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Research Papers

Estimated in Vivo Postnatal Surface Growth Patterns of the Ovine Main Pulmonary Artery and Ascending Aorta

[+] Author and Article Information
Bahar Fata

Department of Bioengineering,
University of Pittsburgh,
Pittsburgh, PA 15219

John E. Mayer

Cardiac Surgery Program,
Boston Children's Hospital,
Harvard Medical School,
Boston, MA 02115

Michael S. Sacks

Professor of Biomedical Engineering
Department of Biomedical Engineering,
Institute for Computational Engineering and Science,
University of Texas,
Austin, TX 78712
e-mail: msacks@ices.utexas.edu

1Corresponding author.

Contributed by the Bioengineering Division of ASME for publication in the JOURNAL OF BIOMECHANICAL ENGINEERING. Manuscript received December 26, 2012; final manuscript received April 26, 2013; accepted manuscript posted May 22, 2013; published online June 11, 2013. Assoc. Editor: Keith Gooch.

J Biomech Eng 135(7), 071010 (Jun 11, 2013) (12 pages) Paper No: BIO-12-1635; doi: 10.1115/1.4024619 History: Received December 26, 2012; Revised April 26, 2013; Accepted May 22, 2013

Delineating the normal postnatal development of the pulmonary artery (PA) and ascending aorta (AA) can inform our understanding of congenital abnormalities, as well as pulmonary and systolic hypertension. We thus conducted the following study to delineate the PA and AA postnatal growth deformation characteristics in an ovine model. MR images were obtained from endoluminal surfaces of 11 animals whose ages ranged from 1.5 months/15.3 kg mass (very young) to 12 months/56.6 kg mass (adult). A bicubic Hermite finite element surface representation was developed for the each artery from each animal. Under the assumption that the relative locations of surface points were retained during growth, the individual animal surface fits were subsequently used to develop a method to estimate the time-evolving local effective surface growth (relative to the youngest measured animal) in the end-diastolic state. Results indicated that the spatial and temporal surface growth deformation patterns of both arteries, especially in the circumferential direction, were heterogeneous, leading to an increase in taper and increase in cross-sectional ellipticity of the PA. The longitudinal PA growth stretch of a large segment on the posterior wall reached 2.57 ± 0.078 (mean ± SD) at the adult stage. In contrast, the longitudinal growth of the AA was smaller and more uniform (1.80 ± 0.047). Interestingly, a region of the medial wall of both arteries where both arteries are in contact showed smaller circumferential growth stretches—specifically 1.12 ± 0.012 in the PA and 1.43 ± 0.071 in the AA at the adult stage. Overall, our results indicated that contact between the PA and AA resulted in increasing spatial heterogeneity in postnatal growth, with the PA demonstrating the greatest changes. Parametric studies using simplified geometric models of curved arteries during growth suggest that heterogeneous effective surface growth deformations must occur to account for the changes in measured arterial shapes during the postnatal growth period. This result suggests that these first results are a reasonable first-approximation to the actual effective growth patterns. Moreover, this study clearly underscores how functional growth of the PA and AA during postnatal maturation involves complex, local adaptations in tissue formation. Moreover, the present results will help to lay the basis for functional replacement by defining critical geometric metrics.

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Figures

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Fig. 1

(a) 3D rendered anatomical positions of the ascending aorta (AA) and pulmonary trunk (PT), shown in the anterior view (Top), with the medial aspect outlined as a dashed square), and in the posterior view (Bottom). (b) and (c) illustrate nonregistered images of the oldest adult pulmonary artery (PA) and AA (Top), and registered to their corresponding templates of youngest animal (Bottom). Note that the main side branch coming off of AA in ovine branches off to brachiocephalic, left common carotid and left subclavian arteries at a more distal point.

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Fig. 2

(a) The common center axis of the PA along with individual center axes points (black) from multiple time points (scaled), with the Frenet frame and global Cartesian coordinate systems. Note the high degree of consistency between the centerline paths from the animals studied. Also shown in (b) are the AA and PA center axes from two perspectives to demonstrate larger tortuosity of PA compared to AA. (c) A schematic surface parameterization and deformation showing the base vectors in the reference to the end-diastolic loaded state of the youngest animal (15 kg) and those of current or ‘deformed’ geometry and the fitted centerline (CL).

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Fig. 3

Basic geometric information of the growing AA and PA. (a) Orientation of cross-section major axes along the center axis coordinate s (as an index of twist), showing while that of the PA remained mostly unaltered, the AA reduced with growth. (b) Alteration in arterial taper with growth, as measured by the ratio of cross-sectional areas of BFN or end-ROI to the STJ, was substantially more prominent in the PA than AA. (c) Cross-sectional ellipticity of the PA increased substantially with growth (left), whereas in the AA it was relatively maintained (right). These simple measures underscore the geometric complexities of great vessel growth during the post-natal period.

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Fig. 4

Time-interpolated circumferential growth stretches on medial/posterior walls of PA (top) and AA (bottom). Both arteries demonstrated highly heterogeneous distributions, likely due to mutual mechanical interactions. Note in particular the effect of impingement on the PA medial wall by the AA, which resulted in reduced local deformations.

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Fig. 5

Time-interpolated circumferential growth stretch on anterior and lateral walls of PA (top) and AA (bottom). Overall, this aspect of both vessels experienced more homogenous growth, with the PA of slightly higher heterogeneity.

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Fig. 6

Time-interpolated longitudinal growth stretch of posterior and a segment of medial walls of PA (top) were significantly larger, due to a larger curvature, than that of the posterior wall of AA (bottom)

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Fig. 7

(a) Time-interpolated longitudinal growth stretch of anterior walls of PA (top) and AA (bottom), showing relatively uniformly changed with age with larger values in the PA at the 60 kg growth stage due to its larger curvature than AA. (b) Longitudinal growth stretch profiles shown along four walls of PA (left) and AA (right)

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Fig. 8

(a) Stretch profiles at the adult stage (60 kg) of the PA and AA taken from paths along four wall locations along the length of each artery. (b) Circumferential growth stretch profiles of medial (M), lateral (L), anterior (A) and posterior (P) walls of the PA and AA. Note: In a small region after AA main side branch, towards which is oriented, slower circumferential growth rate was measured. (c) