Respiratory consequences of prematurity: evolution of a diagnosis and development of a comprehensive approach

Nathalie L Maitre, Roberta A Ballard, Jonas H Ellenberg, Stephanie D Davis, James M Greenberg, Aaron Hamvas, Gloria S Pryhuber, Prematurity and Respiratory Outcomes Program, Claire Chougnet, Robert Frenk, James M Greenberg, William Hardie, Alan H Jobe, Karen McDowell, Barbara Alexander, Tari Gratton, Cathy Grigsby, Beth Koch, Kelly Thornton, Thomas Ferkol, Aaron Hamvas, Mark R Holland, James Kemp, Philip T Levy, Phillip Tarr, Gautam K Singh, Barbara Warner, Pamela Bates, Claudia Cleveland, Julie Hoffmann, Laura Linneman, Jayne Sicard-Su, Gina Simpson, Philip L Ballard, Roberta A Ballard, David J Durand, Eric C Eichenwald, Roberta L Keller, Amir M Khan, Leslie Lusk, Jeffrey D Merrill, Dennis W Nielson, Elizabeth E Rogers, Jeanette M Asselin, Samantha Balan, Katrina Burson, Cheryl Chapin, Erna Josiah-Davis, Carmen Garcia, Hart Horneman, Rick Hinojosa, Christopher Johnson, Susan Kelley, Karin L Knowles, M Layne Lillie, Karen Martin, Sarah Martin, Julie Arldt-McAlister, Lori Pacello, Shawna Rodgers, Daniel K Sperry, Scott Guthrie, Paul Moore, Marshall Summar, Amy B Beller, Theresa J Rogers, Steven Steele, Sharon Wadley, Carl D'Angio, Vasanth Kumar, Tom Mariani, Gloria Pryhuber, Clement Ren, Anne Marie Reynolds, Rita M Ryan, Kristin Scheible, Timothy Stevens, Shannon Castiglione, Aimee Horan, Deanna Maffet, Jane O'Donnell, Michael Sacilowski, Tanya Scalise, Elizabeth Werner, Jason Zayac, Heidie Huyck, Valerie Lunger, Kim Bordeaux, Pam Brown, Julia Epping, Lisa Flattery-Walsh, Donna Germuga, Nancy Jenks, Mary Platt, Eileen Popplewell, Sandra Prentice, C Michael Cotten, Kim Fisher, Jack Sharp, Judith A Voynow, Kim Ciccio, Stephanie Davis, Brenda Poindexter, Charles Clem, Susan Gunn, Lauren Jewett, Jonas Ellenberg, Rui Feng, Melissa Fernando, Howard Panitch, Barbara Schmidt, Pamela Shaw, Ann Tierney, Maria Blanco, Denise Cifelli, Sara DeMauro, Lynn M Taussig, Nathalie L Maitre, Roberta A Ballard, Jonas H Ellenberg, Stephanie D Davis, James M Greenberg, Aaron Hamvas, Gloria S Pryhuber, Prematurity and Respiratory Outcomes Program, Claire Chougnet, Robert Frenk, James M Greenberg, William Hardie, Alan H Jobe, Karen McDowell, Barbara Alexander, Tari Gratton, Cathy Grigsby, Beth Koch, Kelly Thornton, Thomas Ferkol, Aaron Hamvas, Mark R Holland, James Kemp, Philip T Levy, Phillip Tarr, Gautam K Singh, Barbara Warner, Pamela Bates, Claudia Cleveland, Julie Hoffmann, Laura Linneman, Jayne Sicard-Su, Gina Simpson, Philip L Ballard, Roberta A Ballard, David J Durand, Eric C Eichenwald, Roberta L Keller, Amir M Khan, Leslie Lusk, Jeffrey D Merrill, Dennis W Nielson, Elizabeth E Rogers, Jeanette M Asselin, Samantha Balan, Katrina Burson, Cheryl Chapin, Erna Josiah-Davis, Carmen Garcia, Hart Horneman, Rick Hinojosa, Christopher Johnson, Susan Kelley, Karin L Knowles, M Layne Lillie, Karen Martin, Sarah Martin, Julie Arldt-McAlister, Lori Pacello, Shawna Rodgers, Daniel K Sperry, Scott Guthrie, Paul Moore, Marshall Summar, Amy B Beller, Theresa J Rogers, Steven Steele, Sharon Wadley, Carl D'Angio, Vasanth Kumar, Tom Mariani, Gloria Pryhuber, Clement Ren, Anne Marie Reynolds, Rita M Ryan, Kristin Scheible, Timothy Stevens, Shannon Castiglione, Aimee Horan, Deanna Maffet, Jane O'Donnell, Michael Sacilowski, Tanya Scalise, Elizabeth Werner, Jason Zayac, Heidie Huyck, Valerie Lunger, Kim Bordeaux, Pam Brown, Julia Epping, Lisa Flattery-Walsh, Donna Germuga, Nancy Jenks, Mary Platt, Eileen Popplewell, Sandra Prentice, C Michael Cotten, Kim Fisher, Jack Sharp, Judith A Voynow, Kim Ciccio, Stephanie Davis, Brenda Poindexter, Charles Clem, Susan Gunn, Lauren Jewett, Jonas Ellenberg, Rui Feng, Melissa Fernando, Howard Panitch, Barbara Schmidt, Pamela Shaw, Ann Tierney, Maria Blanco, Denise Cifelli, Sara DeMauro, Lynn M Taussig

Abstract

Bronchopulmonary dysplasia (BPD) is the most common respiratory consequence of premature birth and contributes to significant short- and long-term morbidity, mortality and resource utilization. Initially defined as a radiographic, clinical and histopathological entity, the chronic lung disease known as BPD has evolved as obstetrical and neonatal care have improved the survival of lower gestational age infants. Now, definitions based on the need for supplementary oxygen at 28 days and/or 36 weeks provide a useful reference point in the neonatal intensive-care unit (NICU), but are no longer based on histopathological findings, and are neither designed to predict longer term respiratory consequences nor to study the evolution of a multifactorial disease. The aims of this review are to critically examine the evolution of the diagnosis of BPD and the challenges inherent to current classifications. We found that the increasing use of respiratory support strategies that administer ambient air without supplementary oxygen confounds oxygen-based definitions of BPD. Furthermore, lack of reproducible, genetic, biochemical and physiological biomarkers limits the ability to identify an impending BPD for early intervention, quantify disease severity for standardized classification and approaches and reliably predict the long-term outcomes. More comprehensive, multidisciplinary approaches to overcome these challenges involve longitudinal observation of extremely preterm infants, not only those with BPD, using genetic, environmental, physiological and clinical data as well as large databases of patient samples. The Prematurity and Respiratory Outcomes Program (PROP) will provide such a framework to address these challenges through high-resolution characterization of both NICU and post-NICU discharge outcomes.

Figures

Figure 1
Figure 1
Continuum of evaluation in lung disease of prematurity. In addition to clinical and medication data information, a series of biospecimens obtained during the NICU hospitalization can provide valuable evidence and mechanisms for disease. Physiologic testing of pulmonary function, and physical and observational assessments of pulmonary function, technology and health care utilization must occur both in the NICU and at 1 year corrected age to address a continuum of function. Neurodevelopmental outcomes are indirectly but importantly linked with lung disease of prematurity and are therefore designated by dotted lines.

