Pre-emptive and continuous inhaled NO counteracts the cardiopulmonary consequences of extracorporeal circulation in a pig model

Nitric Oxide - Biology and Chemistry

Volumn 14, Issue 3, 2006, Pages 261-271

  Troncy, Eric ^a   Hubert, Bernard ^b,c   Pang, Daniel ^a   Taha, Rame ^b   Gauvin, Dominique ^b   Beauchamp, Guy ^a   Veldhuizen, Ruud A W ^d   Blaise, Gilbert A ^b  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

^c UNIVERSITY OF LIÈGE   (Belgium)

^d UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

Cardiopulmonary bypass; Inflammation; Inhalation; Lung; Nitric oxide; Post pump syndrome

Indexed keywords

LIPOPOLYSACCHARIDE; LUNG SURFACTANT; NITRIC OXIDE;

ANESTHESIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERIAL PRESSURE; ARTICLE; ARTIFICIAL VENTILATION; CARDIOPULMONARY BYPASS; CARDIOPULMONARY FUNCTION; CARDIOPULMONARY HEMODYNAMICS; CARDIOVASCULAR PARAMETERS; CENTRAL VENOUS PRESSURE; CONTROLLED STUDY; EXTRACORPOREAL CIRCULATION; HEART RATE; HEART STROKE VOLUME; HOMEOSTASIS; INFLAMMATION; LUNG HEMODYNAMICS; LUNG INJURY; LUNG MECHANICS; MALE; NONHUMAN; OXYGENATION; PRIORITY JOURNAL; RANDOMIZATION; REPERFUSION INJURY; STATISTICAL SIGNIFICANCE; SWINE;

ADMINISTRATION, INHALATION; ANIMALS; BRONCHOALVEOLAR LAVAGE FLUID; CARDIOPULMONARY BYPASS; HEMODYNAMIC PROCESSES; LEUKOCYTE COUNT; LIPOPOLYSACCHARIDES; LUNG; MALE; MODELS, ANIMAL; NITRIC OXIDE; PERIOPERATIVE CARE; PULMONARY GAS EXCHANGE; PULMONARY SURFACTANTS; REPERFUSION INJURY; SWINE;

ANIMALIA; SUS SCROFA;

EID: 33646489553     PISSN: 10898603     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.niox.2006.01.004     Document Type: Article

References (76)

