The Journal of Pediatrics
Volume 151, Issue 1 , Pages 10-15 , July 2007

Inhaled Nitric Oxide in the Premature Newborn

  • John P. Kinsella, MD

      Affiliations

    • Pediatric Heart-Lung Center, Sections of Neonatology and Pulmonary Medicine, Denver, Colorado
    • Corresponding Author InformationReprint requests: John P. Kinsella, MD, The Children’s Hospital, Box B070, 1056 E. 19th Avenue, Denver, CO 80218.
    • ,
  • Steven H. Abman, MD

      Affiliations

    • The Children’s Hospital/University of Colorado School of Medicine, Denver, Colorado.

Received 8 November 2006 ,Revised 16 January 2007 ,Accepted 2 February 2007.

References 

  1. Kinsella JP, Neish SR, Shaffer E, Abman SH. Low-dose inhalational nitric oxide in persistent pulmonary hypertension of the newborn. Lancet. 1992;340:819–820
  2. Roberts JD, Polaner DM, Lang P, Zapol WM. Inhaled nitric oxide in persistent pulmonary hypertension of the newborn. Lancet. 1992;340:818–819
  3. Clark RH, Kueser TJ, Walker MW, Southgate WM, Huckaby JL, Perez JA, et al. Randomized, controlled trial of low-dose inhaled nitric oxide treatment of persistent pulmonary hypertension of the newborn. N Engl J Med. 2000;17:342;469-74
  4. Neonatal Inhaled Nitric Oxide Study Group. Inhaled nitric oxide in full-term and nearly full-term infants with hypoxic respiratory failure. N Engl J Med. 1997;336:597–604
  5. Northway WH, Rosan RC, Porter DY. Pulmonary disease following respirator therapy of hyaline-membrane disease (Bronchopulmonary dysplasia). N Engl J Med. 1967;276:357–368
  6. Abman SH, Kinsella JP, Schaffer MS, Wilkening RB. Inhaled nitric oxide in the management of a premature newborn with severe respiratory distress and pulmonary hypertension. Pediatrics. 1993;92:606–609
  7. Kinsella JP, McQueston J, Rosenberg AA, Abman SH. Hemodynamic effects of exogenous nitric oxide in ovine transitional pulmonary circulation. Am J Physiol. 1992;262:H875–H880
  8. Roberts JD, Chen TY, Kawai N, Wain J, Dupuy P, Shimouchi A, et al. Inhaled nitric oxide reverses pulmonary vasoconstriction in the hypoxic and acidotic newborn lamb. Circ Res. 1993;72:246–254
  9. Kinsella JP, Ivy DD, Abman SH. Ontogeny of NO activity and response to inhaled NO in the developing ovine pulmonary circulation. Am J Physiol. 1994;267:H1955–H1961
  10. Kinsella JP, Ivy DD, Abman SH. Inhaled nitric oxide lowers pulmonary vascular resistance and improves gas exchange in severe experimental hyaline membrane disease. Pediatr Res. 1994;36:402–408
  11. Kanwar S, Kubes P. Nitric oxide is an antiadhesive molecule for leukocytes. New Horizons. 1995;3:93–104
  12. Kinsella JP, Parker TA, Galan H, Sheridan BC, Halbower AC, Abman SH. Effects of inhaled nitric oxide on pulmonary edema and lung neutrophil accumulation in severe experimental hyaline membrane disease. Pediatr Res. 1997;41:457–463
  13. Merritt TA, Cochrane CG, Holcomb K, Bohl B, Hallman M, Strayer D, et al. Elastase and α-1-proteinase inhibitor activity in tracheal aspirates during respiratory distress syndrome. J Clin Invest. 1983;72:656–666
  14. Ogden BE, Murphy S, Saunders GC, Johnson JD. Lung lavage of newborns with respiratory distress syndrome: prolonged neutrophil influx is associated with bronchopulmonary dysplasia. Chest. 1983;83:31–33
  15. Speer CP, Ruess D, Harms K, Herting E, Gefeller O. Neutrophil elastase and acute pulmonary damage in neonates with severe respiratory distress syndrome. Pediatrics. 1993;91:794–799
  16. Brus F, Van Oeveren W, Heikamp A, Okken A, Oetomo SB. Leakage of protein into lungs of preterm ventilated rabbits is correlated with activation of clotting, complement, and polymorphonuclear leukocytes in plasma. Pediatr Res. 1996;39:958–965
  17. Storme L, Zerimech F, Riou Y, Martin-Ponthieu A, Devisme L, Slomianny C, et al. Inhaled nitric oxide neither alters oxidative stress parameters nor induces lung inflammation in premature lambs with moderate hyaline membrane disease. Bio Neo. 1998;73:172–181
  18. Nelin LD, Welty SE, Morrisey JF, Dawson CA. Nitric oxide increases the survival of rats with a high oxygen exposure. Pediatr Res. 1998;43:727–732
  19. Gutierrez HH, Nieves B, Chumley P, Rivera A, Freeman BA. Nitric oxide regulation of superoxide-dependent lung injury: oxidant-protective actions of endogenously produced and exogenously administered nitric oxide. Free Radic Biol Med. 1996;21:43–52
  20. Issa A, Lappalainen U, Kleinman M, Bry K, Hallman M. Inhaled nitric oxide decreases hyperoxia-induced surfactant abnormality in preterm rabbits. Pediatr Res. 1999;45:247–254
  21. MacRitchie AN, Albertine KH, Sun J, Lei PS, Jensen SC, Freestone AA, et al. Reduced endothelial nitric oxide synthase in lungs of chronically ventilated preterm lambs. Am J Physiol Lung Cell Mol Physiol. 2001;281:L1011–L1020
  22. Afshar S, Gibson LL, Yuhanna IS, Sherman TS, Kerecman JD, Grubb PH, et al. Pulmonary NO synthase expression is attenuated in a fetal baboon model of chronic lung disease. Am J Physiol Lung Cell Mol Physiol. 2003;284:L749–L758
  23. Han RN, Babaei S, Robb M, Lee TL, Risdale R, Ackerley C, et al. Defective lung vascular development and fatal respiratory distress in eNOS deficient mice: a model of alveolar capillary dysplasia?. Circ Res. 2004;94:1115–1123
  24. Balasubramaniam V, Tang JR, Maxey A, Plopper CG, Abman SH. Mild hypoxia impairs alveolarization in the endothelial nitric oxide synthase-deficient mouse. Am J Physiol Lung Cell Mol Physiol. 2003;284:L964–L971
  25. Tang JR, Markham NE, Lin YJ, McMurty IF, Maxey A, Kinsella JP, et al. Inhaled nitric oxide attenuates pulmonary hypertension and improves lung growth in infant rats after neonatal treatment with a VEGF receptor inhibitor. Am J Physiol Lung Cell Mol Physiol. 2004;287:L344–L351
  26. Lin YJ, Markham NE, Balasubramaniam V, Tang JR, Maxey A, Kinsella JP, et al. Inhaled nitric oxide enhances distal lung growth after exposure to hyperoxia in neonatal rats. Pediatr Res. 2005;58:22–29
  27. McCurnin DC, Pierce RA, Chang LY, Gibson LL, Osborne-Lawrence S, Yoder BA, et al. Inhaled NO improves early pulmonary function and modifies lung growth and elastin deposition in a baboon model of neonatal chronic lung disease. Am J Physiol – Lung. 2005;288:450–459
  28. Bland RD, Albertine KH, Carlton DP, MacRitchie AJ. Inhaled nitric oxide effects on lung structure and function in chronically ventilated preterm lambs. Am J Respir Crit Care Med. 2005;172:899–906
  29. Peliowski A, Finer NN, Etches PC, Tierney AJ, Ryan CA. Inhaled nitric oxide for premature infants after prolonged rupture of the membranes. J Pediatr. 1995;126:450–453
  30. Meurs KP, Rhine WD, Asselin JM, Duran DJ Preemie NO Collaborative Group. Response of premature infants with severe respiratory failure to inhaled nitric oxide. Pediatr Pulmonol. 1997;24:319–323
  31. Abman SH. Bronchopulmonary dysplasia: a “vascular hypothesis.”. Am J Respir Crit Care Med. 2001;164:1755–1756
  32. Hogman M, Frostell C, Arnberg H, Hedenstierna G. Bleeding time prolongation and NO inhalation. Lancet. 1993;341:1664–1665
  33. Simon DI, Stamler JS, Jaraki O, Keaney JF, Osborne JA, Francis SA, et al. Antiplatelet properties of protein S-nitrosothiols derived from nitric oxide and endothelium-derived relaxing factor. Arterioscler Thromb. 1993;13:791–799
  34. George TN, Johnson KJ, Bates JN, Segar JL. The effect of inhaled nitric oxide therapy on bleeding time and platelet aggregation in neonates. J Pediatr. 1998;132:731–734
