Bronchopulmonary dysplasia

Bronchopulmonary dysplasia

SYMPOSIUM: NEONATOLOGY Bronchopulmonary dysplasia Definition Classic BPD Defining BPD is challenging and remains inconsistent. The original definitio...

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SYMPOSIUM: NEONATOLOGY

Bronchopulmonary dysplasia

Definition Classic BPD Defining BPD is challenging and remains inconsistent. The original definition has been altered numerous times to better match the changing presentation as management improved. By the end of the 1970s, neonatologists had proposed including infants who required ventilation in the first week of life, had signs of chronic respiratory disease for more than 28 days, required supplemental oxygen for more than 28 days and had consistent chest radiograph signs. However, with further advances in medical care, more preterm infants on oxygen at 28 days did not need it before discharge and so this became less useful in predicting medium to long term outcomes. By the end of the 1980s, the definition shifted again when neonatologists proposed redefining BPD as oxygen supplementation at 36 weeks postmenstrual age (PMA), which more accurately predicted poor pulmonary outcome at 2 years of age.

Assim Javaid Ian Morris

Abstract Bronchopulmonary dysplasia (BPD) is the most common sequelae of preterm birth. It has proven a difficult condition to define as improving early management of the premature infant has led to a changing clinical picture over time. However, despite the advances in neonatal care, rates of BPD are at best unchanged and may even have risen. As BPD has significant long-term consequences, particularly from respiratory, cardiovascular and neurodevelopmentary perspectives, effective early management is key to improving long term outcomes. In this review the various definitions of BPD, and their limitations, are discussed alongside the evidence behind effective management of preterm infants, including the long-term management needed after discharge from hospital.

New BPD The definition was reviewed again by the National Institute of Child Health and Human Development (NICHD) in 2000. The chest radiograph changes described above were seen far less frequently with improved management of the premature neonate, instead only showing haziness or decreased lung fluid, which had previously made them difficult to categorise as BPD according to existing definitions. There was also an increasing trend towards premature infants not needing oxygen at the time of assessment due to improved management with non-invasive respiratory support. This meant that even though these infants had a degree of chronic lung disease, they did not fulfil the criteria available to be classified as having BPD. This phenotype is often dubbed the “New” BPD. The NICHD proposed a severitybased definition shown in Table 1 below.

Keywords antenatal corticosteroids; bronchopulmonary dysplasia; chronic lung disease; home oxygen therapy; postnatal corticosteroids; ventilator-induced lung injury

Introduction BPD, also known as chronic lung disease (CLD), is the most common major long-term morbidity associated with prematurity. It presents an increased risk of mortality and neurodevelopmental and pulmonary sequelae. The term originated in the last part of the 1960s and was originally created to describe the clinical and radiological features of a group of premature infants who had developed respiratory distress syndrome (RDS) and had needed prolonged ventilation with high inspired concentrations of oxygen leading to chronic lung disease. These infants had a mean gestational age of 34 weeks, required oxygen at 28 days of life and had consistent radiological changes; cystic changes, scarring and areas of atelectasis and hyperinflation. This severe form of BPD, often dubbed “Classic BPD”, has become far less common with current management of premature infants with antenatal steroids, surfactant and gentler ventilation techniques. It is rare to see BPD in infants with a gestational age greater than 30 weeks or a weight greater than 1200g. However, despite these advances in care, the prevalence of BPD remains the same, if not higher, leaving a cohort of patients who may need complex management in the long-term.

Physiologic definition One of the long-standing difficulties with all the above definitions of BPD was the requirement of oxygen as a criterion. There is no current consensus on the optimal saturations to aim for, with literature suggesting anywhere from 88% to 98%. Hence, the FiO2 an infant may be receiving is a clinical decision and can vary hugely from centre to centre and clinician to clinician. This led some researchers to propose a physiologic definition, which was largely the same as the NICHD definition but also required all infants to undergo a stepwise oxygen test to attempt to wean them to room air. Those who were unsuccessful were labelled as having BPD. This proposal eliminated a degree of inter-clinician variability in the assessment of severity of BPD and reduced incidence. The limitations of multiple definitions Due to the multiple definitions being used in research, making comparisons between studies has proven difficult. The need for oxygen supplementation as a diagnostic criterion offers its own limitations, as many factors can affect its use. In addition to varying target oxygen saturations, the use of oxygen at the time of assessment may reflect an acute change, rather than be a sign of a chronic condition. Furthermore, the more prematurely an infant is born the longer it will need oxygen in order to meet the criterion at assessment at 36 weeks, so the total duration of

