Structural and Functional Development of the Respiratory System in a Newborn Marsupial with Cutaneous Gas Exchange

Abstract

Marsupials are born with structurally immature lungs and rely, to varying degrees, on cutaneous gas exchange. With a gestation of 13 d and a birth weight of 13 mg, the fat-tailed dunnart (Sminthopsis crassicaudata) is one of the smallest and most immature marsupial newborns. We determined that the skin is almost solely responsible for gas exchange in the early neonatal period. Indeed, fewer than 35% of newborn dunnarts were observed to make any respiratory effort on the day of birth, with pulmonary ventilation alone not meeting the demand for oxygen until approximately 35 d postpartum. Despite the lack of pulmonary ventilation, the phrenic nerve had made contact with the diaphragm, and the respiratory epithelium was sufficiently developed to support gas exchange on the day of birth. Both type I and type II (surfactant-producing) alveolar epithelial cells were present, with fewer than 7% of the cells resembling undifferentiated alveolar epithelial precursor cells. The type I epithelial cells did, however, display thickened cytoplasmic extensions, leading to a high diffusion distance for oxygen. In addition, the architecture of the lung was immature, resembling the early canalicular stage, with alveolarization not commencing until 45 d postpartum. The pulmonary vasculature was also immature, with a centrally positioned single-capillary layer not evident until 100 d postbirth. These structural limitations may impede efficient pulmonary gas exchange, forcing the neonatal fat-tailed dunnart to rely predominately on its skin, a phenomenon supported by a low metabolic rate and small size.

The ventilatory response to hypoxia and hypercapnia is absent in the neonatal fat-tailed dunnart

“…Ventilatory and metabolic responses to inspired gases (air, hypercapnia, hypoxia) were measured in fat-tailed dunnart, Sminthopsis crassicaudata (Gould 1844), pouch young in different individuals at P0 (the day of birth) (N12, 6, 4), P5 (N7, 4, 4), P12 (N9, 6, 5) and P23 (N9, 4, 5) using a closed respirometry system as previously described (Frappell et al, 1989;Simpson et al, 2011). Briefly, an animal was masked and placed into a waterjacketed chamber maintained at a constant temperature of 36°C (pouch temperature) and 100% relative humidity, the chamber effectively separating the head and body.…”

“…When analysing V E , at least 50 consecutive breaths were analysed for tidal volume (V T ), inspiratory time (T I ), expiratory time (T E ), post-inspiratory pause (T P ; note that T P is fractional to T E because it represents the passivestatic component of T E , achieved with closed glottis), total breath time (T TOT T I +T E ), respiratory frequency (f60/T TOT ), mean inspiratory flow (V T /T I ), duty cycle (T I /T TOT ) and minute ventilation (V E V T xf). V E in P0 animals displayed marked instability with prolonged apnoea (Simpson et al, 2011); therefore, all recorded breaths were analysed in these animals. Animals in which V E was not discernible were not included in the analysis.…”

“…Where a ventilatory pattern was detected, breathing was generally accompanied by extended periods of apnoea, such that breathing may not have been observed again for the remainder of the measurement period. By P5, the continuously expressed breathing pattern was characterised by a post-inspiratory pause, together with frequent augmented breaths, or sighs [see Simpson et al (Simpson et al, 2011) for representative breathing traces]. There were some periods of instability, as indicated by the coefficients of variation for T TOT and V T being 11% and 45% respectively.…”

“…However, in some marsupials, such as the newborn fat-tailed dunnart (body mass 13mg), the skin is almost solely responsible for gas exchange, with discernible respiratory efforts generally absent on the day of birth (Mortola et al, 1999;Simpson et al, 2011). A central rhythm generator and sufficiently mature respiratory motoneurones and muscles are essential for coordinated ventilation to occur at birth (Feldman et al, 2003).…”

“…In the fattailed dunnart, phrenic motoneurons have made contact with the diaphragm at birth, yet continuous breathing does not occur until P3 (Frappell and MacFarlane, 2006;Simpson et al, 2011). If the central pattern generator(s) of the fat-tailed dunnart fires rhythmically, as in the opossum, then there may be an insufficient inspiratory drive, preventing the emergence of normal breathing.…”