1. Shroyer A.L., Coombs L.P., Peterson E.D., Eiken M.C., DeLong E.R., Chen A., Ferguson Jr. T.B., Grover F.L., and Edwards F.H. Society of Thoracic Surgeons, The Society of Thoracic Surgeons: 30-day operative mortality and morbidity risk models. Ann. Thorac. Surg. 75 6 (2003) 1856-1864
2. Taggart D.P., el Fiky M., Carter R., Bowman A., and Wheatley D.J. Respiratory dysfunction after uncomplicated cardiopulmonary bypass. Ann. Thorac. Surg. 56 (1993) 1123-1128
3. Massoudy P., Zahler S., Becker B.F., Braun S.L., Barankay A., and Meisner H. Evidence for inflammatory responses of the lungs during coronary artery bypass grafting with cardiopulmonary bypass. Chest 119 (2001) 31-36
4. Ng C.S., Wan S., Yim A.P., and Arifi A.A. Pulmonary dysfunction after cardiac surgery. Chest 121 (2002) 1269-1277
5. Khadaroo R.G., and Marshall J.C. ARDS and the multiple organ dysfunction syndrome. Common mechanisms of a common systemic process. Crit. Care Clin. 18 1 (2002) 127-141
6. Messent M., Sullivan K., Keogh B.F., Morgan C.J., and Evans T.W. Adult respiratory distress syndrome following cardiopulmonary bypass: incidence and prediction. Anaesthesia 47 3 (1992) 267-268
7. Laffey J.G., Boylan J.F., and Cheng D.C. The systemic inflammatory response to cardiac surgery: implications for the anesthesiologist. Anesthesiology 97 1 (2002) 215-252
8. Tasaka S., Hasegawa N., and Ishizaka A. Pharmacology of acute lung injury. Pulm. Pharmacol. Ther. 15 2 (2002) 83-95
9. Rady M.Y., Ryan T., and Starr N.J. Early onset of acute pulmonary dysfunction after cardiovascular surgery: risk factors and clinical outcome. Crit. Care Med. 25 11 (1997) 1831-1839
10. Tonz M., Mihaljevic T., von Segesser L.K., Fehr J., Schmid E.R., and Turina M.I. Acute lung injury during cardiopulmonary bypass. Are the neutrophils responsible?. Chest 108 6 (1995) 1551-1556
11. Rossaint R., Gerlach H., Schmidt-Ruhnke H., Pappert D., Lewandowski K., Steudel W., and Falke K. Efficacy of inhaled nitric oxide in patients with severe ARDS. Chest 107 (1995) 1107-1115
12. Troncy E., Collet J.-P., Shapiro S., Guimond J.-G., Blair L., Ducruet T., Francoeur M., Charbonneau M., and Blaise G. Inhaled nitric oxide in acute respiratory distress syndrome: a pilot randomized controlled study. Am. J. Respir. Crit. Care Med. 157 5 Pt. 1 (1998) 1483-1488
13. Faintuch S., Lang E.V., Cohen R.I., and Pinto D.S. Inhaled nitric oxide as an adjunct to suction thrombectomy for pulmonary embolism. J. Vasc. Interv. Radiol. 15 11 (2004) 1311-1315
14. Rea R.S., Ansani N.T., and Seybert A.L. Role of inhaled nitric oxide in adult heart or lung transplant recipients. Ann. Pharmacother. 39 5 (2005) 913-917
15. Rich G.F., Murphy Jr. G.D., Roos C.M., and Johns R.A. Inhaled nitric oxide: selective pulmonary vasodilation in cardiac surgical patients. Anesthesiology 78 (1993) 1028-1035
16. Beck J.R., Mongero L.B., Kroslowitz R.M., Choudhri A.F., Chen J.M., DeRose J.J., Argenziano M., Smerling A.J., and Oz M.C. Inhaled nitric oxide improves hemodynamics in patients with acute pulmonary hypertension after high-risk cardiac surgery. Perfusion 14 (1999) 37-42
17. Yoshimura N., Yamaguchi M., Oka S., Yoshida M., Murakami H., Kagawa T., and Suzuki T. Inhaled nitric oxide therapy after Fontan-type operations. Surg. Today 35 1 (2005) 31-35
18. Wagner F., Dandel M., Gunther G., Loebe M., Schulze-Neick I., Laucke U., Kuhly R., Weng Y., and Hetzer R. Nitric oxide inhalation in the treatment of right ventricular dysfunction following left ventricular assist device implantation. Circulation 96 9 Suppl. (1997) II291-II296
19. Wagner F., Buz S., Neumeyer H.H., Hetzer R., and Hocher B. Nitric oxide inhalation modulates endothelin-1 plasma concentration gradients following left ventricular assist device implantation. J. Cardiovasc. Pharmacol. 44 (2004) S89-S91
20. Guidot D.M., Hybertson B.M., Kitlowski R.P., and Repine J.E. Inhaled NO prevents IL-1-induced neutrophil accumulation and associated edema in isolated rat lungs. Am. J. Physiol. 271 (1996) L225-L229
