Glycosaminoglycans modulate compressive stiffness and circumferential residual stress in the porcine thoracic aorta

Abstract

The mechanical properties of the aorta are influenced by the extracellular matrix, a network mainly comprised of fibers and glycosaminoglycans (GAG). In this work, we demonstrate that GAG contribute to the opening angle (a marker of circumferential residual stresses) in intact and glycated aortic tissue. Enzymatic GAG depletion was associated with a decrease in the opening angle, by approximately 25% (p = 0.009) in the ascending (AS) region, 32% (p = 0.003) in the aortic arch (AR), and 42% (p = 0.001) in the lower descending thoracic (LDT) region. A similar effect of GAG depletion on aortic ring opening angle was also observed in previously glycated tissues. Using indentation testing, we found that the radial compressive stiffness significantly increased in the AS region following GAG depletion, compared to fresh (p = 0.006) and control samples (p = 0.021), and that the compressive properties are heterogeneous along the aortic tree. A small loss of water content was also detected after GAG depletion, which was most prominent under hypotonic conditions. Finally, the AS region was also associated with a significant loss of compressive deformation (circumferential stretch that is < 1) in the inner layer of the aorta following GAG depletion, suggesting that GAG interact with ECM fibers in their effect on aortic mechanics. The importance of this work lies in its identification of the role of GAG in modulating the mechanical properties of the aorta, namely the circumferential residual stresses and the radial compressive stiffness, as well as contributing to the swelling state and the level of circumferential prestretch in the tissue. Statement of significanceThe mechanical properties of the aorta are influenced by the composition and organization of its extracellular matrix (ECM) and are highly relevant to medical conditions affecting the structural integrity of the aorta. The extent of contribution of glycosaminoglycans (GAG), a relatively minor ECM component, to the mechanical properties of the aorta, remains poorly characterized. This works shows that GAG contribute on average 30% to the opening angle (an indicator of circumferential residual stresses) of porcine aortas, and that GAG-depletion is associated with an increased radial compressive stiffness of the aorta. GAG-depletion was also associated with a loss of water content and compressive deformation in the inner layers of the aortic wall providing insight into potential mechanisms for their biomechanical role.