Positive end-expiratory pressure and surfactant decrease lung injury during initiation of ventilation in fetal sheep

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 301, Issue 5, 2011, Pages

  Hillman, Noah H ^a   Nitsos, Ilias ^b   Berry, Clare ^b   Pillow, J Jane ^b   Kallapur, Suhas G ^a,b   Jobe, Alan H ^a,b  

^a UNIVERSITY OF CINCINNATI   (United States)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Acute phase response genes; Bronchopulmonary dysplasia; Lung inflammation; Prematurity; Respiratory distress syndrome

Indexed keywords

EARLY GROWTH RESPONSE FACTOR 1; HEAT SHOCK PROTEIN 60; HEAT SHOCK PROTEIN 70; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; NITROGEN; PORACTANT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ARTIFICIAL VENTILATION; CYTOKINE RELEASE; FETUS; GESTATIONAL AGE; HUMIDITY; HYSTEROTOMY; LUNG COMPLIANCE; LUNG FLUID; LUNG INJURY; LUNG LAVAGE; LUNG PARENCHYMA; NONHUMAN; OBSTETRIC ANESTHESIA; PEAK INSPIRATORY FLOW; PLACENTA CIRCULATION; POSITIVE END EXPIRATORY PRESSURE; PRIORITY JOURNAL; SHEEP; TIDAL VOLUME; TREATMENT OUTCOME;

ANIMALS; BLOTTING, WESTERN; BRONCHOALVEOLAR LAVAGE FLUID; CYTOKINES; FEMALE; FETUS; GESTATIONAL AGE; HEAT-SHOCK PROTEINS; HUMANS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; INFANT, NEWBORN; INFANT, PREMATURE, DISEASES; LUNG; LUNG INJURY; POSITIVE-PRESSURE RESPIRATION; PULMONARY SURFACTANTS; RESPIRATORY DISTRESS SYNDROME, NEWBORN; RNA, MESSENGER; SHEEP, DOMESTIC; TIDAL VOLUME;

EID: 80055116704     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00157.2011     Document Type: Article

References (61)

1. Abman SH. Impaired vascular endothelial growth factor signaling in the pathogenesis of neonatal pulmonary vascular disease. Adv Exp Med Biol 661: 323-335, 2010.
2. Ball MK, Jobe AH, Polglase GR, Kallapur SG, Cheah FC, Hillman NH, Pillow JJ. High and low body temperature during the initiation of ventilation for near-term lambs. Resuscitation 80: 133-137, 2009.
3. Bjorklund LL, Ingimarsson J, Curstedt T, John J, Robertson B, Werner O, Vilstrup CT. Manual ventilation with a few large breaths at birth compromises the therapeutic effect of subsequent surfactant replacement in immature lambs. Pediatr Res 42: 348-355, 1997.
4. Brigstock DR. The CCN family: a new stimulus package. J Endocrinol 178: 169-175, 2003.
5. Cattarossi L, Copetti R, Poskurica B, Miserocchi G. Surfactant administration for neonatal respiratory distress does not improve lung interstitial fluid clearance: echographic and experimental evidence. J Perinat Med 38: 557-563, 2010.
6. Chaqour B, Goppelt-Struebe M. Mechanical regulation of the Cyr61/CCN1 and CTGF/CCN2 proteins. FEBS J 273: 3639-3649, 2006.
7. Chase MA, Wheeler DS, Lierl KM, Hughes VS, Wong HR, Page K. Hsp72 induces inflammation and regulates cytokine production in airway epithelium through a TLR4- and NF-kappaB-dependent mechanism. J Immunol 179: 6318-6324, 2007.
8. Cheah FC, Pillow JJ, Kramer BW, Polglase GR, Nitsos I, Newnham JP, Jobe AH, Kallapur SG. Airway inflammatory cell responses to intra-amniotic lipopolysaccharide in a sheep model of chorioamnionitis. Am J Physiol Lung Cell Mol Physiol 296: L384-L393, 2009.
9. Chen S, Ron M, Platteau A, Hehre D, Smith H, Ruiz P, Whitsett JA, Bancalari E, Wu S. CTGF disrupts alveolarization and induces pulmonary hypertension in neonatal mice: implication in the pathogenesis of severe bronchopulmonary dysplasia. Am J Physiol Lung Cell Mol Physiol 300: L330-L340, 2011.
10. Cheng Z, Volkers M, Din S, Avitabile D, Khan M, Gude N, Mohsin S, Bo T, Truffa S, Alvarez R, Mason M, Fischer KM, Konstandin MH, Zhang XK, Brown JH, Sussman MA. Mitochondrial translocation of Nur77 mediates cardiomyocyte apoptosis. Eur Heart J. In press.
11. Copland IB, Kavanagh BP, Engelberts D, McKerlie C, Belik J, Post M. Early changes in lung gene expression due to high tidal volume. Am J Respir Crit Care Med 168: 1051-1059, 2003.
12. Dawson JA, Schmolzer GM, Kamlin CO, Te Pas AB, O'Donnell CP, Donath SM, Davis PG, Morley CJ. Oxygenation with T-piece vs. self-inflating bag for ventilation of extremely preterm infants at birth: a randomized controlled trial. J Pediatr 158: 912-918.e1-e2, 2011.
13. De Paepe ME, Greco D, Mao Q. Angiogenesis-related gene expression profiling in ventilated preterm human lungs. Exp Lung Res 36: 399-410, 2010.
14. Dolinay T, Kaminski N, Felgendreher M, Kim HP, Reynolds P, Watkins SC, Karp D, Uhlig S, Choi AM. Gene expression profiling of target genes in ventilator-induced lung injury. Physiol Genomics 26: 68-75, 2006.
15. Fanaroff AA, Stoll BJ, Wright LL, Carlo WA, Ehrenkranz RA, Stark AR, Bauer CR, Donovan EF, Korones SB, Laptook AR, Lemons JA, Oh W, Papile LA, Shankaran S, Stevenson DK, Tyson JE, Poole WK. Trends in neonatal morbidity and mortality for very low birthweight infants. Am J Obstet Gynecol 196: 147 e141-e148, 2007.
16. Finer NN, Carlo WA, Walsh MC, Rich W, Gantz MG, Laptook AR, Yoder BA, Faix RG, Das A, Poole WK, Donovan EF, Newman NS, Ambalavanan N, Frantz ID, 3rd Buchter S, Sanchez PJ, Kennedy KA, Laroia N, Poindexter BB, Cotten CM, Van Meurs KP, Duara S, Narendran V, Sood BG, O'Shea TM, Bell EF, Bhandari V, Watterberg KL, Higgins RD. Early CPAP versus surfactant in extremely preterm infants. N Engl J Med 362: 1970-1979, 2010.
17. Hillman N, Kallapur SG, Pillow JJ, Polglase GR, Nitsos I, Ikegami M, Jobe AH. Inhibitors of inflammation and endogenous surfactant pool size as modulators of lung injury with initiation of ventilation in preterm sheep. Respir Res 11: 151, 2010.
18. Hillman NH, Kallapur SG, Pillow JJ, Moss TJ, Polglase GR, Nitsos I, Jobe AH. Airway injury from initiating ventilation in preterm sheep. Pediatr Res 67: 60-65, 2010.
19. Hillman NH, Moss TJ, Kallapur SG, Bachurski C, Pillow JJ, Polglase GR, Nitsos I, Kramer BW, Jobe AH. Brief, large tidal volume ventilation initiates lung injury and a systemic response in fetal sheep. Am J Respir Crit Care Med 176: 575-581, 2007.
20. Hillman NH, Polglase GR, Jane Pillow J, Saito M, Kallapur SG, Jobe AH. Inflammation and lung maturation from stretch injury in preterm fetal sheep. Am J Physiol Lung Cell Mol Physiol 300: L232-L241, 2011.
