The effects of aneurysm on the biaxial mechanical behavior of human abdominal aorta

https://doi.org/10.1016/j.jbiomech.2005.03.003Get rights and content

Abstract

The biomechanical response of normal and pathologic human abdominal aortic tissue to uniaxial loading conditions is insufficient for the characterization of its three-dimensional (3D) mechanical behavior. Planar biaxial mechanical evaluation allows for 3D constitutive modeling of nearly incompressible tissues, as well as the investigation of the nature of mechanical anisotropy. In the current study, 26 abdominal aortic aneurysm (AAA) tissue samples and 8 age-matched (>60 years of age) nonaneurysmal abdominal aortic (AA) tissue samples were obtained and tested using a tension-controlled biaxial testing protocol. Graphical response functions (Sun et al., 2003. J. Biomech. Eng. 125, 372–380) were used as a guide to describe the pseudo-elastic response of AA and AAA. Based on the observed pseudo-elastic response, a four-parameter exponential strain energy function developed by Vito (1990. J. Biomech. Eng. 112, 153–159) was used from which both an individual specimen and group material parameter sets were determined for both AA and AAA. Peak Green strain values in the circumferential (Eθθ,max) and longitudinal (ELL,max) directions under an equibiaxial tension of 120 N/m were also compared. The strain energy function fit all of the individual specimens well with an average R2 of 0.95±0.02 and 0.90±0.02 (mean±SEM) for the AA and AAA groups, respectively. The average Eθθ,max at 200 N/m equibiaxial tension was found to be significantly smaller for AAAs as compared to AAs (0.07±0.01 versus 0.13±0.03, respectively; p<0.01). There was also a pronounced increase in the circumferential stiffness for AAA tissue as compared to AA tissue, indicating a larger degree of anisotropy for this tissue as compared to age-matched AA tissue. We also observed that the four-parameter Fung-elastic model was not able to fit the AAA tissue mechanical response using physically realistic material parameter values. It was concluded that aneurysmal degeneration of the abdominal aorta is associated with an increase in mechanical anisotropy, with preferential stiffening in the circumferential direction.

Introduction

Abdominal aortic aneurysm (AAA) is a localized dilation of the infrarenal aorta, representing a significant disease in the western population. There are approximately 200,000 patients in the US and 500,000 patients worldwide diagnosed with AAA every year (Bosch et al., 2001), and rupture of AAA currently ranks as the 13th leading cause of death in the US. (Silverberg and Lubera, 1987) In the past 30 years, the diagnosis of AAA has tripled in the Western world, and this will likely increase in the coming years as the average age of the population is increasing. (Bosch et al., 2001)

The biomechanical response of human AAA, as well as nonaneurysmal abdominal aorta (AA), to uniaxial loading conditions has been previously reported by our laboratory and others (He and Roach, 1994; Raghavan et al., 1996; Raghavan and Vorp, 2000; Thubrikar et al., 2001). However, mechanical data derived from uniaxial tensile testing is insufficient for the characterization of the three-dimensional (3D) mechanical response. Yet, most 3D stress analysis models of AAA reported in the literature have been based on our previous uniaxial tensile testing data (Raghavan and Vorp, 2000; Raghavan et al., 2000; Fillinger et al., 2002; Wang et al., 2002; Fillinger et al., 2003; Venkatasubramaniam et al., 2004).

Clearly, 3D multi-axial mechanical evaluation would allow for more appropriate modeling of aneurysmal tissue, especially the nature and extent of mechanical anisotropy. Such data would also lead to a better understanding of this disease and its progression. Yet, to date there are no extant data on the biaxial mechanical response of AAA tissue. In the current investigation, biaxial tensile testing was performed on human AAA and AA tissue in order to characterize the biaxial mechanical response of both tissue types and to gain insight into differences between them.

Section snippets

Specimen preparation

All AA and AAA tissue specimens were retrieved according to University of Pittsburgh Institutional Review Board guidelines. AAA samples were obtained from open surgical aneurysm repair, primarily from the anterior portion of the aneurysm. Age-matched (>60 years of age) AA tissue samples were harvested from autopsy within 24 h of death. All samples were stored in 0.9% saline in a 4 °C refrigerator and tested within 48 h from harvest (Medynsky et al., 1998). Square specimens, approximately 2.0 cm×2.0 

Results

A total of 26 tissue specimens from the AAA (mean diameter 6.5±0.2) of 26 patients (mean age=72.3±1.8) and eight AA specimens from eight subjects (mean age=70.6±1.9, p=0.64 in comparison to AAA group) were tested and analyzed. The mean measured thickness values were 1.49±0.11 and 1.32±0.08 mm for the AA and AAA specimens, respectively (p=0.29). The mean variance in measured thickness values within each specimen were 0.014±0.01 and 0.019±0.01 mm for the AA and AAA, respectively.

General observations

The biaxial testing of aneurysmal and non-aneurysmal aortic tissue allows for the investigation of anisotropy as well as the derivation of a more appropriate constitutive model for this tissue. Our results suggest that aneurysmal degeneration of the human abdominal aorta is associated with a marked alteration in mechanical behavior. For example, AAA tissue is stiffer than AA (Fig. 1, Fig. 3, Fig. 4, Fig. 5) as well as exhibiting a decrease in its extensibility under the same stress state (Fig. 2

Acknowledgments

This work was supported by grants from the NIH (R01-HL-60670) to DAV as well as The Pittsburgh Foundation (♯M2000-0027) to DAV. The authors would like to acknowledge the assistance from the Engineered Tissue Mechanics Laboratory, Larry Nichols MD, Elena Di Martino PhD, Ajay Bohra MS, as well as Michel Makaroun, MD and the rest of the Division of Vascular Surgery at the University of Pittsburgh Medical Center. MSS is an Established Investigator of the AHA.

References (30)

  • D.H. Wang et al.

    Effect of intraluminal thrombus on wall stress in patient-specific models of abdominal aortic aneurysm

    Journal of Vascular Surgery

    (2002)
  • B.T. Baxter et al.

    Abdominal aortic aneurysms are associated with altered matrix proteins of the nonaneurysmal aortic segments

    Journal of Vascular Surgery

    (1994)
  • J.L. Bosch et al.

    Hospital costs for elective endovascular and surgical repairs of infrarenal abdominal aortic aneurysms

    Radiology

    (2001)
  • H.S. Choi et al.

    Two-dimensional stress–strain relationship for canine pericardium

    Journal of Biomechanical Engineering

    (1990)
  • C.J. Chuong et al.

    On residual stresses in arteries [erratum appears in Journal of Biomechanical Engineering 1990 August; 112(3): 249]

    Journal of Biomechanical Engineering

    (1986)
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