References

    1. Martin JA, Hamilton BE, Ventura SJ, Osterman MJK, Mathews TJ. Births: Final Data for 2011. In: Services USDoHaH, editor. National Vital Statistics Reports. National Center of Health Statistics; Hyattsville, MD: 2013. pp. 1–69.
    1. Vom Hove M, Prenzel F, Uhlig HH, Robel-Tillig E. Pulmonary outcome in former preterm, very low birth weight children with bronchopulmonary dysplasia: a case-control follow-up at school age. J Pediatr. 2014;164(1):40–45. e44.
    1. Halterman JS, Lynch KA, Conn KM, Hernandez TE, Perry TT, Stevens TP. Environmental exposures and respiratory morbidity among very low birth weight infants at 1 year of life. Arch Dis Child. 2009;94(1):28–32.
    1. Peacock JL, Marston L, Marlow N, Calvert SA, Greenough A. Neonatal and infant outcome in boys and girls born very prematurely. Pediatr Res. 2012;71(3):305–310.
    1. Walsh MC, Wilson-Costello D, Zadell A, Newman N, Fanaroff A. Safety, reliability, and validity of a physiologic definition of bronchopulmonary dysplasia. J Perinatol. 2003;23(6):451–456.
    1. Lovering AT, Elliott JE, Laurie SS, Beasley KM, Gust CE, Mangum TS, et al. Ventilatory and sensory responses in adult survivors of preterm birth and bronchopulmonary dysplasia with reuced exercise capacity. Ann Am Thorac Soc. 2014;11(10):1528–1537.
    1. Clemm HH, Vollsaeter M, Roksund OD, Eide GE, Markestad T, Halvorsen T. Exercise capacity after extremely preterm birth. Development from adolescence to adulthood. Ann Am Thorac Soc. 2014;11(4):537–545.
    1. 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(4):F320–323.
    1. NHLBI, Division of Lung Diseases and Office of Prevention Education and Control. 1998 Publication No. 98-4081.
    1. Underwood MA, Danielsen B, Gilbert WM. Cost, causes and rates of rehospitalization of preterm infants. J Perinatol. 2007;27:614–619.
    1. 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(1):108–113.
    1. Stroustrup A, Trasande L. Epidemiological Characteristics and Resource Use in Neonates With Bronchopulmonary Dysplasia: 1993–2006. Pediatrics. 2010126(2):291–297.
    1. Northway WH, Jr., Rosan RC, Porter DY. Pulmonary disease following respirator therapy of hyaline-membrane disease. Bronchopulmonary dysplasia. N Engl J Med. 1967;276(7):357–368.
    1. Tooley WH. Epidemiology of bronchopulmonary dysplasia. J Pediatr. 1979;95(5 Pt 2):851–858.
    1. Shennan AT, Dunn MS, Ohlsson A, Lennox K, Hoskins EM. Abnormal pulmonary outcomes in premature infants: prediction from oxygen requirement in the neonatal period. Pediatrics. 1988;82(4):527–532.
    1. Jobe AJ. The new BPD: an arrest of lung development. Pediatr Res. 1999;46(6):641–643.
    1. Jobe AH, Bancalari E. Bronchopulmonary dysplasia. Am J Respir Crit Care Med. 2001;163(7):1723–1729.
    1. Walsh MC, Yao Q, Gettner P, Hale E, Collins M, Hensman A, et al. Impact of a physiologic definition on bronchopulmonary dysplasia rates. Pediatrics. 2004;114(5):1305–1311.
    1. Natarajan G, Pappas A, Shankaran S, Kendrick DE, Das A, Higgins RD, et al. Outcomes of extremely low birth weight infants with bronchopulmonary dysplasia: impact of the physiologic definition. Early Hum Dev. 2012;88(7):509–515.
    1. Ryan RM. A new look at bronchopulmonary dysplasia classification. J Perinatol. 2006;26(4):207–209.
    1. Beam KS, Aliaga S, Ahlfeld SK, Cohen-Wolkowiez M, Smith PB, Laughon MM. A systematic review of randomized controlled trials for the prevention of bronchopulmonary dysplasia in infants. J Perinatol. 2014;34(9):705–710.
    1. 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(6):1353–1360.
    1. Lefkowitz W, Rosenberg SH. Bronchopulmonary dysplasia: pathway from disease to long-term outcome. J Perinatol. 2008;28(12):837–840.
    1. Kaplan E, Bar-Yishay E, Prais D, Klinger G, Mei-Zahav M, Mussaffi H, et al. Encouraging pulmonary outcome for surviving, neurologically intact, extremely premature infants in the postsurfactant era. Chest. 2012;142(3):725–733.
