Bronchopulmonary dysplasia early changes leading to long-term consequences

Frontiers in Medicine

Volumn 2, Issue FEB, 2015, Pages

  Hilgendorff, Anne ^a,b   O'Reilly, Michael A ^c  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

^b LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^c UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

Animal models; Bronchopulmonary dysplasia; Hyperoxia; Inflammation; Long term consequences; Lung development; Mechanical ventilation; Neonatal chronic lung disease

Indexed keywords

EID: 85014414553     PISSN: None     EISSN: 2296858X     Source Type: Journal    
DOI: 10.3389/fmed.2015.00002     Document Type: Short Survey

References (158)

1. Jobe AH, Bancalari E. Bronchopulmonary dysplasia. Am J Respir Crit Care Med (2001) 163:1723-9. doi:10.1164/ajrccm.163.7.2011060
2. Stoll BJ, Hansen NI, Bell EF, Shankaran S, Laptook AR, Walsh MC, et al. Neonatal outcomes of extremely preterm infants from the nichd neonatal research network. Pediatrics (2010) 126:443-56. doi:10.1542/peds.2009-2959
3. Johnson AH, Peacock JL, Greenough A, Marlow N, Limb ES, Marston L, et al. High-frequency oscillatory ventilation for the prevention of chronic lung disease of prematurity. N Engl J Med (2002) 347:633-42. doi:10.1056/NEJMoa020432
4. Ehrenkranz RA, Walsh MC, Vohr BR, Jobe AH, Wright LL, Fanaroff AA, et al. Validation of the national institutes of health consensus definition of bronchopulmonary dysplasia. Pediatrics (2005) 116:1353-60. doi:10.1542/peds.2005-0249
5. Gortner L, Misselwitz B, Milligan D, Zeitlin J, Kollee L, Boerch K, et al. Rates of bronchopulmonary dysplasia in very preterm neonates in Europe: results from the mosaic cohort. Neonatology (2011) 99:112-7. doi:10.1159/000313024
6. Vachon E, Bourbonnais Y, Bingle CD, Rowe SJ, Janelle MF, Tremblay GM. Anti-inflammatory effect of pre-elafin in lipopolysaccharide-induced acute lung inflammation. Biol Chem (2002) 383:1249-56. doi:10.1515/BC.2002.138
7. Van Marter LJ, Pagano M, Allred EN, Leviton A, Kuban KC. Rate of bronchopulmonary dysplasia as a function of neonatal intensive care practices. J Pediatr (1992) 120:938-46. doi:10.1016/S0022-3476(05)81968-7
8. Doyle LW. Evaluation of neonatal intensive care for extremely-low-birth-weight infants. Semin Fetal Neonatal Med (2006) 11:139-45. doi:10.1016/j.siny.2005.11.009
9. Lopez E, Mathlouthi J, Lescure S, Krauss B, Jarreau PH, Moriette G. Capnography in spontaneously breathing preterm infants with bronchopulmonary dysplasia. Pediatr Pulmonol (2011) 46:896-902. doi:10.1002/ppul.21445
10. Petersson J, Glenny RW. Gas exchange and ventilation-perfusion relationships in the lung. Eur Respir J (2014) 44(4):1023-41. doi:10.1183/09031936.00037014
11. Hilgendorff A, Reiss I, Gortner L, Schuler D, Weber K, Lindemann H. Impact of airway obstruction on lung function in very preterm infants at term. Pediatr Crit Care Med (2008) 9:629-35. doi:10.1097/PCC.0b013e31818d17c8
12. May C, Kennedy C, Milner AD, Rafferty GF, Peacock JL, Greenough A. Lung function abnormalities in infants developing bronchopulmonary dysplasia. Arch Dis Child (2011) 96:1014-9. doi:10.1136/adc.2011.212332
13. Kinsella JP, Greenough A, Abman SH. Bronchopulmonary dysplasia. Lancet (2006) 367:1421-31. doi:10.1016/S0140-6736(06)68615-7
14. Steinhorn RH. Neonatal pulmonary hypertension. Pediatr Crit Care Med (2010) 11:S79-84. doi:10.1097/PCC.0b013e3181c76cdc
15. Korhonen P, Tammela O, Koivisto AM, Laippala P, Ikonen S. Frequency and risk factors in bronchopulmonary dysplasia in a cohort of very low birth weight infants. Early Hum Dev (1999) 54:245-58. doi:10.1016/S0378-3782(98)00101-7
16. Clyman R, Cassady G, Kirklin JK, Collins M, Philips JB III. The role of patent ductus arteriosus ligation in bronchopulmonary dysplasia: reexamining a randomized controlled trial. J Pediatr (2009) 154:873-6. doi:10.1016/j.jpeds.2009.01.005
17. Oh W, Poindexter BB, Perritt R, Lemons JA, Bauer CR, Ehrenkranz RA, et al. Association between fluid intake and weight loss during the first ten days of life and risk of bronchopulmonary dysplasia in extremely low birth weight infants. J Pediatr (2005) 147:786-90. doi:10.1016/j.jpeds.2005.06.039
18. Kramer BW. Antenatal inflammation and lung injury: prenatal origin of neonatal disease. J Perinatol (2008) 28(Suppl 1):S21-7. doi:10.1038/jp.2008.46
