Abstract
The transition from fetal to postnatal life involves clearance of liquid from the lung and airways, and rapid formation of a functional residual capacity. Despite the importance of the diaphragm in this process, the impact of birth on the mechanical and functional activity of its muscle fibers is not known. This study determined the contractile characteristics of individual “skinned” diaphragm fibers from 70 days (0.47) gestation to after birth in sheep. Based on differential sensitivity to the divalent ions calcium (Ca2+) and strontium (Sr2+), all fibers in the fetal diaphragm were classified as “fast,” whereas fibers from the adult sheep diaphragm exhibited a “hybrid” phenotype where both “fast” and “slow” characteristics were present within each single fiber. Transition to the hybrid phenotype occurred at birth, was evident after only 40 min of spontaneous breathing, and could be induced by simple mechanical stretch of diaphragm fibers from near-term fetuses (∼147 days gestation). Both physical stretch of isolated fibers, and mechanical ventilation of the fetal diaphragm in situ, significantly increased sensitivity to Ca2+ and Sr2+, maximum force generating capacity, and decreased passive tension in near-term and preterm fetuses; however, only fibers from near-term fetuses showed a complete transition to a “hybrid” activation profile. These findings suggest that stretch associated with the transition from a liquid to air-filled lung at birth induces physical changes of proteins determining the activation and elastic properties of the diaphragm. These changes may allow the diaphragm to meet the increased mechanical demands of breathing immediately after birth.
Highlights
Before birth the lungs are filled with liquid and take no part in gas exchange, which occurs between the maternal and fetal circulations in the placenta
At 127 days gestational age (0.87 full-term) the force–pCa curve remained unchanged compared to data from the earlier fetal ages, but the force–pSr curve of diaphragm fibers presented with two distinct phases, each of which had significantly different slopes, and the entire data was best described by a double sigmoid function (F -test, P < 0.05; Figure 2)
In fibers obtained from the adult diaphragm the increased slope was related to the more pronounced sub-maximal plateau that appears in the force–pSr activation profile between birth and adulthood (Table 2)
Summary
Before birth the lungs are filled with liquid and take no part in gas exchange, which occurs between the maternal and fetal circulations in the placenta. The respiratory system undergoes important changes to ensure a successful transition of the lungs from a liquid-filled to an air-filled environment – this involves removal of liquid from the airways and alveoli, and the formation of a functional residual capacity (Bland et al, 1980; Olver et al, 2004; Siew et al, 2009) These processes provoke further changes necessary for the lungs to become efficient in gas exchange, including: increased pulmonary blood flow, a reduction in intrapleural pressure, lung recoil, and closure of the ductus arteriosus initiated, in part, by the increase in blood oxygenation (Rudolph, 1985; Hooper and Harding, 2005; Crossley et al, 2009). In baboons, Maxwell et al (1983) showed that the phenotype of respiratory muscle www.frontiersin.org
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