    1. Cazzato S, Ridolfi L, Bernardi F, Faldella G, Bertelli L. Lung function outcome at school age in very low birth weight children. Pediatr Pulmonol. 2013;48(8):830–837.
    1. Landry JS, Chan T, Lands L, Menzies D. Long-term impact of bronchopulmonary dysplasia on pulmonary function. Can Respir J. 2011;18(5):265–270.
    1. Drysdale SB, Alcazar M, Wilson T, Smith M, Zuckerman M, Lauinger IL, et al. Respiratory outcome of prematurely born infants following human rhinovirus A and C infections. Eur J Pediatr. 2014;173(7):913–919.
    1. Drysdale SB, Lo J, Prendergast M, Alcazar M, Wilson T, Zuckerman M, et al. Lung function of preterm infants before and after viral infections. Eur J Pediatr. 2014;173(11):1497–1504.
    1. Bhattacharya S, Go D, Krenitsky DL, Huyck HL, Solleti SK, Lunger VA, et al. Genome-wide transcriptional profiling reveals connective tissue mast cell accumulation in bronchopulmonary dysplasia. Am J Respir Crit Care Med. 2012;186(4):349–358.
    1. O'Reilly M, Harding R, Sozo F. Altered small airways in aged mice following neonatal exposure to hyperoxic gas. Neonatology. 2014;105(1):39–45.
    1. Albertine KH. Progress in understanding the pathogenesis of BPD using the baboon and sheep models. Semin Perinatol. 2013;37(2):60–68.
    1. Collins JJ, Kunzmann S, Kuypers E, Kemp MW, Speer CP, Newnham JP, et al. Antenatal glucocorticoids counteract LPS changes in TGF-beta pathway and caveolin-1 in ovine fetal lung. Am J Physiol Lung Cell Mol Physiol. 2013;304(6):L438–444.
    1. Maniscalco WM, Watkins RH, Roper JM, Staversky R, O'Reilly MA. Hyperoxic ventilated premature baboons have increased p53, oxidant DNA damage and decreased VEGF expression. Pediatr Res. 2005;58(3):549–556.
    1. Backstrom E, Hogmalm A, Lappalainen U, Bry K. Developmental stage is a major determinant of lung injury in a murine model of bronchopulmonary dysplasia. Pediatr Res. 2011;69(4):312–318.
    1. Choo-Wing R, Syed MA, Harijith A, Bowen B, Pryhuber G, Janer C, et al. Hyperoxia and interferon-gamma-induced injury in developing lungs occur via cyclooxygenase-2 and the endoplasmic reticulum stress-dependent pathway. Am J Respir Cell Mol Biol. 2013;48(6):749–757.
    1. Madurga A, Mizikova I, Ruiz-Camp J, Morty RE. Recent advances in late lung development and the pathogenesis of bronchopulmonary dysplasia. Am J Physiol Lung Cell Mol Physiol. 2013;305(12):L893–905.
    1. Hilgendorff A, Reiss I, Ehrhardt H, Eickelberg O, Alvira CM. Chronic lung disease in the preterm infant. Lessons learned from animal models. Am J Respir Cell Mol Biol. 2014;50(2):233–245.
    1. O'Reilly MA, Marr SH, Yee M, McGrath-Morrow SA, Lawrence BP. Neonatal hyperoxia enhances the inflammatory response in adult mice infected with influenza A virus. Am J Respir Crit Care Med. 2008;177(10):1103–1110.
    1. Bose CL, Dammann CE, Laughon MM. Bronchopulmonary dysplasia and inflammatory biomarkers in the premature neonate. Arch Dis Child Fetal Neonatal Ed. 2008;93(6):F455–461.
    1. Ambalavanan N, Carlo WA, D'Angio CT, McDonald SA, Das A, Schendel D, et al. Cytokines associated with bronchopulmonary dysplasia or death in extremely low birth weight infants. Pediatrics. 2009;123(4):1132–1141.
    1. Schneibel KR, Fitzpatrick AM, Ping XD, Brown LA, Gauthier TW. Inflammatory mediator patterns in tracheal aspirate and their association with bronchopulmonary dysplasia in very low birth weight neonates. J Perinatol. 2013;33(5):383–387.
    1. Speer CP. Pulmonary inflammation and bronchopulmonary dysplasia. J Perinatol. 2006;26(Suppl 1):S57–62. discussion S63-54.
    1. Bhandari A, Bhandari V. Biomarkers in bronchopulmonary dysplasia. Paediatr Respir Rev. 2013;14(3):173–179.
    1. Bhandari A, Bhandari V. Pitfalls, problems, and progress in bronchopulmonary dysplasia. Pediatrics. 2009;123(6):1562–1573.
    1. Drysdale SB, Prendergast M, Alcazar M, Wilson T, Smith M, Zuckerman M, et al. Genetic predisposition of RSV infection-related respiratory morbidity in preterm infants. Eur J Pediatr. 2014;173(7):905–912.