  35. Subhedar NV, Ryan SW, Shaw NJ. Open randomised controlled trial of inhaled nitric oxide and early dexamethasone in high risk preterm infants. Arch Dis Child. 1997;77:F185–F190
  36. Kinsella JP, Walsh WF, Bose CL, Gerstmann DR, Labella JJ, Sardesai S, et al. Inhaled nitric oxide in premature neonates with severe hypoxaemic respiratory failure: a randomised controlled trial. Lancet. 1999;354:1061–1065
  37. The Franco-Belgium Collaborative NO Trial Group. Early compared with delayed inhaled nitric oxide in moderately hypoxaemic neonates with respiratory failure: a randomised controlled trial. Lancet. 1999;354:1066–1071
  38. Hascoet JM, Fresson J, Claris O, Hamon I, Lombet J, Liska A, et al. The safety and efficacy of nitric oxide therapy in premature infants. J Pediatr. 2005;146:318–323
  39. Finer NN. Inhaled nitric oxide for preterm infants: a therapy in search of an indication? (The search continues). J Pediatr. 2005;146:301–302
  40. Hamon I, Fresson J, Nicolas MB, Buchweiller MC, Franck P, Hascoet JM. Early inhaled nitric oxide improves oxidative balance in very preterm infants. Pediatr Res. 2005;57:637–643
  41. Field D, Elbourne D, Truesdale A, Grieve R, Hardy P, Fenton AC, et al. Neonatal ventilation with inhaled nitric oxide versus ventilatory support without inhaled nitric oxide for preterm infants with severe respiratory failure: the INNOVO multicentre randomized controlled trial. Pediatrics. 2005;115:926–936
  42. Field DJ. Nitric oxide—still no consensus. Early Human Development. 2005;81:1–4
  43. Schreiber MD, Gin-Mestan K, Marks JD, Huo D, Lee G, Srisuparp P. Inhaled nitric oxide in premature infants with the respiratory distress syndrome. N Engl J Med. 2003;349:2099–2107
  44. Van Meurs KP, Wright LL, Ehrenkranz RA, Lemons JA, Ball MB, Poole WK, et al. Inhaled nitric oxide for premature infants with severe respiratory failure. N Engl J Med. 2005;353:13–22
  45. Ballard RA, Truog WE, Cnaan A, Martin RJ, Ballard PR, Merrill JD, et al. Inhaled nitric oxide in preterm infants undergoing mechanical ventilation. N Engl J Med. 2006;205:343–353
  46. Kinsella JP, Cutter GR, Walsh WF, Gerstmann DR, Bose CL, Hart C, et al. Early inhaled nitric oxide therapy in premature newborns with respiratory failure. N Engl J Med. 2006;205:354–364
  47. Mestan KK, Marks JD, Hecox K, Huo D, Schreiber MD. Neurodevelopmental outcomes of premature infants treated with inhaled nitric oxide. N Engl J Med. 2005;353:23–32
  48. Martin RJ, Walsh MC. Inhaled nitric oxide for preterm infants—Who benefits?. N Engl J Med. 2005;353:82–84
  49. Viscardi RM, Muhumuza CK, Rodriquez A, Fairchild KD, Sun CC, Gross GW, et al. Inflammatory markers in intrauterine and fetal blood and cerebrospinal fluid compartments are associated with adverse pulmonary and neurologic outcomes in preterm infants. Pediatr Res. 2004;55:1009–1017
  50. Haynes RL, Baud O, Li J, Kinney HC, Volpe JJ, Folkerth DR. Oxidative and nitrative injury in periventricular leukomalacia. Brain Pathol. 2005;15:225–233
  51. Aaltonen M, Soukka H, Halkola L, Jalonen J, Kalimo H, Holopainen IE, et al. Inhaled nitric oxide treatment inhibits neuronal injury after meconium aspiration in piglets. Early Human Dev. 2007;83:77–85
  52. Palowski JR, Hess DT, Stamler JS. Export by red blood cells of nitric oxide bioactivity. Nature. 2001;409:622–626
  53. Sugiura M, McCulloch PR, Wren S, Dawson RH, Froese AB. Ventilator pattern influences neutrophil influx and activation in atelectasis-prone rabbit lung. J Appl Physiol. 1994;77:1355–1365

PII: S0022-3476(07)00129-1

doi: 10.1016/j.jpeds.2007.02.010

The Journal of Pediatrics
Volume 151, Issue 1 , Pages 10-15 , July 2007

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