carroll MA, Jiang H, Smith CJ, Connetta JA, Falck JR, Shesely EG, Koller A, Kaley G. EDHF mediates flow-induced dilation in skeletal muscle arterioles of female eNOS-KO mice. Am J Physiol Heart Circ Physiol 2001, 280:H2462-H2469. 11356599.