21. Friese R.S., Fullerton D.A., McIntyre Jr. R.C., Rehring T.F., Agrafojo J., Banerjee A., and Harken A.H. NO prevents neutrophil-mediated pulmonary vasomotor dysfunction in acute lung injury. J. Surg. Res. 63 1 (1996) 23-28
22. Fullerton D.A., Eisenach J.H., McIntyre Jr. R.C., Friese R.S., Sheridan B.C., Roe G.B., Agrafojo J., Banerjee A., and Harken A.H. Inhaled nitric oxide prevents pulmonary endothelial dysfunction after mesenteric ischemia-reperfusion. Am. J. Physiol. 271 2 Pt. 1 (1996) L326-L331
23. Malmros C., Blomquist S., Dahm P., Martensson L., and Thorne J. Nitric oxide inhalation decreases pulmonary platelet and neutrophil sequestration during extracorporeal circulation in the pig. Crit. Care Med. 24 5 (1996) 845-849
24. Dahm P.L., Blomquist S., De Robertis E., Jonson B., Myhre E., Svantesson C., and Thorne J. Effects of NO inhalation on pulmonary leukocyte sequestration and blood volume in porcine endotoxaemia. Intensive Care Med. 26 3 (2000) 336-343
25. Chollet-Martin S., Gatecel C., Kermarrec N., Gougerot-Pocidalo M.A., and Payen D.M. Alveolar neutrophil functions and cytokine levels in patients with the adult respiratory distress syndrome during nitric oxide inhalation. Am. J. Respir. Crit. Care Med. 153 3 (1996) 985-990
26. Raychaudhuri B., Dweik R., Connors M.J., Buhrow L., Malur A., Drazba J., Arroliga A.C., Erzurum S.C., Kavuru M.S., and Thomassen M.J. Nitric oxide blocks nuclear factor-kappaB activation in alveolar macrophages. Am. J. Respir. Cell Mol. Biol. 21 3 (1999) 311-316
27. Walley K.R., McDonald T.E., Higashimoto Y., and Hayashi S. Modulation of proinflammatory cytokines by nitric oxide in murine acute lung injury. Am. J. Respir. Crit. Care Med. 160 (1999) 698-704
28. Kang J.L., Park W., Pack I.S., Lee H.S., Kim M.J., Lim C.M., and Koh Y. Inhaled nitric oxide attenuates acute lung injury via inhibition of nuclear factor-kappa B and inflammation. J. Appl. Physiol. 92 2 (2002) 795-801
29. Troncy E., Francoeur M., Salazkin I., Yang F., Charbonneau M., Leclerc G., Vinay P., and Blaise G. Extra-pulmonary effects of inhaled nitric oxide in swine with and without phenylephrine. Br. J. Anaesth. 79 5 (1997) 631-640
30. Fox-Robichaud A., Payne D., Hasan S.U., Ostrovsky L., Fairhead T., Reinhardt P., and Kubes P. Inhaled NO as a viable antiadhesive therapy for ischemia/reperfusion injury of distal microvascular beds. J. Clin. Invest. 101 11 (1998) 2497-2505
31. Hubert M.B., Salazkin I., Desjardins J., and Blaise G. Cardiopulmonary bypass surgery in swine: a research model. J. Exp. Anim. Sci. 43 (2003) 135-149
32. Picone A.L., Lutz C.J., Finck C., Carney D., Gatto L.A., Paskanik A., Searles B., Snyder K., and Nieman G. Multiple sequential insults cause post-pump syndrome. Ann. Thorac. Surg. 67 (1999) 978-985
33. Shah N.S., Nakayama D.K., Jacob T.D., Nishio I., Imai T., Billiar T.R., Exler R., Yousem S.A., Motoyama E.K., and Peitzman A.B. Efficacy of inhaled nitric oxide in a porcine model of adult respiratory distress syndrome. Arch. Surg. 129 (1994) 158-164
34. Dube L., Francoeur M., Troncy E., Carrier R., and Blaise G. Comparison of two administration techniques of inhaled nitric oxide on nitrogen dioxide production. Can. J. Anaesth. 42 (1995) 922-927
35. El Kebir D., Taha R., Hubert B., Gauvin D., Gangal M., and Blaise G. The anti-inflammatory effect of inhaled nitric oxide on pulmonary inflammation in a swine model. Can. J. Physiol. Pharmacol. 83 3 (2005) 252-258
36. El Kebir D., Hubert B., Taha R., Troncy E., Wang T., Gauvin D., Gangal M., and Blaise G. Effects of inhaled nitric oxide on inflammation and apoptosis after cardiopulmonary bypass. Chest 128 4 (2005) 2910-2917
37. B. Hubert, E. Troncy, D. Gauvin, R. Taha, D. Pang, A. Radomski, M.W. Radomski, G.A. Blaise, Increased alveolar and plasma gelatinases activity following porcine cardiopulmonary bypass: Inhibition by inhaled nitric oxide, Nitric Oxide: Biol. Chem., accepted for publication.