Assim Javaid MBChB MPharm is a Paediatric Specialty Trainee with the Neonatal intensive care unit, Department of Child Health, University Hospital Wales, Cardiff, UK. Conflict of interest: None declared. Ian Morris MBBS (Hons) MRCPCH is a Neonatal consultant with the Neonatal intensive care unit, Department of Child Health, University Hospital Wales, Cardiff, UK. Conflict of interest: None declared.

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NICHD definition of BPD

Table 1

oxygen therapy is not taken into account. Finally, oxygen use can also be effected by ventilatory support, concurrent medication use and altitude. Even with a single definition, the results can vary depending upon the prepositions placed within it. The NICHD criteria require the use of supplementary oxygen for 28 days but studies have found that this if often misinterpreted as at 28 days. This small change can change incidence of BPD in a unit by a large margin. There is also ambiguity on how to classify infants who are receiving humidified high-flow air, as this may impact on whether they need oxygen and, hence, which category of severity an infant will fall into.

Neonatal Research Network used three different definitions to assess the rates of BPD in extremely premature infants, i.e. those born between 22 and 28 weeks gestational age. They found that 68% were classified as having BPD by their own definition (27% mild, 23% moderate and 18% severe), compared to 42% when using the late 1980s definition for ‘classic BPD’ and 40% when using the physiologic definition. This closely mirrors other similar studies. Despite the improved management of infants born prematurely rates of BPD have remained constant or, as some studies have found, increased slightly. This increase is likely due to greater survival of extremely premature infants.

Incidence

Pathology

The incidence of BPD is inversely proportional to weight and gestational age, roughly doubling for every additional week of prematurity. It is uncommon among infants born after 32 weeks or weighing more than 1200g. However, establishing an actual incidence is notoriously difficult due to inconsistencies in definition. The NICHD

BPD is a complex and multifactorial condition, contributed to by both pre- and postnatal factors that influence normal lung development. Classic BPD was characterised by airway inflammation, emphysema and smooth muscle hypertrophy in the airways and pulmonary vasculature. A lack of endogenous surfactant made

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Placental transfusion: delayed cord clamping at birth does not reduce BPD rates in spite of short term benefits. Umbilical cord milking, however, does appear to reduce BPD and the implementation of one of these strategies to increase placental transfusion is advisable.

the lungs more difficult to ventilate, so greater pressures were used. This led to a heterogenic expansion of the lungs, with areas of both over-distension and atelectasis, resulting in a release of pro-inflammatory mediators into the local tissue. In “New” BPD, administration of surfactant and gentler ventilation strategies result in a different presentation, with potentially less mechanical trauma if excess pressure and volumes are avoided. However, with advancing technology, mechanical ventilation can now be started before alveolarization of the lungs, during the saccular or even canalicular stages, leading to early arrest of lung development. As such, infants tend to have fewer, larger alveoli and a reduced number of total arteries. On the other hand, these lungs do have less airway epithelial disease, less fibrosis and better vasculature than infants affected by classic BPD. Whilst BPD occurs almost exclusively in infants receiving positive pressure ventilation, other factors are known to contribute. Oxygen toxicity results from overproduction of oxygen metabolites causing cellular damage, further enhanced by the immature anti-oxidant mechanisms in the preterm infant. Additionally, post-natal infection, intra-uterine growth restriction, gender (increased incidence in males) and genetics (monozygotic twins are more likely to develop BPD than dizygotic twins) all appear to play a role. Chorioamnioinits induces early lung maturation, promotes surfactant production and reduces the risk of RDS. Conversely, several studies have reported an association with BPD.