    1. Hadchouel A, Franco-Montoya ML, Delacourt C. Altered lung development in bronchopulmonary dysplasia. Birth Defects Res A Clin Mol Teratol. 2014;100(3):158–167.
    1. Schmolzer GM, Kumar M, Pichler G, Aziz K, O'Reilly M, Cheung PY. Noninvasive versus invasive respiratory support in preterm infants at birth: systematic review and meta-analysis. BMJ. 2013;347:f5980.
    1. Bhandari V. The potential of non-invasive ventilation to decrease BPD. Semin Perinatol. 2013;37(2):108–114.
    1. Carroll JL, Agarwal A. Development of ventilatory control in infants. Paediatr Respir Rev. 2010;11(4):199–207.
    1. Bates ML, Pillers DA, Palta M, Farrell ET, Eldridge MW. Ventilatory control in infants, children, and adults with bronchopulmonary dysplasia. Respir Physiol Neurobiol. 2013;189(2):329–337.
    1. Kim DH, Kim HS, Choi CW, Kim EK, Kim BI, Choi JH. Risk factors for pulmonary artery hypertension in preterm infants with moderate or severe bronchopulmonary dysplasia. Neonatology. 2012;101(1):40–46.
    1. Rhein LM, Dobson NR, Darnall RA, Corwin MJ, Heeren TC, Poets CF, et al. Effects of caffeine on intermittent hypoxia in infants born prematurely: a randomized clinical trial. JAMA Pediatr. 2014;168(3):250–257.
    1. Heldt GP. Development of stability of the respiratory system in preterm infants. J Appl Physiol (1985) 1988;65(1):441–444.
    1. Davis PG, Thorpe K, Roberts R, Schmidt B, Doyle LW, Kirpalani H, et al. Evaluating “old” definitions for the “new” bronchopulmonary dysplasia. J Pediatr. 2002;140(5):555–560.
    1. Hjalmarson O, Brynjarsson H, Nilsson S, Sandberg KL. Persisting hypoxaemia is an insufficient measure of adverse lung function in very immature infants. Arch Dis Child Fetal Neonatal Ed. 2014;99:F257–262.
    1. Bhandari A, Panitch HB. Pulmonary outcomes in bronchopulmonary dysplasia. Semin Perinatol. 2006;30(4):219–226.
    1. Robin B, Kim YJ, Huth J, Klocksieben J, Torres M, Tepper RS, et al. Pulmonary function in bronchopulmonary dysplasia. Pediatr Pulmonol. 2004;37(3):236–242.
    1. Sanchez-Solis M, Garcia-Marcos L, Bosch-Gimenez V, Perez-Fernandez V, Pastor-Vivero MD, Mondejar-Lopez P. Lung function among infants born preterm, with or without bronchopulmonary dysplasia. Pediatr Pulmonol. 2012;47(7):674–681.
    1. Friedrich L, Pitrez PM, Stein RT, Goldani M, Tepper R, Jones MH. Growth rate of lung function in healthy preterm infants. Am J Respir Crit Care Med. 2007;176(12):1269–1273.
    1. Been JV, Lugtenberg MJ, Smets E, van Schayck CP, Kramer BW, Mommers M, et al. Preterm birth and childhood wheezing disorders: a systematic review and meta-analysis. PLoS Med. 2014;11(1):e1001596.
    1. Schuh S, Coates AL, Binnie R, Allin T, Goia C, Corey M, et al. Efficacy of oral dexamethasone in outpatients with acute bronchiolitis. J Pediatr. 2002;140(1):27–32.
    1. Hoo AF, Dezateux C, Henschen M, Costeloe K, Stocks J. Development of airway function in infancy after preterm delivery. J Pediatr. 2002;141(5):652–658.
    1. Friedrich L, Stein RT, Pitrez PM, Corso AL, Jones MH. Reduced lung function in healthy preterm infants in the first months of life. Am J Respir Crit Care Med. 2006;173(4):442–447.
    1. American Thoracic S, European Respiratory S. ATS/ERS statement: raised volume forced expirations in infants: guidelines for current practice. Am J Respir Crit Care Med. 2005;172(11):1463–1471.
    1. Broughton S, Sylvester KP, Fox G, Zuckerman M, Smith M, Milner AD, et al. Lung function in prematurely born infants after viral lower respiratory tract infections. Pediatr Infect Dis J. 2007;26(11):1019–1024.
    1. Davis SD, Rosenfeld M, Kerby GS, Brumback L, Kloster MH, Acton JD, et al. Multicenter evaluation of infant lung function tests as cystic fibrosis clinical trial endpoints. Am J Respir Crit Care Med. 2010;182(11):1387–1397.

Source: PubMed

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