19. Stevens TP, Harrington EW, Blennow M, Soll RF. Early surfactant administration with brief ventilation vs. Selective surfactant and continued mechanical ventilation for preterm infants with or at risk for respiratory distress syndrome. Cochrane Database Syst Rev (2007) 4:CD003063
20. Mittendorf R, Covert R, Montag AG, elMasri W, Muraskas J, Lee KS, et al. Special relationships between fetal inflammatory response syndrome and bronchopulmonary dysplasia in neonates. J Perinat Med (2005) 33:428-34. doi:10.1515/JPM.2005.076
21. Jobe AH, Ikegami M. Mechanisms initiating lung injury in the preterm. Early Hum Dev (1998) 53:81-94. doi:10.1016/S0378-3782(98)00045-0
22. Watterberg KL, Demers LM, Scott SM, Murphy S. Chorioamnionitis and early lung inflammation in infants in whom bronchopulmonary dysplasia develops. Pediatrics (1996) 97:210-5
23. Hislop AA, Wigglesworth JS, Desai R, Aber V. The effects of preterm delivery and mechanical ventilation on human lung growth. Early Hum Dev (1987) 15:147-64. doi:10.1016/0378-3782(87)90003-X
24. Brew N, Hooper SB, Allison BJ, Wallace MJ, Harding R. Injury and repair in the very immature lung following brief mechanical ventilation. Am J Physiol Lung Cell Mol Physiol (2011) 301:L917-26. doi:10.1152/ajplung.00207.2011
25. Wheeler KI, Klingenberg C, Morley CJ, Davis PG. Volume-targeted versus pressure-limited ventilation for preterm infants: a systematic review and meta-analysis. Neonatology (2011) 100:219-27. doi:10.1159/000326080
26. Saugstad OD, Aune D. In search of the optimal oxygen saturation for extremely low birth weight infants: a systematic review and meta-analysis. Neonatology (2011) 100:1-8. doi:10.1159/000322001
27. Biniwale MA, Ehrenkranz RA. The role of nutrition in the prevention and management of bronchopulmonary dysplasia. Semin Perinatol (2006) 30:200-8. doi:10.1053/j.semperi.2006.05.007
28. Shenai JP, Chytil F, Stahlman MT. Vitamin a status of neonates with bronchopulmonary dysplasia. Pediatr Res (1985) 19:185-8. doi:10.1203/00006450-198502000-00007
29. Watterberg KL, Scott SM. Evidence of early adrenal insufficiency in babies who develop bronchopulmonary dysplasia. Pediatrics (1995) 95:120-5
30. Regev RH, Lusky A, Dolfin T, Litmanovitz I, Arnon S, Reichman B. Excess mortality and morbidity among small-for-gestational-age premature infants: a population-based study. J Pediatr (2003) 143:186-91. doi:10.1067/S0022-3476(03)00181-1
31. Reiss I, Landmann E, Heckmann M, Misselwitz B, Gortner L. Increased risk of bronchopulmonary dysplasia and increased mortality in very preterm infants being small for gestational age. Arch Gynecol Obstet (2003) 269:40-4. doi:10.1007/s00404-003-0486-9
32. Walsh MC, Yao Q, Horbar JD, Carpenter JH, Lee SK, Ohlsson A. Changes in the use of postnatal steroids for bronchopulmonary dysplasia in 3 large neonatal networks. Pediatrics (2006) 118:e1328-35. doi:10.1542/peds.2006-0359
33. Rieger-Fackeldey E, Schulze A, Pohlandt F, Schwarze R, Dinger J, Lindner W. Short-term outcome in infants with a birthweight less than 501 grams. Acta Paediatr (2005) 94:211-6. doi:10.1111/j.1651-2227.2005.tb01893.x
34. Bose C, Van Marter LJ, Laughon M, O'Shea TM, Allred EN, Karna P, et al. Fetal growth restriction and chronic lung disease among infants born before the 28th week of gestation. Pediatrics (2009) 124:e450-8. doi:10.1542/peds.2008-3249
35. Rozance PJ, Seedorf GJ, Brown A, Roe GB, O'Meara MC, Gien J, et al. Intrauterine growth restriction decreases pulmonary alveolar and vessel growth and causes pulmonary artery endothelial cell dysfunction in vitro in fetal sheep. Am J Physiol Lung Cell Mol Physiol (2011) 301(6):L860-71. doi:10.1152/ajplung.00197.2011
36. Kramer BW, Kallapur S, Newnham J, Jobe AH. Prenatal inflammation and lung development. Semin Fetal Neonatal Med (2009) 14:2-7. doi:10.1016/j.siny.2008.08.011
37. Bhandari V, Bizzarro MJ, Shetty A, Zhong X, Page GP, Zhang H, et al. Familial and genetic susceptibility to major neonatal morbidities in preterm twins. Pediatrics (2006) 117:1901-6. doi:10.1542/peds.2005-1414
38. Hallman M, Haataja R. Genetic influences and neonatal lung disease. Semin Neonatol (2003) 8:19-27. doi:10.1016/S1084-2756(02)00196-3
39. Hilgendorff A, Heidinger K, Pfeiffer A, Bohnert A, Konig IR, Ziegler A, et al. Association of polymorphisms in the mannose-binding lectin gene and pulmonary morbidity in preterm infants. Genes Immun (2007) 8:671-7. doi:10.1038/sj.gene.6364432
40. Wang H, St Julien KR, Stevenson DK, Hoffmann TJ, Witte JS, Lazzeroni LC, et al. A genome-wide association study (gwas) for bronchopulmonary dysplasia. Pediatrics (2013) 132:290-7. doi:10.1542/peds.2013-0533
