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Research Papers

Insights Into Regional Adaptations in the Growing Pulmonary Artery Using a Meso-Scale Structural Model: Effects of Ascending Aorta Impingement

[+] Author and Article Information
Bahar Fata

Department of Bioengineering,
University of Pittsburgh,
Pittsburgh, PA 19104;
Center for Cardiovascular Simulation,
Institute for Computational
Engineering and Science,
Department of Biomedical Engineering,
University of Texas,
Austin, TX 78712

Will Zhang

Center for Cardiovascular Simulation,
Institute for Computational
Engineering and Science,
Department of Biomedical Engineering,
University of Texas,
Austin, TX 78712

Rouzbeh Amini

Department of Biomedical Engineering,
Auburn Science and Engineering Center 275,
West Tower,
The University of Akron,
Akron, OH 44325

Michael S. Sacks

Professor
W. A. “Tex” Moncrief, Jr. Simulation-Based
Engineering Science Chair I,
Center for Cardiovascular Simulation,
Institute for Computational
Engineering and Science,
Department of Biomedical Engineering,
University of Texas,
Austin, TX 78712
e-mail: msacks@ices.utexas.edu

1Present address: Institute for Computational Engineering and Sciences (ICES), The University of Texas at Austin, 201 East 24th Street, ACES 5.438, 1 University Station, C0200, Austin TX 78712-0027.

2Corresponding author.

Contributed by the Bioengineering Division of ASME for publication in the Journal of Biomechanical Engineering. Manuscript received October 21, 2013; final manuscript received January 7, 2014; accepted manuscript posted January 10, 2014; published online February 5, 2014. Editor: Beth Winkelstein.

J Biomech Eng 136(2), 021009 (Feb 05, 2014) (13 pages) Paper No: BIO-13-1498; doi: 10.1115/1.4026457 History: Received October 21, 2013; Revised January 07, 2014; Accepted January 10, 2014

As the next step in our investigations into the structural adaptations of the main pulmonary artery (PA) during postnatal growth, we utilized the extensive experimental measurements of the growing ovine PA from our previous study (Fata et al., 2013, “Estimated in vivo Postnatal Surface Growth Patterns of the Ovine Main Pulmonary Artery and Ascending Aorta,” J. Biomech. Eng., 135(7), pp. 71010–71012). to develop a structural constitutive model for the PA wall tissue. Novel to the present approach was the treatment of the elastin network as a distributed fiber network rather than a continuum phase. We then utilized this model to delineate structure-function differences in the PA wall at the juvenile and adult stages. Overall, the predicted elastin moduli exhibited minor differences remained largely unchanged with age and region (in the range of 150 to 200 kPa). Similarly, the predicted collagen moduli ranged from ∼1,600 to 2700 kPa in the four regions studied in the juvenile state. Interestingly, we found for the medial region that the elastin and collagen fiber splay underwent opposite changes (collagen standard deviation juvenile = 17 deg to adult = 28 deg, elastin standard deviation juvenile = 35 deg to adult = 27 deg), along with a trend towards more rapid collagen fiber strain recruitment with age, along with a drop in collagen fiber moduli, which went from 2700 kPa for the juvenile stage to 746 kPa in the adult. These changes were likely due to the previously observed impingement of the relatively stiff ascending aorta on the growing PA medial region. Intuitively, the effects of the local impingement would be to lower the local wall stress, consistent with the observed parallel decrease in collagen modulus. These results suggest that during the postnatal somatic growth period local stresses can substantially modulate regional tissue microstructure and mechanical behaviors in the PA. We further underscore that our previous studies indicated an increase in effective PA wall stress with postnatal maturation. When taken together with the fact that the observed changes in mechanical behavior and structure in the growing PA wall were modest in the other three regions studied, our collective results suggest that the majority of the growing PA wall is subjected to increasing stress levels with age without undergoing major structural adaptations. This observation is contrary to the accepted theory of maintenance of homeostatic stress levels in the regulation of vascular function, and suggests alternative mechanisms might regulate postnatal somatic growth. Understanding the underlying mechanisms will help to improve our understanding of congenital defects of the PA and lay the basis for functional duplication in their repair and replacement.

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References

Figures

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Fig. 1

(a) 3D reconstruction of the ovine ascending aorta (AA) and the pulmonary artery showing the pulmonary trunk (PT) view, with the white dashed box indicating area of contact between the two great vessels. Also shown are the posterior, anterior, lateral, and medial regions of the PA. (b) Transmural micrograph of the ovine PA and volume fraction results of the PA at the juvenile and adult states. Note that all regions demonstrated an increase in collagen mass with age, with the medial region indicating the largest mass fraction in the adult state.

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Fig. 2

Final average elastin and collagen measured orientation distributions and the Modified Beta distribution probability distribution fits in the juvenile and adult states

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Fig. 3

(a) Results of the bicubic Hermite surface interpolation of the 2nd Piola-Kirchhof stress biaxial test responses to allow interpolation of an equi-biaxial strain path, shown here in red. (b) Fit of the medial region collagen fiber recruitment using a Beta cumulative distribution function for both juvenile and adult states, revealing both an excellent fit to the data along with a trend towards more rapid recruitment with strain in the adult stage.

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Fig. 4

Fiber ensemble stress-strain results for the interpolated equi-biaxial strain path responses for all four regions at both age time points

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Fig. 5

Fiber ensemble tangent modulus-strain results for the interpolated equi-biaxial strain path responses for all four regions at both age time points. Note here the sharp increase in stiffness due to collagen fiber engagement (arrows). Also note the decreases in stiffness with age in the lateral and medial regions.

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Fig. 6

Using the results of Fig. 5, the collagen engagement strain (Elb) results for all four regions at both age time points. There were in general slightly large values for the anterior and lateral regions, and minimal changes with age.

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Fig. 7

(a) Constitutive model fit to the average five-protocol biaxial stress-stretch data (protocols 2–6, see inset) of juvenile and adult medial PA wall specimens. (b) Predicted fit results to protocols 1 and 7 (see inset), showing excellent agreement.

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Fig. 8

Predicted collagen and elastin moduli for the medial region using the actual experimental data and the β distributions. No differences were observed, suggesting the modified Beta distribution for the fiber splay (see Fig. 2) is sufficient to capture the in-plane responses of the ovine PA.

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Fig. 9

Predicted values for (a) elastin (de) and (b) collagen (dc) values for all four regions at both age time points. Here the medial region had the large values for de (statistically different from the anterior and posterior regions), whereas dc exhibited no statistically significant regional or age differences.

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Fig. 10

Predicted fiber splay deviation parameter σ for (a) elastin (σe) and (b) collagen (σc) fibers for all four regions at both age time points. While some modest differences with region and age occurred, the main finding was the medial region's drop in σe and increase in σc with age. Values presented as radians, and in degrees these changes are σc: juvenile = 17 deg to adult = 28 deg, σe: juvenile = 35 deg to adult = 27 deg.

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Fig. 11

Predicted collagen fiber recruitment for (a) mean (μr) and (b) standard deviation (σr) for all four regions at both age time points. The main observed changes were found for σr, which demonstrated decreases with age in the anterior, posterior, and lateral regions, but an increase in the medial region.

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Fig. 12

Predicted (a) collagen (κc) and (b) elastin (κe) fiber moduli regions at both age time points. The most drastic changes were for the elastin modulus ke increasing by ∼50% and the collagen modulus kc decreasing to only ∼25% of the juvenile value in the medial region.

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