Resuscitation: preterm lungs are particularly susceptible to barotrauma and volutrauma and just a few large volume ventilation breaths can cause inflammatory changes. Judicious use of positive pressure is vital and should be guided by close observation of the neonatal heart rate, chest wall movement and preductal saturations. The early use of positive end expiratory pressure (PEEP), in preference to mechanical ventilation where possible, may reduce BPD rates. Surfactant: like antenatal steroids, the use of surfactant has been pivotal in advancing perinatal medicine over the last few decades. It reduces respiratory morbidity, pulmonary air leak and death, but uncertainty remains over optimal dosing and timing of administration and which preparations and modes of administration are most suitable. Best evidence would suggest that early rescue after the onset of RDS, rather than prophylactic administration, is best for reducing BPD rates. Where given, natural preparations with an initial dose of 200mg/kg of porcine surfactant are recommended, with targeted repeat dosing for deteriorating infants showing a good initial response. Minimally invasive administration techniques may confer additional advantage over traditional intubation, with research ongoing in this area.

Prevention of BPD Initial management on the neonatal unit Respiratory Support: using nasal continuous positive airway pressure (CPAP) in preference to mechanical ventilation reduces rates of BPD. Smaller studies have found other non-invasive ventilatory methods to successfully reduce the need for intubation, such as non-invasive positive pressure ventilation (NIPPV) or bilevel positive airway pressure (BiPAP). In cases where noninvasive techniques are used, a low threshold should be in place to allow neonates who haven’t received surfactant early to receive it. An FiO2 threshold of 45% has been shown to reduce the time to surfactant without increasing intubation rates. If mechanical ventilation proves necessary, strategies aiming at volume-targeted ventilation should be employed over pressure targeted modes where possible. Whilst “permissive hypercapnia” is adopted in a number of units it does not seem to reduce rates of BPD.

Most infants developing BPD are born prematurely and there is often prior warning of impending delivery. The potential exists for obstetric, midwifery and neonatal teams to initiate strategies to prevent BPD or minimize its severity. Antenatal No single management strategy has consistently been shown to delay preterm birth but the provision of quality antenatal care and promotion of healthy maternal lifestyle are important. Teenage pregnancy, social deprivation, poor nutrition and poor antenatal attendance are all associated with premature delivery and adverse neonatal outcome. Behavioural influences such as alcohol, smoking and recreational drug use are further risk factors. Corticosteroids: corticosteroids aid in the maturation of the premature lung and have significant short term benefits when administered to women at risk of delivery from 23 to 34 weeks. They do not, however, reduce BPD in this group, with significant reductions seen only in late preterm births (more than 34 weeks).

Saturation Targets: no particular oxygen saturation target has been shown to reduce BPD incidence. However, lower target ranges (85e89%) have been found to increase mortality and rates of necrotising enterocolitis and current consensus would support a target peripheral oxygen saturation range of 91e95%.

Magnesium Sulphate: magnesium sulphate should be infused in women in established preterm labour as it offers neuroprotection between 24 and 30 weeks. There is no clear evidence that it reduces BPD.

Caffeine: caffeine has been found to cause a significant reduction in the rates of BPD and, at follow-up, was shown to be associated with improved rates of survival without neurodisability at 18e22 months. The exact mechanism by which caffeine exerts its protective affect is unknown.

Delivery room management There is evidence to suggest that delivery in a unit with on-site tertiary neonatal facilities can improve overall outcomes in premature infants. Early management can have a significant impact on mortality and long-term morbidity.

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Vitamin A: vitamin A plays a role in maintaining the integrity of the respiratory tract epithelium and is a key regulator in lung

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society. After spending many months on a neonatal unit, affected infants face increased rates of hospitalisation in their early years, with some problems persisting well in to adult life.

growth. Intramuscular injection of Vitamin A has been found to show a modest reduction in rates of BPD. However, this route is associated with significant discomfort and an increased risk of infection.