41. Bream EN, Leppellere CR, Cooper ME, Dagle JM, Merrill DC, Christensen K, et al. Candidate gene linkage approach to identify DNA variants that predispose to preterm birth. Pediatr Res (2013) 73:135-41. doi:10.1038/pr.2012.166
42. Laughon MM, Langer JC, Bose CL, Smith PB, Ambalavanan N, Kennedy KA, et al. Prediction of bronchopulmonary dysplasia by postnatal age in extremely premature infants. Am J Respir Crit Care Med (2011) 183:1715-22. doi:10.1164/rccm.201101-0055OC
43. Binet ME, Bujold E, Lefebvre F, Tremblay Y, Piedboeuf B. Role of gender in morbidity and mortality of extremely premature neonates. Am J Perinatol (2012) 29(3):159-66. doi:10.1055/s-0031-1284225
44. Trotter A, Maier L, Kron M, Pohlandt F. Effect of oestradiol and progesterone replacement on bronchopulmonary dysplasia in extremely preterm infants. Arch Dis Child Fetal Neonatal Ed (2007) 92:F94-8. doi:10.1136/adc.2006.097170
45. Vrijlandt EJ, Gerritsen J, Boezen HM, Duiverman EJ. Gender differences in respiratory symptoms in 19-year-old adults born preterm. Respir Res (2005) 6:117. doi:10.1186/1465-9921-6-117
46. Zeltner TB, Burri PH. The postnatal development and growth of the human lung. II. Morphology. Respir Physiol (1987) 67:269-82. doi:10.1016/0034-5687(87)90057-0
47. Hyde DM, Blozis SA, Avdalovic MV, Putney LF, Dettorre R, Quesenberry NJ, et al. Alveoli increase in number but not size from birth to adulthood in rhesus monkeys. Am J Physiol Lung Cell Mol Physiol (2007) 293:L570-9. doi:10.1152/ajplung.00467.2006
48. Schittny JC, Mund SI, Stampanoni M. Evidence and structural mechanism for late lung alveolarization. Am J Physiol Lung Cell Mol Physiol (2008) 294:L246-54. doi:10.1152/ajplung.00296.2007
49. Tschanz SA, Salm LA, Roth-Kleiner M, Barre SF, Burri PH, Schittny JC. Rat lungs show a biphasic formation of new alveoli during postnatal development. J Appl Physiol (2014) 117:89-95. doi:10.1152/japplphysiol.01355.2013
50. Jobe AH. Postnatal corticosteroids for bronchopulmonary dysplasia. Clin Perinatol (2009) 36:177-88. doi:10.1016/j.clp.2008.09.016
51. Massaro D, Teich N, Maxwell S, Massaro GD, Whitney P. Postnatal development of alveoli. Regulation and evidence for a critical period in rats. J Clin Invest (1985) 76:1297-305. doi:10.1172/JCI112103
52. Roth-Kleiner M, Berger TM, Gremlich S, Tschanz SA, Mund SI, Post M, et al. Neonatal steroids induce a down-regulation of tenascin-c and elastin and cause a deceleration of the first phase and an acceleration of the second phase of lung alveolarization. Histochem Cell Biol (2014) 141:75-84. doi:10.1007/s00418-013-1132-7
53. Doyle LW, Ehrenkranz RA, Halliday HL. Early (< 8 days) postnatal corticosteroids for preventing chronic lung disease in preterm infants. Cochrane Database Syst Rev (2014) 5:CD001146. doi:10.1002/14651858.CD001146.pub4
54. Halliday HL, Ehrenkranz RA, Doyle LW. Early (> 8 days) postnatal corticosteroids for preventing chronic lung disease in preterm infants. Cochrane Database Syst Rev (2010) 1:CD001146. doi:10.1002/14651858.CD001146.pub3
55. Northway WH Jr, Rosan RC, Porter DY. Pulmonary disease following respirator therapy of hyaline-membrane disease. bronchopulmonary dysplasia. N Engl J Med (1967) 276:357-68. doi:10.1056/NEJM196702162760701
56. Husain AN, Siddiqui NH, Stocker JT. Pathology of arrested acinar development in postsurfactant bronchopulmonary dysplasia. Hum Pathol (1998) 29:710-7. doi:10.1016/S0046-8177(98)90280-5
57. Pierce RA, Albertine KH, Starcher BC, Bohnsack JF, Carlton DP, Bland RD. Chronic lung injury in preterm lambs: disordered pulmonary elastin deposition. Am J Physiol (1997) 272:L452-60
58. Thibeault DW, Mabry SM, Ekekezie II, Truog WE. Lung elastic tissue maturation and perturbations during the evolution of chronic lung disease. Pediatrics (2000) 106:1452-9. doi:10.1542/peds.106.6.1452
59. Thibeault DW, Mabry SM, Ekekezie II, Zhang X, Truog WE. Collagen scaffolding during development and its deformation with chronic lung disease. Pediatrics (2003) 111:766-76. doi:10.1542/peds.111.4.766
60. Bruce MC, Schuyler M, Martin RJ, Starcher BC, Tomashefski JF Jr, Wedig KE. Risk factors for the degradation of lung elastic fibers in the ventilated neonate. Implications for impaired lung development in bronchopulmonary dysplasia. Am Rev Respir Dis (1992) 146:204-12. doi:10.1164/ajrccm/146.1.204
