Dissection Propagation via Avalanches in Human Descending Thoracic Aorta: Effect of Aging

Understanding of the risk factors and underlying mechanisms of aortic dissection (AD) is critical for improved clinical management of the disease. How aging, a prominent risk factor for AD, impairs the dissection resistance capabilities of the aorta has not been elucidated. This study integrated mechanical testing, multiphoton imaging and finite element (FE) modeling to investigate the multiscale dissection behavior of human descending thoracic aortas (DTAs) from a wide range of ages. Mechanical testing demonstrated that aging diminishes bonding between the lamellar layers within the media of human DTA. Moreover, dissection propagation in aortic media is associated with dissection tension drops that follow a power-law distribution. Multiphoton imaging of dissected DTA media revealed less organized elastic lamellae and fewer visible collagen with aging. The discrete FE model of dissection propagation recapitulated the power-law behavior that originates from avalanches of interlamellar collagen fiber (ICF) failures. Simulation revealed prominent interlamellar structural rearrangement of ICFs in the aging DTA, including lower density and higher dispersion, of which the former strongly correlates with the weakened interlamellar bonding while the latter is vital in triggering the fast-propagating avalanches and power-law behavior of AD. Furthermore, small avalanches occur more often with aging, which makes dissection propagation faster and AD more dangerous for the elderly population. STATEMENT OF SIGNIFICANCE: Early diagnosis of aortic dissection (AD) is crucial for effective disease management, and it requires a comprehensive understanding of the risk factors. This study explores the microstructural mechanisms that underlie the age-augmented risk of AD through a multiscale investigation of the dissection mechanics of human descending thoracic aortas (DTAs). Our findings reveal the presence of avalanches and power-law behavior in dissection propagation, which is age-dependent and can be recapitulated using a novel computational model that accounts for the failure of discrete interlamellar fibers. Using this model, we demonstrated that aging weakens the dissection resistance of the DTA, characterized by a reduction in the number and increased dispersion of interlamellar collagen fibers. The avalanches and power-law behavior not only plays a fundamental role in the rapid progression of AD but also offers new perspectives on the interlamellar microstructure-function relationship in both aortic health and disease.