38. Bligh E.G., and Dyer W.J. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37 8 (1959) 911-917
39. Veldhuizen R.A., McCaig L.A., Akino T., and Lewis J.F. Pulmonary surfactant subfractions in patients with the acute respiratory distress syndrome. Am. J. Respir. Crit. Care Med. 152 6 Pt. 1 (1995) 1867-1871
40. Anderson B.O., Moore E.E., and Banerjee A. Phospholipase A2 regulates critical inflammatory mediators of multiple organ failure. J. Surg. Res. 56 (1994) 199-205
41. Kim F.J., Moore E.E., Moore F.A., Biffl W.L., Fontes B., and Banerjee A. Reperfused gut elaborates PAF that chemoattracts and primes neutrophils. J. Surg. Res. 58 (1996) 636-640
42. Waisman D., Brod V., Dickstein R., Abramovich A., Rotschild A., and Bitterman H. Effects of inhaled nitric oxide on lung injury after intestinal ischemia-reperfusion in rats. Shock 23 2 (2005) 150-155
43. Lutz C.J., Picone A., Gatto L.A., Paskanik A.P., Landas S., and Nieman G.F. Exogenous surfactant and positive end-expiratory pressure in the treatment of endotoxin-induced lung injury. Crit. Care Med. 26 (1998) 1379-1389
44. Waldow T., Alexiou K., Witt W., Wagner F.M., Kappert U., Knaut M., and Matschke K. Protection of lung tissue against ischemia/reperfusion injury by preconditioning with inhaled nitric oxide in an in situ pig model of normothermic pulmonary ischemia. Nitric Oxide 10 4 (2004) 195-201
45. Luiking Y.C., Poeze M., Dejong C.H., Ramsay G., and Deutz N.E. Sepsis: an arginine deficiency state?. Crit. Care Med. 32 10 (2004) 2135-2145
46. Blaise G.A., Gauvin D., Gangal M., and Authier S. Nitric oxide, cell signaling and cell death. Toxicology 208 2 (2005) 177-192
47. Kurose I., Kubes P., Wolf R., Anderson D.C., Paulson J., Miyasaka M., and Granger D.N. Inhibition of nitric oxide production mechanism of vascular albumin leakage. Circ. Res. 73 (1993) 164-171
48. Loscalzo J. Nitric oxide and vascular disease. N. Engl. J. Med. 333 (1995) 251-253
49. Gauthier T.W., Davenpeck K.L., and Lefer A.M. Nitric oxide attenuates leukocyte-endothelial interaction via P-selectin in splanchnic ischemia-reperfusion. Am. J. Physiol. 267 (1994) G562-G568
50. Griese M. Pulmonary surfactant in health and human lung diseases: state of the art. Eur. Respir. J. 13 6 (1999) 1455-1476
51. Rooney S.A., Young S.L., and Mendelson C.R. Molecular and cellular processing of lung surfactant. FASEB J. 8 (1994) 957-967
52. Putman E., van Golde L.M.G., and Haagsman H.P. Toxic oxidant species and their impact on the pulmonary surfactant system. Lung 175 (1997) 75-103
53. Griese M., Wilnhammer C., Jansen S., and Rinker C. Cardiopulmonary bypass reduces pulmonary surfactant activity in infants. J. Thorac. Cardiovasc. Surg. 118 2 (1999) 237-244
54. Middelveld R.J., and Alving K. Endotoxin-induced shock in the pig-limited effects of low and high concentrations of inhaled nitric oxide. Acta Physiol. Scand. 179 2 (2003) 203-211
55. Gries D.M., Tam E.K., Blaisdell J.M., Iwamoto L.M., Fujiwara N., Uyehara C.F., and Nakamura K.T. Differential effects of inhaled nitric oxide and hyperoxia on pulmonary dysfunction in newborn guinea pigs. Am. J. Physiol. Regul. Integr. Comp. Physiol. 279 (2000) R1525-R1530
56. Hickey M.J., Granger D.N., and Kubes P. Inducible nitric oxide synthase (iNOS) and regulation of leukocyte/endothelial cell interactions: studies in iNOS-deficient mice. Acta Physiol. Scand. 173 (2001) 119-126
57. Ng E.S., Jourd'heuil D., McCord J.M., Hernandez D., Yasui M., Knight D., and Kubes P. Enhanced S-nitroso-albumin formation from inhaled NO during ischemia/reperfusion. Circ. Res. 94 4 (2004) 559-565
58. Hascoet J.M., Fresson J., Claris O., Hamon I., Lombet J., Liska A., Cantagrel S., Al Hosri J., Thiriez G., Valdes V., Vittu G., Egreteau L., Henrot A., Buchweiller M.C., and Onody P. The safety and efficacy of nitric oxide therapy in premature infants. J. Pediatr. 146 3 (2005) 318-323