61. Bruce MC, Wedig KE, Jentoft N, Martin RJ, Cheng PW, Boat TF, et al. Altered urinary excretion of elastin cross-links in premature infants who develop bronchopulmonary dysplasia. Am Rev Respir Dis (1985) 131:568-72
62. Merritt TA, Cochrane CG, Holcomb K, Bohl B, Hallman M, Strayer D, et al. Elastase and alpha 1-proteinase inhibitor activity in tracheal aspirates during respiratory distress syndrome. Role of inflammation in the pathogenesis of bronchopulmonary dysplasia. J Clin Invest (1983) 72:656-66. doi:10.1172/JCI111015
63. Lukkarinen H, Hogmalm A, Lappalainen U, Bry K. Matrix metalloproteinase-9 deficiency worsens lung injury in a model of bronchopulmonary dysplasia. Am J Respir Cell Mol Biol (2009) 41:59-68. doi:10.1165/rcmb.2008-0179OC
64. Kroon AA, Wang J, Kavanagh BP, Huang Z, Kuliszewski M, van Goudoever JB, et al. Prolonged mechanical ventilation induces cell cycle arrest in newborn rat lung. PLoS One (2011) 6:e16910. doi:10.1371/journal.pone.0016910
65. Mokres LM, Parai K, Hilgendorff A, Ertsey R, Alvira CM, Rabinovitch M, et al. Prolonged mechanical ventilation with air induces apoptosis and causes failure of alveolar septation and angiogenesis in lungs of newborn mice. Am J Physiol Lung Cell Mol Physiol (2010) 298:L23-35. doi:10.1152/ajplung.00251.2009
66. Bland RD, Ertsey R, Mokres LM, Xu L, Jacobson BE, Jiang S, et al. Mechanical ventilation uncouples synthesis and assembly of elastin and increases apoptosis in lungs of newborn mice. Prelude to defective alveolar septation during lung development? Am J Physiol Lung Cell Mol Physiol (2008) 294:L3-14. doi:10.1152/ajplung.00362.2007
67. Bland RD, Mokres LM, Ertsey R, Jacobson BE, Jiang S, Rabinovitch M, et al. Mechanical ventilation with 40% oxygen reduces pulmonary expression of genes that regulate lung development and impairs alveolar septation in newborn mice. Am J Physiol Lung Cell Mol Physiol (2005) 293(5):L1099-110
68. Hilgendorff A, Parai K, Ertsey R, Jain N, Navarro EF, Peterson JL, et al. Inhibiting lung elastase activity enables lung growth in mechanically ventilated newborn mice. Am J Respir Crit Care Med (2011) 184(5):537-46. doi:10.1164/rccm.201012-2010OC
69. Hilgendorff A, Parai K, Ertsey R, Juliana Rey-Parra G, Thebaud B, Tamosiuniene R, et al. Neonatal mice genetically modified to express the elastase inhibitor elafin are protected against the adverse effects of mechanical ventilation on lung growth. Am J Physiol Lung Cell Mol Physiol (2012) 303:L215-27. doi:10.1152/ajplung.00405.2011
70. Stoll BJ, Gordon T, Korones SB, Shankaran S, Tyson JE, Bauer CR, et al. Early-onset sepsis in very low birth weight neonates: a report from the national institute of child health and human development neonatal research network. J Pediatr (1996) 129:72-80. doi:10.1016/S0022-3476(96)70192-0
71. Yoon BH, Romero R, Jun JK, Park KH, Park JD, Ghezzi F, et al. Amniotic fluid cytokines (interleukin-6, tumor necrosis factor-alpha, interleukin-1 beta, and interleukin-8) and the risk for the development of bronchopulmonary dysplasia. Am J Obstet Gynecol (1997) 177:825-30. doi:10.1016/S0002-9378(97)70276-X
72. Speer CP. Pulmonary inflammation and bronchopulmonary dysplasia. J Perinatol (2006) 26(Suppl 1):S57-62 discussion S63-54. doi:10.1038/sj.jp.7211476
73. Todd DA, Earl M, Lloyd J, Greenberg M, John E. Cytological changes in endotracheal aspirates associated with chronic lung disease. Early Hum Dev (1998) 51:13-22. doi:10.1016/S0378-3782(97)00069-8
74. Atochina-Vasserman EN, Bates SR, Zhang P, Abramova H, Zhang Z, Gonzales L, et al. Early alveolar epithelial dysfunction promotes lung inflammation in a mouse model of Hermansky-Pudlak syndrome. Am J Respir Crit Care Med (2011) 184:449-58. doi:10.1164/rccm.201011-1882OC
75. Polglase GR, Dalton RG, Nitsos I, Knox CL, Pillow JJ, Jobe AH, et al. Pulmonary vascular and alveolar development in preterm lambs chronically colonized with Ureaplasma parvum. Am J Physiol Lung Cell Mol Physiol (2010) 299:L232-41. doi:10.1152/ajplung.00369.2009
76. Kunzmann S, Speer CP, Jobe AH, Kramer BW. Antenatal inflammation induced tgf-beta1 but suppressed ctgf in preterm lungs. Am J Physiol Lung Cell Mol Physiol (2007) 292:L223-31. doi:10.1152/ajplung.00159.2006
77. Jankov RP, Tanswell AK. Growth factors, postnatal lung growth and bronchopulmonary dysplasia. Paediatr Respir Rev (2004) 5:S265-75. doi:10.1016/S1526-0542(04)90050-4
78. Thebaud B. Angiogenesis in lung development, injury and repair: implications for chronic lung disease of prematurity. Neonatology (2007) 91:291-7. doi:10.1159/000101344