Pulmonary: infants with mild or moderate BPD that were discharged home with oxygen therapy are usually weaned off this by two years of age, probably due to ongoing alveolar growth, resulting in improved gas exchange. However, half of infants with BPD will require hospitalisation within their first year, with over 50% of these readmissions being for respiratory reasons alone. The readmission rate is highest for those who have had a Respiratory Syncytial Virus (RSV) infection and/or oxygen therapy at home. It is common for preterm infants with BPD to have persistent respiratory symptoms, closely resembling those of asthmatic patients. The infants usually present with coughing and wheeze but, unlike infants with asthma, have a poorer response to inhaled corticosteroids. Current literature suggests that the mechanism of injury leads to a different inflammatory process in survivors of BPD from infants with asthma, with the underlying airflow limitation being caused by structural airway changes rather than eosinophilic airway inflammation. Though lung function has been found to improve with age, studies of teenagers and young adults who had survived BPD have shown impaired pulmonary function. Research has found a decreased forced expiratory volume in 1 s (FEV1) and a decreased forced vital capacity (FVC) when compared to peers who had no history of BPD. This has been attributed to dysanaptic pulmonary growth, in which lung parenchyma grows at a faster rate than the airways leading to fixed small airway obstruction. High-resolution CT images of young adults with a history of BPD has confirmed this. It is hence unsurprising to find that survivors of BPD also have reduced exercise tolerance, with significant risk of exercise-induced bronchoconstriction and evidence of poor gas exchange during physical activity. Survivors of BPD are also at increased risk of pulmonary arterial hypertension (PAH) due to their dysmorphic pulmonary vasculature leading to an increase in pulmonary pressures. Infants with BPD and PAH have been found to be at risk of early mortality.

Nutrition and Fluids: good nutrition is important for normal lung development. Insufficient protein intake increases the susceptibility of the preterm infant to lung injury from oxygen free radicals. High fluid intake is associated with an increased risk of developing BPD. Restricting fluid intake showed a trend towards reduced risk of developing BPD but this is not statistically significant. Corticosteroids: the use of post natal corticosteroids is controversial, with early studies suggesting reduced BPD incidence but at the expensive of short term morbidity, in the form of intraventricular haemorrhage and gut haemorrhage and perforation, and long term adverse neurodevelopment outcomes. The use of early (within week 1) or late (after week 1 of life) of dexamethasone reduces BPD. Routine early use is not recommended due to the associated morbidity but targeted use of late dexamethasone, most often with the low-dose DART regimen, is commonly employed to facilitate extubation. Hydrocortisone has generally been less frequently used, with little evidence of benefit or harm. The recent PREMILOC trial of early low dose systemic hydrocortisone suggests an increase in survival without BPD, with no significant difference to controls at two-year neuro-developmental follow-up and may influence future practice. Early inhaled corticosteroids may also be effective in improving disease free survival but there is currently insufficient evidence to support their routine use. Macrolide Antibiotics: Ureaplasma urealyticum colonisation of the respiratory tract in preterm infants has been found to associated with an increased incidence of BPD. Treatment with erythromycin has shown to be of no benefit in reducing the rates of BPD but there is a modest reduction in the combined risk of death and BPD. Studies are underway to determine the effect, if any, of early use of azithromycin.

Cardiovascular: cardiovascular complications of BPD include hypertension and univentricular or biventricular hypertrophy, with up to 50% of school-aged survivors being found to have right ventricular hypertrophy. However, further studies have found that by adolescence rates of hypertension and hypertrophy had significantly decreased. It is also worth noting that infants with a history of BPD are at increased risk of sudden unexplained death in infancy (SUDI).

Managing established BPD Nutrition: infants with BPD have a 20e40% higher energy demand than those without BPD. A high-calorie intake of 130e 150cals/kg/day is needed to meet these requirements, and the use of breast milk fortifiers and/or higher energy formula feeds are often considered. Ensuring adequate nutrition helps lung maturation and has been shown to decrease the duration of oxygen use and improve neurodevelopmental outcome.

Growth Failure: the high energy demand of BPD persists into infancy and failure to thrive is often seen at follow up. However, this poor growth may also be related to other factors such as birth weight and gestational age.

Diuretics: diuretic therapy can improve short term lung function by reducing interstitial oedema to aid lung compliance and pulmonary mechanics but there is little evidence that they reduce BPD or that longer term use provides any additional benefits.

