Unravelling the complexities of the first breaths of life

Abstract

ABSTRACTBackgroundThe transition to air-breathing at birth is a seminal, but poorly understood, respiratory event common to all humans. The objectives of this prospective, observational study were to describe the spatiotemporal gas flow, aeration and ventilation patterns occurring within the lung in neonates during successful respiratory transition.MethodsElectrical impedance tomography was used to image intrathoracic volume patterns for every breath until six minutes from birth in term infants not needing resuscitation. Breaths were classified by video data, and measures of lung aeration, tidal flow conditions and intrathoracic volume distribution calculated for each inflation.Findings1401 breaths (n=17 neonates) met eligibility and data analysis criteria. Stable functional residual capacity was obtained by median (IQR) 43 (21, 77) breaths. Breathing patterns changed from predominantly crying (80.9% first minute) to tidal breathing (65.3% sixth minute). Tidal ventilation was inhomogeneous at birth, favouring the right and non-dependent lung; p<0.001 versus left and dependent lung (mixed effects model). Initial crying created a unique pattern with delayed mid-expiratory gas flow associated with intrathoracic volume redistribution (pendelluft flow) within the lung. This preserved functional residual capacity (70.8% cries), especially within the dorsal and right lung.InterpretationThe commencement of air-breathing at birth generates unique flow and volume states associated with marked spatiotemporal ventilation inhomogeneity not seen elsewhere in respiratory physiology. At birth neonates innately brake expiratory flow to defend functional residual capacity gains and redistribute gas to less aerated regions.FundingNational Health and Medical Research Council (Australia).Research in contextEvidence before this studyBirth requires the rapid transition from a fluid-filled to aerated lung. Despite being a seminal event for all humans, very little is understood about the physiological processes supporting the transition to air-breathing. Radiological and interventional studies from more than 40 years ago suggest that respiratory success at birth requires high intrathoracic pressure and flow states. Imaging studies in animals indicate that braking expiratory flow aids generating functional residual capacity.Added value of this studyIn term neonates during successful respiratory transition, breath-by-breath imaging of the intrathoracic gas flow and volume patterns within the lungs was possible with electrical impedance tomography. We found that aeration and ventilation were not uniform, with highly inhomogeneous, spatiotemporal volume patterns during attainment of functional residual capacity. Crying at birth created a unique expiratory pattern that allowed intrathoracic volume redistribution (pendelluft flow) within the lung, and preserved functional residual capacity. We hypothesise that newborns defend aeration from intrathoracic lung-fluid shifts by innately braking flow using the glottis and diaphragm.Implications of all the available evidenceReal-time imaging of intrathoracic volume patterns in humans is practical and may offer measures that identify neonates needing resuscitation. Whilst inspiration generated aeration, expiration is equally important to the respiratory transition. Expiratory braking is essential as a mechanism of defending aeration; suggesting that positive end-expiratory pressure is likely to be the most important method of supporting the failing human lung at birth.