79. De Paepe ME, Greco D, Mao Q. Angiogenesis-related gene expression profiling in ventilated preterm human lungs. Exp Lung Res (2010) 36:399-410. doi:10.3109/01902141003714031
80. De Paepe ME, Mao Q, Powell J, Rubin SE, DeKoninck P, Appel N, et al. Growth of pulmonary microvasculature in ventilated preterm infants. Am J Respir Crit Care Med (2006) 173:204-11. doi:10.1164/rccm.200506-927OC
81. Bland RD, Ling CY, Albertine KH, Carlton DP, MacRitchie AJ, Day RW, et al. Pulmonary vascular dysfunction in preterm lambs with chronic lung disease. Am J Physiol Lung Cell Mol Physiol (2003) 285(1):L76-85
82. Vyas-Read S, Shaul PW, Yuhanna IS, Willis BC. Nitric oxide attenuates epithelial-mesenchymal transition in alveolar epithelial cells. Am J Physiol Lung Cell Mol Physiol (2007) 293:L212-21. doi:10.1152/ajplung.00475.2006
83. Wark PA, Murphy V, Mattes J. The interaction between mother and fetus and the development of allergic asthma. Expert Rev Respir Med (2014) 8:57-66. doi:10.1586/17476348.2014.848795
84. Velten M, Hutchinson KR, Gorr MW, Wold LE, Lucchesi PA, Rogers LK. Systemic maternal inflammation and neonatal hyperoxia induces remodeling and left ventricular dysfunction in mice. PLoS One (2011) 6:e24544. doi:10.1371/journal.pone.0024544
85. Rose MJ, Stenger MR, Joshi MS, Welty SE, Bauer JA, Nelin LD. Inhaled nitric oxide decreases leukocyte trafficking in the neonatal mouse lung during exposure to >95% oxygen. Pediatr Res (2010) 67:244-9. doi:10.1203/PDR.0b013e3181ca0d93
86. Bose CL, Dammann CE, Laughon MM. Bronchopulmonary dysplasia and inflammatory biomarkers in the premature neonate. Arch Dis Child Fetal Neonatal Ed (2008) 93:F455-61. doi:10.1136/adc.2007.121327
87. Vento G, Tirone C, Lulli P, Capoluongo E, Ameglio F, Lozzi S, et al. Bronchoalveolar lavage fluid peptidomics suggests a possible matrix metalloproteinase-3 role in bronchopulmonary dysplasia. Intensive Care Med (2009) 35:2115-24. doi:10.1007/s00134-009-1646-6
88. Watterberg KL, Carmichael DF, Gerdes JS, Werner S, Backstrom C, Murphy S. Secretory leukocyte protease inhibitor and lung inflammation in developing bronchopulmonary dysplasia. J Pediatr (1994) 125:264-9. doi:10.1016/S0022-3476(94)70209-8
89. Weinberger B, Anwar M, Henien S, Sosnovsky A, Hiatt M, Jochnowitz N, et al. Association of lipid peroxidation with antenatal betamethasone and oxygen radial disorders in preterm infants. Biol Neonate (2004) 85:121-7. doi:10.1159/000074968
90. Poggi C, Giusti B, Vestri A, Pasquini E, Abbate R, Dani C. Genetic polymorphisms of antioxidant enzymes in preterm infants. J Matern Fetal Neonatal Med (2012) 25(Suppl 4):131-4. doi:10.3109/14767058.2012.714976
91. Buczynski BW, Maduekwe ET, O'Reilly MA. The role of hyperoxia in the pathogenesis of experimental bpd. Semin Perinatol (2013) 37:69-78. doi:10.1053/j.semperi.2013.01.002
92. Warner BB, Stuart LA, Papes RA, Wispe JR. Functional and pathological effects of prolonged hyperoxia in neonatal mice. Am J Physiol (1998) 275:L110-7
93. Bonikos DS, Bensch KG, Ludwin SK, Northway WH Jr. Oxygen toxicity in the newborn. The effect of prolonged 100 per cent o2 exposure on the lungs of newborn mice. Lab Invest (1975) 32:619-35
94. Maeda Y, Dave V, Whitsett JA. Transcriptional control of lung morphogenesis. Physiol Rev (2007) 87:219-44. doi:10.1152/physrev.00028.2006
95. Balasubramaniam V, Mervis CF, Maxey AM, Markham NE, Abman SH. Hyperoxia reduces bone marrow, circulating, and lung endothelial progenitor cells in the developing lung: implications for the pathogenesis of bronchopulmonary dysplasia. Am J Physiol Lung Cell Mol Physiol (2007) 292:L1073-84. doi:10.1152/ajplung.00347.2006
96. Buczynski BW, Yee M, Paige Lawrence B, O'Reilly MA. Lung development and the host response to influenza a virus are altered by different doses of neonatal oxygen in mice. Am J Physiol Lung Cell Mol Physiol (2012) 302:L1078-87. doi:10.1152/ajplung.00026.2012
97. Jobe AH, Ikegami M. Prevention of bronchopulmonary dysplasia. Curr Opin Pediatr (2001) 13:124-9. doi:10.1097/00008480-200104000-00006
98. Newman JB, Debastos AG, Batton D, Raz S. Neonatal respiratory dysfunction and neuropsychological performance at the preschool age: a study of very preterm infants with bronchopulmonary dysplasia. Neuropsychology (2011) 25:666-78. doi:10.1037/a0023895
99. Greenough A, Alexander J, Burgess S, Bytham J, Chetcuti PA, Hagan J, et al. Preschool healthcare utilisation related to home oxygen status. Arch Dis Child Fetal Neonatal Ed (2006) 91:F337-41. doi:10.1136/adc.2005.088823
100. Greenough A, Alexander J, Burgess S, Chetcuti PA, Cox S, Lenney W, et al. Home oxygen status and rehospitalisation and primary care requirements of infants with chronic lung disease. Arch Dis Child (2002) 86:40-3. doi:10.1136/adc.86.1.40
101. Greenough A, Cox S, Alexander J, Lenney W, Turnbull F, Burgess S, et al. Health care utilisation of infants with chronic lung disease, related to hospitalisation for RSV infection. Arch Dis Child (2001) 85:463-8. doi:10.1136/adc.85.6.463
102. Broughton S, Roberts A, Fox G, Pollina E, Zuckerman M, Chaudhry S, et al. Prospective study of healthcare utilisation and respiratory morbidity due to RSV infection in prematurely born infants. Thorax (2005) 60:1039-44. doi:10.1136/thx.2004.037853
103. Broughton S, Thomas MR, Marston L, Calvert SA, Marlow N, Peacock JL, et al. Very prematurely born infants wheezing at follow-up: lung function and risk factors. Arch Dis Child (2007) 92:776-80. doi:10.1136/adc.2006.112623
104. Yuksel B, Greenough A. Relationship of symptoms to lung function abnormalities in preterm infants at follow-up. Pediatr Pulmonol (1991) 11:202-6. doi:10.1002/ppul.1950110304
105. Pelkonen AS, Hakulinen AL, Turpeinen M. Bronchial lability and responsiveness in school children born very preterm. Am J Respir Crit Care Med (1997) 156:1178-84. doi:10.1164/ajrccm.156.4.9610028
106. Greenough A, Limb E, Marston L, Marlow N, Calvert S, Peacock J. Risk factors for respiratory morbidity in infancy after very premature birth. Arch Dis Child Fetal Neonatal Ed (2005) 90:F320-3. doi:10.1136/adc.2004.062018
107. Baraldi E, Carraro S, Filippone M. Bronchopulmonary dysplasia: definitions and long-term respiratory outcome. Early Hum Dev (2009) 85:S1-3. doi:10.1016/j.earlhumdev.2009.08.002
108. Gross SJ, Iannuzzi DM, Kveselis DA, Anbar RD. Effect of preterm birth on pulmonary function at school age: a prospective controlled study. J Pediatr (1998) 133:188-92. doi:10.1016/S0022-3476(98)70219-7
109. Northway WH Jr, Moss RB, Carlisle KB, Parker BR, Popp RL, Pitlick PT, et al. Late pulmonary sequelae of bronchopulmonary dysplasia. N Engl J Med (1990) 323:1793-9. doi:10.1056/NEJM199012273232603
110. Welsh L, Kirkby J, Lum S, Odendaal D, Marlow N, Derrick G, et al. The epicure study: maximal exercise and physical activity in school children born extremely preterm. Thorax (2010) 65:165-72. doi:10.1136/thx.2008.107474
111. Greenough A, Dimitriou G, Bhat RY, Broughton S, Hannam S, Rafferty GF, et al. Lung volumes in infants who had mild to moderate bronchopulmonary dysplasia. Eur J Pediatr (2005) 164(9):583-6. doi:10.1007/s00431-005-1706-z
112. Hjalmarson O, Sandberg KL. Lung function at term reflects severity of bronchopulmonary dysplasia. J Pediatr (2005) 146:86-90. doi:10.1016/j.jpeds.2004.08.044
113. Doyle LW, Faber B, Callanan C, Freezer N, Ford GW, Davis NM. Bronchopulmonary dysplasia in very low birth weight subjects and lung function in late adolescence. Pediatrics (2006) 118:108-13. doi:10.1542/peds.2005-2522
114. Filippone M, Carraro S, Baraldi E. From bpd to copd? The hypothesis is intriguing but we lack lung pathology data in humans. Eur Respir J (2010) 35:1419-20 author reply 1420. doi:10.1183/09031936.00013310
115. Bonvillain RW, Danchuk S, Sullivan DE, Betancourt AM, Semon JA, Eagle ME, et al. A nonhuman primate model of lung regeneration: detergent-mediated decellularization and initial in vitro recellularization with mesenchymal stem cells. Tissue Eng Part A (2012) 18(23-24):2437-52. doi:10.1089/ten.TEA.2011.0594
116. Jensen T, Roszell B, Zang F, Girard E, Matson A, Thrall R, et al. A rapid lung de-cellularization protocol supports embryonic stem cell differentiation in vitro and following implantation. Tissue Eng Part C Methods (2012) 18:632-46. doi:10.1089/ten.TEC.2011.0584
117. Ito Y, Betsuyaku T, Nagai K, Nasuhara Y, Nishimura M. Expression of pulmonary VEGF family declines with age and is further down-regulated in lipopolysaccharide (LPS)-induced lung injury. Exp Gerontol (2005) 40:315-23. doi:10.1016/j.exger.2005.01.009
118. Kamba T, Tam BY, Hashizume H, Haskell A, Sennino B, Mancuso MR, et al. VEGF-dependent plasticity of fenestrated capillaries in the normal adult microvasculature. Am J Physiol Heart Circ Physiol (2006) 290:H560-76. doi:10.1152/ajpheart.00133.2005
119. Yee M, White RJ, Awad HA, Bates WA, McGrath-Morrow SA, O'Reilly MA. Neonatal hyperoxia causes pulmonary vascular disease and shortens life span in aging mice. Am J Pathol (2011) 178:2601-10. doi:10.1016/j.ajpath.2011.02.010