Neurodevelopmental: preterm infants with a history of BPD are more likely to have neurological difficulties. BPD was found to be a significant risk factor in the development of cerebral palsy and other movement disorders affecting the limbs, neck, trunk and

Long-term outcomes The impact of BPD is multi-faceted, with medical, social, financial and emotional implications for infants, their families and

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Home Oxygen Therapy (adapted from BTS guidelines) Discharge Criteria

Follow-up at Home

Withdrawal Criteria

Infant’s Health C Oxygen requirements should be stable with a mean oxygen saturation of >93% C Oxygen saturations should not fall below 90% for more than 5% of the recording period C No other clinical conditions precluding discharge C Medically Stable C Satisfactory weight gain C Up to date with immunisations C Influenza immunisation arranged as appropriate C Palivizumab to be considered Parents C Willing and capable of managing an infant on home oxygen C Advised about smoking cessation C Advised about travel with oxygen cylinders C Must inform their home and car insurers C Provide home in a satisfactory condition Healthcare Professionals C Appropriate support (e.g. community paediatrician, social worker, nurse specialist) must be in place C Communication with the GP should have taken place C Parents provided with a list of phone numbers for advice and emergency help C Parents provided with open access to the local paediatric unit C All infants should be followed up by a community nurse or nurse specialist within 24 h of discharge C Their oxygen saturations should be checked within one week of discharge, then 3e4 weekly there after C A hospital follow-up appointment should be arranged for within 4e6 weeks of discharge Decision to Withdraw C Withdrawal can usually be managed at home C Consider withdrawal once oxygen requirement is down to 0.1 l/min C Oxygen saturations should be stable with a mean oxygen saturation of >93% once oxygen is withdrawn Once Withdrawn C Oxygen equipment should be left in the home for at least three months after the child has stopped using it C The child should have two normal oximetry recordings one month apart Re-assessment C If oxygen requirements persist beyond a year, specialist referral is needed to rule out concomitant conditions

Table 2

oral-buccal-lingual movements. BPD has also been associated with poorer fine and gross motor skills, cognitive delay, attentional impairment, behavioural problems, speech and language disorders, memory difficulties, visual-spatial perceptual defects and poorer academic performance.

characterised by expectations of death, critical illness and low expectations for the future. As such, parents need to be supported in the process of caring for their child from an emotional and psychological perspective as much as from a practical one. Home Oxygen: the British Thoracic Society (BTS) recommends the use of long-term oxygen therapy (LTOT) in BPD. Supplementary oxygen can reduce or prevent PAH, reduce intermittent desaturations, reduce airway resistance and promote growth. It is also likely to be beneficial for neurodevelopment and may reduce the risk of SUDI. LTOT actually reduces health service costs, as care at home is significantly less expensive than care on a neonatal unit. More pragmatically, home oxygen is preferable to a prolonged hospital stay both in terms of quality of life and the psychological impact on the infant and family. It allows parents and their family to lead more ordinary lives and promotes social inclusion, thereby meeting the family-centred service that is recommended by the National Service Framework for Children. Table 2 summarises some of the key BTS recommendations when considering home oxygen.

Long-term management Affected infants have multiple, complex needs that often persist well into adult life. Multidisciplinary discharge planning is needed to cater for both difficulties at the time of discharge and to guide families towards avenues of support for future problems. Discharge planning should closely involve parents and they should have the opportunity to meet the members of the team involved in the care of their child to help establish a long-term rapport. The parents will also need to be trained to recognise signs and symptoms of worsening health of their infant. Regular multidisciplinary follow-up in Neonatal Clinic during the first few years of life helps establish progress and ongoing needs. The impact on parents is significant. A recent qualitative study into the experiences of parents whose children had BPD found that the first few years of their lives was often

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Nutrition: failure to thrive is seen frequently in infants with a history of BPD due to the high energy demand placed on them either by BPD, their prematurity, their low birth weight, or a combination of the three. As mentioned before, good quality, high-calorie nutrition is needed for infants with BPD to achieve similar growth velocities as those without BPD. Constipation is frequently seen in preterm infants on high-calorie feeds and should be treated according to local guidelines.

