Abstract

Arterial mechanics plays an important role in vascular pathophysiology and repair, and advanced imaging can inform constitutive models of vascular behavior. We have measured the mechanical properties of 14 human superficial femoral arteries (SFAs) (age 12–70, mean 48±19 years) using planar biaxial extension, and determined the preferred collagen fiber direction and dispersion using multiphoton microscopy. The collagen fiber direction and dispersion were evaluated using second-harmonic generation imaging and modeled using bivariate von Mises distributions. The microstructures of elastin and collagen were assessed using two-photon fluorescence imaging and conventional bidirectional histology. The mechanical and structural data were used to describe the SFA mechanical behavior using two- and four-fiber family invariant-based constitutive models. Older SFAs were stiffer and mechanically more nonlinear than younger specimens. In the adventitia, collagen fibers were undulated and diagonally-oriented, while in the media, they were straight and circumferentially-oriented. The media was rich in collagen that surrounded the circumferentially-oriented smooth muscle cells, and the elastin was present primarily in the internal and external elastic laminae. Older SFAs had a more circumferential collagen fiber alignment, a decreased circumferential-radial fiber dispersion, but the same circumferential-longitudinal fiber dispersion as younger specimens. Both the two- and the four-fiber family constitutive models were able to capture the experimental data, and the fits were better for the four-fiber family formulation. Our data provide additional details on the SFA intramural structure and inform structurally-based constitutive models.

Highlights

  • Arterial mechanics plays an important role in vascular physiology and pathophysiology, and it profoundly influences the design of devices and materials for open and endovascular repair [1,2,3,4]

  • The two-fiber family model—We model the planar biaxial stress-stretch behavior of superficial femoral arteries (SFA) using a strain-energy function that sums the contributions of the ground substance Ψg, and the two families of collagen fibers Ψfi, with the assumption that the mechanical properties of the two families are the same [36]

  • The ultimate goal of arterial mechanical testing is the determination of constitutive model parameters that allow to simulate arteries in silico and assess a variety of mechanical characteristics that cannot be measured in vivo

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Summary

Introduction

Arterial mechanics plays an important role in vascular physiology and pathophysiology, and it profoundly influences the design of devices and materials for open and endovascular repair [1,2,3,4]. Extension-inflation and planar biaxial extension tests are frequently used to characterize the multiaxial stress-stretch responses of arteries [5,6,7,8,9,10,11,12] and to obtain sufficient data for mathematical modeling of their mechanical behavior [13,14,15,16,17,18]. Structural models [18,19,20,21,22,23,24,25,26,27,28] describe the behavior of tissue by modeling individual responses of its constituents and their interactions They are instrumental for exploring various mechanobiological mechanisms but require detailed information on the organization, properties, loading conditions, and contact characteristics of each constituent at each deformation state, which, for many cases, is difficult, if not impossible, to measure directly. With the advances in imaging techniques, this new type of models has become increasingly popular as the investigators were able to explicitly include preferred fiber orientation, dispersion, or active cellular responses into their constitutive formulations [14,37,40,41,42,43,44,45]

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