120. Belik J, Jankov RP, Pan J, Yi M, Chaudhry I, Tanswell AK. Chronic O2 exposure in the newborn rat results in decreased pulmonary arterial nitric oxide release and altered smooth muscle response to isoprostane. J Appl Physiol (1985) 96(2):725-30
121. Filippone M, Bonetto G, Corradi M, Frigo AC, Baraldi E. Evidence of unexpected oxidative stress in airways of adolescents born very pre-term. Eur Respir J (2012) 40:1253-9. doi:10.1183/09031936.00185511
122. Iosef C, Alastalo TP, Hou Y, Chen C, Adams ES, Lyu SC, et al. Inhibiting NF-kappaB in the developing lung disrupts angiogenesis and alveolarization. Am J Physiol Lung Cell Mol Physiol (2012) 302:L1023-36. doi:10.1152/ajplung.00230.2011
123. Didon L, Roos AB, Elmberger GP, Gonzalez FJ, Nord M. Lung-specific inactivation of ccaat/enhancer binding protein alpha causes a pathological pattern characteristic of copd. Eur Respir J (2010) 35:186-97. doi:10.1183/09031936.00185008
124. Alvira CM, Abate A, Yang G, Dennery PA, Rabinovitch M. Nuclear factor-kappab activation in neonatal mouse lung protects against lipopolysaccharide-induced inflammation. Am J Respir Crit Care Med (2007) 175:805-15. doi:10.1164/rccm.200608-1162OC
125. Yang G, Abate A, George AG, Weng YH, Dennery PA. Maturational differences in lung nf-kappab activation and their role in tolerance to hyperoxia. J Clin Invest (2004) 114:669-78. doi:10.1172/JCI200419300
126. Hennessy EM, Bracewell MA, Wood N, Wolke D, Costeloe K, Gibson A, et al. Respiratory health in pre-school and school age children following extremely preterm birth. Arch Dis Child (2008) 93:1037-43. doi:10.1136/adc.2008.140830
127. Merritt TA, Deming DD, Boynton BR. The 'new' bronchopulmonary dysplasia: challenges and commentary. Semin Fetal Neonatal Med (2009) 14:345-57. doi:10.1016/j.siny.2009.08.009
128. Bal MP, de Vries WB, van Oosterhout MF, Baan J, van der Wall EE, van Bel F, et al. Long-term cardiovascular effects of neonatal dexamethasone treatment: hemodynamic follow-up by left ventricular pressure-volume loops in rats. J Appl Physiol (2008) 104:446-50. doi:10.1152/japplphysiol.00951.2007
129. Kamphuis PJ, de Vries WB, Bakker JM, Kavelaars A, van Dijk JE, Schipper ME, et al. Reduced life expectancy in rats after neonatal dexamethasone treatment. Pediatr Res (2007) 61:72-6. doi:10.1203/01.pdr.0000249980.95264.dd
130. Stoll BJ, Hansen N, Fanaroff AA, Wright LL, Carlo WA, Ehrenkranz RA, et al. Changes in pathogens causing early-onset sepsis in very-low-birth-weight infants. N Engl J Med (2002) 347:240-7. doi:10.1056/NEJMoa012657
131. Olszak T, An D, Zeissig S, Vera MP, Richter J, Franke A, et al. Microbial exposure during early life has persistent effects on natural killer T cell function. Science (2012) 336:489-93. doi:10.1126/science.1219328
132. Davis JM, Auten RL. Maturation of the antioxidant system and the effects on preterm birth. Semin Fetal Neonatal Med (2010) 15:191-5. doi:10.1016/j.siny.2010.04.001
133. Wright CJ, Kirpalani H. Targeting inflammation to prevent bronchopulmonary dysplasia: can new insights be translated into therapies? Pediatrics (2011) 128:111-26. doi:10.1542/peds.2010-3875
134. Davis JM, Parad RB, Michele T, Allred E, Price A, Rosenfeld W. North American Recombinant Human CuZn SODSG. Pulmonary outcome at 1 year corrected age in premature infants treated at birth with recombinant human cuzn superoxide dismutase. Pediatrics (2003) 111:469-76. doi:10.1542/peds.111.3.469
135. Kinsella JP, Parker TA, Davis JM, Abman SH. Superoxide dismutase improves gas exchange and pulmonary hemodynamics in premature lambs. Am J Respir Crit Care Med (2005) 172:745-9. doi:10.1164/rccm.200501-146OC
136. Parad RB, Allred EN, Rosenfeld WN, Davis JM. Reduction of retinopathy of prematurity in extremely low gestational age newborns treated with recombinant human cu/zn superoxide dismutase. Neonatology (2012) 102:139-44. doi:10.1159/000336639
137. Auten RL Jr, Mason SN, Tanaka DT, Welty-Wolf K, Whorton MH. Anti-neutrophil chemokine preserves alveolar development in hyperoxia-exposed newborn rats. Am J Physiol Lung Cell Mol Physiol (2001) 281(2):L336-44
138. Auten RL, Whorton MH, Nicholas Mason S. Blocking neutrophil influx reduces DNA damage in hyperoxia-exposed newborn rat lung. Am J Respir Cell Mol Biol (2002) 26:391-7. doi:10.1165/ajrcmb.26.4.4708