Bancalari E, Claure N. Definitions and diagnostic criteria for bronchopulmonary dysplasia. Semin Perinatol 2006; 30: 164e70. Bray L, Shaw NJ, Snodin J. Living and managing with the long-term implications of neonatal chronic lung disease: the experiences and perspectives of children and their parents. Heart Lung 2015; 44: 512e6. Davidson LM, Berkelhamer SK. Bronchopulmonary dysplasia: chronic lung disease of infancy and long-term pulmonary outcomes. J Clin Med 2017; 6: 4. Doyle LW, Anderson PJ. Long-term outcomes of bronchopulmonary dysplasia. Semin Fetal Neonatal Med 2009; 14: 391e5. Eber E, Zach MS. Long term sequelae of bronchopulmonary dysplasia (chronic lung disease of infancy). Thorax 2001; 56: 317e23. Hines D, Modi N, Lee SK, et al. Scoping review shows wide variation in the definitions of bronchopulmonary dysplasia in preterm infants and calls for a consensus. Acta Paediatr 2017; 106: 366e74. Jobe AH, Bancalari E. Bronchopulmonary dysplasia. Am J Respir Crit Care Med 2001; 163: 1723e9. O’Reilly M, Sozo F, Harding R. Impact of preterm birth and bronchopulmonary dysplasia on the developing lung: long-term consequences for respiratory health. Clin Exp Pharmacol Physiol 2013; 40: 765e73. Poon CY, Edwards MO, Kotecha S. Long term cardiovascular consequences of chronic lung disease of prematurity. Paediatr Respir Rev 2013; 14: 242e9. 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: 451e6.

Gastroesophageal reflux: infants with BPD frequently develop gastroesophageal reflux, which usually presents as vomiting, worsening of BPD, wheeze, feed aversion of failure to thrive. It can usually be treated conservatively or with feed thickeners. RSV Prophylaxis: infants with BPD have been found to be more susceptible to lower respiratory infections. In the first year of life respiratory exacerbations are largely caused by viruses. The most common virus to lead to hospitalisation in this group is RSV and Palivizumab, a monoclonal antibody, has been shown to reduce the rate of hospitalisation from this. Infants with BPD due for discharge from October to March should be considered for administration of Palivizumab.

Conclusion BPD in its current form is due to alveolar developmental arrest leading to fewer and larger alveoli, causing less effective gas exchange. The “Classic” form of BPD, caused by mechanical trauma, is seen rarely in modern practice. The management of BPD begins during antenatal care by, where possible, preventing premature birth through advice on alcohol, recreational drug use and smoking, and promoting a healthy lifestyle. Where premature delivery is inevitable, antenatal administration of corticosteroids have proven the single most effective intervention in promoting lung maturation and reducing rates of BPD. Peri- and postnatal management, through surfactant administration and gentle ventilation strategies, can have a significant impact on the long-term outcomes for premature infants. Where BPD has developed long-term management is complex and needs to be tailored to the individual. In terms of further research in the field, consensus is needed on the definitions to be used to make studies more directly comparable and improve our understanding of the constantly evolving nature of this condition. A

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FURTHER READING Bhandari A, McGrath-Marrow S. Long-term pulmonary outcomes of patients with bronchopulmonary dysplasia. Semin Perinatol 2013; 37: 132e7. British Thoracic Society. Guidelines for home oxygen in children. Thorax 2009; 64(suppl II): ii1e26.

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BPD is a complex, multifactorial condition influenced by antenatal and postnatal factors Multiple definitions make comparing practice and incidence difficult, but incidence is inversely related to gestational age and birth weight Preventing preterm birth, improving antenatal care, and optimising delivery room management are important strategies in preventing BPD BPD occurs almost exclusively in mechanically ventilated infants, and strategies aimed at eliminating or limiting intubation are likely to help reduce rates The long term pulmonary and neurodevelopmental sequelae of BPD are significant and multi-disciplinary care is often required Home oxygen therapy is likely to play an increasing role and local and national guidance should be followed when implementing it

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Please cite this article in press as: Javaid A, Morris I, Bronchopulmonary dysplasia, Paediatrics and Child Health (2017), https://doi.org/10.1016/ j.paed.2017.10.004