Mapping microarchitectural degeneration in the dilated ascending aorta with ex vivo diffusion tensor imaging

Abstract

Aims Thoracic aortic aneurysms (TAAs) carry a risk of catastrophic dissection. Current strategies to evaluate this risk entail measuring aortic diameter but do not image medial degeneration, the cause of TAAs. We sought to determine if the advanced magnetic resonance imaging (MRI) acquisition strategy, diffusion tensor imaging (DTI), could delineate medial degeneration in the ascending thoracic aorta. Methods and results Porcine ascending aortas were subjected to enzyme microinjection, which yielded local aortic medial degeneration. These lesions were detected by DTI, using a 9.4 T MRI scanner, based on tensor disorientation, disrupted diffusion tracts, and altered DTI metrics. High-resolution spatial analysis revealed that fractional anisotropy positively correlated, and mean and radial diffusivity inversely correlated, with smooth muscle cell (SMC) and elastin content (P < 0.001 for all). Ten operatively harvested human ascending aorta samples (mean subject age 61.6 ± 13.3 years, diameter range 29–64 mm) showed medial pathology that was more diffuse and more complex. Nonetheless, DTI metrics within an aorta spatially correlated with SMC, elastin, and, especially, glycosaminoglycan (GAG) content. Moreover, there were inter-individual differences in slice-averaged DTI metrics. Glycosaminoglycan accumulation and elastin degradation were captured by reduced fractional anisotropy (R2 = 0.47, P = 0.043; R2 = 0.76, P = 0.002), with GAG accumulation also captured by increased mean diffusivity (R2 = 0.46, P = 0.045) and increased radial diffusivity (R2 = 0.60, P = 0.015). Conclusion Ex vivo high-field DTI can detect ascending aorta medial degeneration and can differentiate TAAs in accordance with their histopathology, especially elastin and GAG changes. This non-destructive window into aortic medial microstructure raises prospects for probing the risks of TAAs beyond lumen dimensions.