21. Huh D, Fujioka H, Tung YC, Futai N, Paine R 3rd, Grotberg JB, Takayama S. Acoustically detectable cellular-level lung injury induced by fluid mechanical stresses in microfluidic airway systems. Proc Natl Acad Sci U S A 104: 18886-18891, 2007.
22. Ikegami M, Jobe AH, Yamada T, Seidner S. Relationship between alveolar saturated phosphatidylcholine pool sizes and compliance of preterm rabbit lungs. The effect of maternal corticosteroid treatment. Am Rev Respir Dis 139: 367-369, 1989.
23. Inoki I, Shiomi T, Hashimoto G, Enomoto H, Nakamura H, Makino K, Ikeda E, Takata S, Kobayashi K, Okada Y. Connective tissue growth factor binds vascular endothelial growth factor (VEGF) and inhibits VEGF-induced angiogenesis. FASEB J 16: 219-221, 2002.
24. Jin Y, Kim HP, Ifedigbo E, Lau LF, Choi AM. Cyr61 protects against hyperoxia-induced cell death via Akt pathway in pulmonary epithelial cells. Am J Respir Cell Mol Biol 33: 297-302, 2005.
25. Jobe A, Kramer BW, Moss TJ, Newnham J, Ikegami M. Decreased indicators of lung injury with continuous positive expiratory pressure in preterm lambs. Pediatr Res 52: 387-392, 2002.
26. Jobe AH, Hillman N, Polglase G, Kramer BW, Kallapur S, Pillow J. Injury and inflammation from resuscitation of the preterm infant. Neonatology 94: 190-196, 2008.
27. Kallapur SG, Nitsos I, Moss TJ, Polglase GR, Pillow JJ, Cheah FC, Kramer BW, Newnham JP, Ikegami M, Jobe AH. IL-1 mediates pulmonary and systemic inflammatory responses to chorioamnionitis induced by LPS. Am J Respir Crit Care Med 179: 955-961, 2009.
28. Kattwinkel J, Perlman JM, Aziz K, Colby C, Fairchild K, Gallagher J, Hazinski MF, Halamek LP, Kumar P, Little G, McGowan JE, Nightengale B, Ramirez MM, Ringer S, Simon WM, Weiner GM, Wyckoff M, Zaichkin J. Neonatal resuscitation: 2010 American Heart Association Guidelines for Cardiopulmonary Resuscitation and Emergency Cardiovascular Care. Pediatrics 126: e1400-e1413, 2010.
29. Kendig JW, Ryan RM, Sinkin RA, Maniscalco WM, Notter RH, Guillet R, Cox C, Dweck HS, Horgan MJ, Reubens LJ, Risemberg H, Phelps DL. Comparison of two strategies for surfactant prophylaxis in very premature infants: a multicenter randomized trial. Pediatrics 101: 1006-1012, 1998.
30. Kramer BW, Ikegami M, Moss TJ, Nitsos I, Newnham JP, Jobe AH. Endotoxin-induced chorioamnionitis modulates innate immunity of monocytes in preterm sheep. Am J Respir Crit Care Med 171: 73-77, 2005.
31. Kramer BW, Moss TJ, Willet KE, Newnham JP, Sly PD, Kallapur SG, Ikegami M, Jobe AH. Dose and time response after intraamniotic endotoxin in preterm lambs. Am J Respir Crit Care Med 164: 982-988, 2001.
32. Laughon M, O'Shea MT, Allred EN, Bose C, Kuban K, Van Marter LJ, Ehrenkranz RA, Leviton A. Chronic lung disease and developmental delay at 2 years of age in children born before 28 weeks' gestation. Pediatrics 124: 637-648, 2009.
33. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265-275, 1951.
34. Menendez JA, Mehmi I, Griggs DW, Lupu R. The angiogenic factor CYR61 in breast cancer: molecular pathology and therapeutic perspectives. Endocr Relat Cancer 10: 141-152, 2003.
35. Michna J, Jobe AH, Ikegami M. Positive end-expiratory pressure preserves surfactant function in preterm lambs. Am J Respir Crit Care Med 160: 634-639, 1999.
36. Morley CJ, Davis PG, Doyle LW, Brion LP, Hascoet JM, Carlin JB. Nasal CPAP or intubation at birth for very preterm infants. N Engl J Med 358: 700-708, 2008.
37. Mulrooney N, Champion Z, Moss TJ, Nitsos I, Ikegami M, Jobe AH. Surfactant and physiological responses of preterm lambs to continuous positive airway pressure. Am J Respir Crit Care Med 171: 1-6, 2005.
38. Musk GC, Polglase GR, Bunnell JB, McLean CJ, Nitsos I, Song Y, Pillow JJ. High positive end-expiratory pressure during high frequency jet ventilation improves oxygenation and ventilation in preterm lambs. Pediatr Res 69: 319-324, 2011.
39. Naik AS, Kallapur SG, Bachurski CJ, Jobe AH, Michna J, Kramer BW, Ikegami M. Effects of ventilation with different positive endexpiratory pressures on cytokine expression in the preterm lamb lung. Am J Respir Crit Care Med 164: 494-498, 2001.
40. Ogawa A, Brown CL, Schlueter MA, Benson BJ, Clements JA, Hawgood S. Lung function, surfactant apoprotein content, and level of PEEP in prematurely delivered rabbits. J Appl Physiol 77: 1840-1849, 1994.
41. Pearen MA, Muscat GE. Minireview: Nuclear hormone receptor 4A signaling: implications for metabolic disease. Mol Endocrinol 24: 1891-1903, 2010.