59. Field D., Elbourne D., Truesdale A., Grieve R., Hardy P., Fenton A.C., Subhedar N., Ahluwalia J., Halliday H.L., Stocks J., Tomlin K., and Normand C. INNOVO Trial Collaborating Group, Neonatal ventilation with inhaled nitric oxide versus ventilatory support without inhaled nitric oxide for preterm infants with severe respiratory failure: the INNOVO multicentre randomised controlled trial (ISRCTN 17821339). Pediatrics 115 4 (2005) 926-936
60. S. Thammasitboon, S. Thammasitboon, A critical appraisal of a systematic review: J. Sokol, S.E. Jacob, D. Bohn D, Inhaled nitric oxide for acute hypoxemic respiratory failure in children and adults. Cochrane Database Syst. Rev. 2003 (1): CD002787, Pediatr. Crit. Care Med. 6 (3) (2005) 340-343.
61. Taylor R.W., Zimmerman J.L., Dellinger R.P., Straube R.C., Criner G.J., Davis Jr. K., Kelly K.M., Smith T.C., and Small R.J. Inhaled Nitric Oxide in ARDS Study Group, Low-dose inhaled nitric oxide in patients with acute lung injury: a randomized controlled trial. JAMA 291 13 (2004) 1603-1609
62. Finer N.N. Inhaled nitric oxide for preterm infants: a therapy in search of an indication? The search continues. J. Pediatr. 146 3 (2005) 301-303
63. Round table conference, Acute lung injury,. Am. J. Respir. Crit. Care Med. 158 2 (1998) 675-679
64. Lesur O., Berthiaume Y., Blaise G., Damas P., Deland E., Guimond J.-G., and Michel R.P. Acute respiratory distress syndrome: 30 years later. Can. Respir. J. 6 1 (1999) 71-86
65. Troncy E., Francoeur M., and Blaise G. Inhaled nitric oxide: clinical applications, indications, and toxicology. Can. J. Anaesth. 44 9 (1997) 973-988
66. Chetham P.M., Sefton W.D., Bridges J.P., Stevens T., and McMurtry I. Inhaled nitric oxide pretreatment but not posttreatment attenuates ischemia-reperfusion induced pulmonary microvascular leak. Anesthesiology 86 (1997) 895-902
67. Bloomfield G.L., Holloway S., Ridings P.C., Fisher B.J., Blocher C.R., Sholley M., Bunch T., Sugerman H.J., and Fowler A.A. Pretreatment with inhaled nitric oxide inhibits neutrophil migration and oxidative activity resulting in attenuated sepsis-induced acute lung injury. Crit. Care Med. 25 (1997) 584-593
68. Emil S., Berkeland J., Kosi M., and Atkinson J. Inhaled nitric oxide prevents experimental platelet activating factor-induced shock. Arch. Surg. 131 (1996) 855-859
69. Nishina K., Mikawa K., Takao Y., and Obara H. Inhaled nitric oxide does not prevent endotoxin-induced lung injury in rabbits. Acta Anaesth. Scand. 41 (1997) 399-407
70. Rayhrer C.S., Edmisten T.D., Cephas G.A., Tribble C.G., Kron I.L., and Young J.S. Nitric oxide potentiates acute lung injury in an isolated rabbit lung model. Ann. Thorac. Surg. 65 (1998) 935-938
71. Razavi H.M., Werhun R., Scott J.A., Weicker S., Wang le F., McCormack D.G., and Mehta S. Effects of inhaled nitric oxide in a mouse model of sepsis-induced acute lung injury. Crit. Care Med. 30 4 (2002) 868-873
72. Schütte H., Witzenrath M., Mayer K., Rosseau S., Seeger W., and Grimminger F. Short-term preconditioning with inhaled nitric oxide protects rabbit lungs against ischemia-reperfusion injury. Transplantation 72 (2001) 1363-1370
73. Eiserich J.P., Hristova M., Cross C.E., Jones A.D., Freeman B.A., Halliwell B., and van der Vliet A. Formation of nitric oxide-mediated inflammatory oxidants by myeloperoxidase in neutrophils. Nature 391 (1998) 393-397
74. Wolkow P.P. Involvement and dual effects of nitric oxide in septic shock. Inflamm. Res. 47 4 (1998) 152-166
75. Murakami S., Bacha E.A., Mazmanian G.M., Detruit H., Chapelier A., Dartevelle P., and Herve P. The Paris-Sud University Lung Transplantation Group, Effects of various timings and concentrations of inhaled nitric oxide in lung ischemia-reperfusion. Am. J. Respir. Crit. Care Med. 156 2 Pt. 1 (1997) 454-458
76. Dodds W.J. The pig model for biomedical research. Fed. Proc. 41 (1982) 247-256