139. Patz A, Hoeck LE, De La Cruz E. Studies on the effect of high oxygen administration in retrolental fibroplasia. I. Nursery observations. Am J Ophthalmol (1952) 35:1248-53. doi:10.1016/0002-9394(52)91140-9
140. Askie LM, Henderson-Smart DJ, Irwig L, Simpson JM. Oxygen-saturation targets and outcomes in extremely preterm infants. N Engl J Med (2003) 349:959-67. doi:10.1056/NEJMoa023080
141. Carlo WA, Finer NN, Walsh MC, Rich W, Gantz MG, Laptook AR, et al. Target ranges of oxygen saturation in extremely preterm infants. N Engl J Med (2010) 362:1959-69. doi:10.1056/NEJMoa0911781
142. BOOST II United Kingdom Collaborative Group, BOOST II Australia Collaborative Group, BOOST II New Zealand Collaborative Group; Stenson BJ, Tarnow-Mordi WO, Darlow BA, et al. Oxygen saturation and outcomes in preterm infants. N Engl J Med (2013) 368:2094-104. doi:10.1056/NEJMoa1302298
143. Supplemental therapeutic oxygen for prethreshold retinopathy of prematurity (STOP-ROP), a randomized, controlled trial. I: primary outcomes. Pediatrics (2000) 105(2):295-310. doi:10.1542/peds.105.2.295
144. Stevens TP, Dylag A, Panthagani I, Pryhuber G, Halterman J. Effect of cumulative oxygen exposure on respiratory symptoms during infancy among VLBW infants without bronchopulmonary dysplasia. Pediatr Pulmonol (2010) 45:371-9. doi:10.1002/ppul.21199
145. Maduekwe ET, Buczynski BW, Yee M, Rangasamy T, Stevens TP, Lawrence BP, et al. Cumulative neonatal oxygen exposure predicts response of adult mice infected with influenza a virus. Pediatr Pulmonol (2014). doi:10.1002/ppul.23063
146. Coalson JJ, Winter VT, Siler-Khodr T, Yoder BA. Neonatal chronic lung disease in extremely immature baboons. Am J Respir Crit Care Med (1999) 160:1333-46. doi:10.1164/ajrccm.160.4.9810071
147. Awasthi S, Coalson JJ, Yoder BA, Crouch E, King RJ. Deficiencies in lung surfactant proteins a and d are associated with lung infection in very premature neonatal baboons. Am J Respir Crit Care Med (2001) 163:389-97. doi:10.1164/ajrccm.163.2.2004168
148. Yoder BA, Siler-Khodr T, Winter VT, Coalson JJ. High-frequency oscillatory ventilation: effects on lung function, mechanics, and airway cytokines in the immature baboon model for neonatal chronic lung disease. Am J Respir Crit Care Med (2000) 162:1867-76. doi:10.1164/ajrccm.162.5.9912145
149. Maniscalco WM, Watkins RH, Pryhuber GS, Bhatt A, Shea C, Huyck H. Angiogenic factors and alveolar vasculature: development and alterations by injury in very premature baboons. Am J Physiol Lung Cell Mol Physiol (2002) 282(4):L811-23
150. 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(5):L749-58
151. Yoder BA, Coalson JJ, Winter VT, Siler-Khodr T, Duffy LB, Cassell GH. Effects of antenatal colonization with Ureaplasma urealyticum on pulmonary disease in the immature baboon. Pediatr Res (2003) 54:797-807. doi:10.1203/01.PDR.0000091284.84322.16
152. 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 Cell Mol Physiol (2005) 288:L450-9. doi:10.1152/ajplung.00347.2004
153. Thomson MA, Yoder BA, Winter VT, Martin H, Catland D, Siler-Khodr TM, et al. Treatment of immature baboons for 28 days with early nasal continuous positive airway pressure. Am J Respir Crit Care Med (2004) 169:1054-62. doi:10.1164/rccm.200309-1276OC
154. Albertine KH, Jones GP, Starcher BC, Bohnsack JF, Davis PL, Cho SC, et al. Chronic lung injury in preterm lambs. Disordered respiratory tract development. Am J Respir Crit Care Med (1999) 159:945-58. doi:10.1164/ajrccm.159.3.9804027
155. Bland RD, Albertine KH, Carlton DP, Kullama L, Davis P, Cho SC, et al. Chronic lung injury in preterm lambs: abnormalities of the pulmonary circulation and lung fluid balance. Pediatr Res (2000) 48:64-74. doi:10.1203/00006450-200007000-00013
156. Maeta H, Raju TN, Vidyasagar D, Bhat R, Esterly J, Matsuda H, et al. Effect of exogenous surfactant on the development of bronchopulmonary dysplasia in a baboon hyaline membrane disease model. Crit Care Med (1990) 18:403-9. doi:10.1097/00003246-199004000-00011
157. Shimada S, Raju TN, Vidyasagar D, Maeta H, Bhat R. Chest radiographic course after exogenous surfactant therapy in baboons with respiratory distress syndrome. Crit Care Med (1990) 18:969-73. doi:10.1097/00003246-199009000-00013
158. Kinsella JP, Gerstmann DR, Clark RH, Null DM Jr, Morrow WR, Taylor AF, et al. High-frequency oscillatory ventilation versus intermittent mandatory ventilation: early hemodynamic effects in the premature baboon with hyaline membrane disease. Pediatr Res (1991) 29:160-6. doi:10.1203/00006450-199102000-00012