42. Pepe PE, Hudson LD, Carrico CJ. Early application of positive endexpiratory pressure in patients at risk for the adult respiratory-distress syndrome. N Engl J Med 311: 281-286, 1984.
43. Polglase GR, Hillman NH, Ball MK, Kramer BW, Kallapur SG, Jobe AH, Pillow JJ. Lung and systemic inflammation in preterm lambs on continuous positive airway pressure or conventional ventilation. Pediatr Res 65: 67-71, 2009.
44. Polglase GR, Hillman NH, Pillow JJ, Cheah FC, Nitsos I, Moss TJ, Kramer BW, Ikegami M, Kallapur SG, Jobe AH. Positive end-expiratory pressure and tidal volume during initial ventilation of preterm lambs. Pediatr Res 64: 517-522, 2008.
45. Probyn ME, Hooper SB, Dargaville PA, McCallion N, Crossley K, Harding R, Morley CJ. Positive end expiratory pressure during resuscitation of premature lambs rapidly improves blood gases without adversely affecting arterial pressure. Pediatr Res 56: 198-204, 2004.
46. Rider ED, Jobe AH, Ikegami M, Sun B. Different ventilation strategies alter surfactant responses in preterm rabbits. J Appl Physiol 73: 2089-2096, 1992.
47. Santiago VR, Rzezinski AF, Nardelli LM, Silva JD, Garcia CS, Maron-Gutierrez T, Ornellas DS, Morales MM, Capelozzi VL, Marini J, Pelosi P, Rocco PR. Recruitment maneuver in experimental acute lung injury: the role of alveolar collapse and edema. Crit Care Med 38: 2207-2214, 2010.
48. Schild C, Trueb B. Three members of the connective tissue growth factor family CCN are differentially regulated by mechanical stress. Biochim Biophys Acta 1691: 33-40, 2004.
49. Schmolzer GM, Kamlin OC, O'Donnell CP, Dawson JA, Morley CJ, Davis PG. Assessment of tidal volume and gas leak during mask ventilation of preterm infants in the delivery room. Arch Dis Child Fetal Neonatal Ed 95: F393-F397, 2010.
50. Shah TA, Hillman NH, Nitsos I, Polglase GR, Pillow JJ, Newnham JP, Jobe AH, Kallapur SG. Pulmonary and systemic expression of monocyte chemotactic proteins in preterm sheep fetuses exposed to lps induced chorioamnionitis. Pediatr Res 68: 210-215, 2010.
51. Siew ML, Te Pas AB, Wallace MJ, Kitchen MJ, Islam M, Lewis RA, Fouras A, Morley CJ, Davis PG, Yagi N, Uesugi K, Hooper SB. Surfactant increases the uniformity of lung aeration at birth in ventilated preterm rabbits. Pediatr Res 70: 50-55, 2011.
52. Siew ML, Te Pas AB, Wallace MJ, Kitchen MJ, Lewis RA, Fouras A, Morley CJ, Davis PG, Yagi N, Uesugi K, Hooper SB. Positive endexpiratory pressure enhances development of a functional residual capacity in preterm rabbits ventilated from birth. J Appl Physiol 106: 1487-1493, 2009.
53. Staffieri F, Driessen B, Monte VD, Grasso S, Crovace A. Effects of positive end-expiratory pressure on anesthesia-induced atelectasis and gas exchange in anesthetized and mechanically ventilated sheep. Am J Vet Res 71: 867-874, 2010.
54. Tong X, O'Kelly J, Xie D, Mori A, Lemp N, McKenna R, Miller CW, Koeffler HP. Cyr61 suppresses the growth of non-small-cell lung cancer cells via the beta-catenin-c-myc-p53 pathway. Oncogene 23: 4847-4855, 2004.
55. Wada K, Jobe AH, Ikegami M. Tidal volume effects on surfactant treatment responses with the initiation of ventilation in preterm lambs. J Appl Physiol 83: 1054-1061, 1997.
56. Wallace MJ, Probyn ME, Zahra VA, Crossley K, Cole TJ, Davis PG, Morley CJ, Hooper SB. Early biomarkers and potential mediators of ventilation-induced lung injury in very preterm lambs. Respiratory research 10: 19, 2009.
57. Wu H, Lin Y, Li W, Sun Z, Gao W, Zhang H, Xie L, Jiang F, Qin B, Yan T, Chen L, Zhao Y, Cao X, Wu Y, Lin B, Zhou H, Wong AS, Zhang XK, Zeng JZ. Regulation of Nur77 expression by beta-catenin and its mitogenic effect in colon cancer cells. FASEB J 25: 192-205, 2011.
58. Yang H, Bushue N, Bu P, Wan YJ. Induction and intracellular localization of Nur77 dictate fenretinide-induced apoptosis of human liver cancer cells. Biochem Pharmacol 79: 948-954, 2010.
59. Zeng H, Qin L, Zhao D, Tan X, Manseau EJ, Van Hoang M, Senger DR, Brown LF, Nagy JA, Dvorak HF. Orphan nuclear receptor TR3/Nur77 regulates VEGF-A-induced angiogenesis through its transcriptional activity. J Exp Med 203: 719-729, 2006.
60. Zhao D, Qin L, Bourbon PM, James L, Dvorak HF, Zeng H. Orphan nuclear transcription factor TR3/Nur77 regulates microvessel permeability by targeting endothelial nitric oxide synthase and destabilizing endothelial junctions. Proc Natl Acad Sci U S A 108: 12066-12071, 2011.
61. Zhao Y, Bruemmer D. NR4A orphan nuclear receptors: transcriptional regulators of gene expression in metabolism and vascular biology. Arterioscler Thromb Vasc Biol 30: 1535-1541, 2010.