Insights Into Regional Adaptations in the Growing Pulmonary Artery Using a Meso-Scale Structural Model: Effects of Ascending Aorta Impingement

Abstract

As the next step in our investigations into the structural adaptations of the main pulmonary artery (PA) during postnatal growth, we utilized the extensive experimental measurements of the growing ovine PA from our previous study (Fata et al., 2013, “Estimated in vivo Postnatal Surface Growth Patterns of the Ovine Main Pulmonary Artery and Ascending Aorta,” J. Biomech. Eng., 135(7), pp. 71010–71012). to develop a structural constitutive model for the PA wall tissue. Novel to the present approach was the treatment of the elastin network as a distributed fiber network rather than a continuum phase. We then utilized this model to delineate structure-function differences in the PA wall at the juvenile and adult stages. Overall, the predicted elastin moduli exhibited minor differences remained largely unchanged with age and region (in the range of 150 to 200 kPa). Similarly, the predicted collagen moduli ranged from ∼1,600 to 2700 kPa in the four regions studied in the juvenile state. Interestingly, we found for the medial region that the elastin and collagen fiber splay underwent opposite changes (collagen standard deviation juvenile = 17 deg to adult = 28 deg, elastin standard deviation juvenile = 35 deg to adult = 27 deg), along with a trend towards more rapid collagen fiber strain recruitment with age, along with a drop in collagen fiber moduli, which went from 2700 kPa for the juvenile stage to 746 kPa in the adult. These changes were likely due to the previously observed impingement of the relatively stiff ascending aorta on the growing PA medial region. Intuitively, the effects of the local impingement would be to lower the local wall stress, consistent with the observed parallel decrease in collagen modulus. These results suggest that during the postnatal somatic growth period local stresses can substantially modulate regional tissue microstructure and mechanical behaviors in the PA. We further underscore that our previous studies indicated an increase in effective PA wall stress with postnatal maturation. When taken together with the fact that the observed changes in mechanical behavior and structure in the growing PA wall were modest in the other three regions studied, our collective results suggest that the majority of the growing PA wall is subjected to increasing stress levels with age without undergoing major structural adaptations. This observation is contrary to the accepted theory of maintenance of homeostatic stress levels in the regulation of vascular function, and suggests alternative mechanisms might regulate postnatal somatic growth. Understanding the underlying mechanisms will help to improve our understanding of congenital defects of the PA and lay the basis for functional duplication in their repair and replacement.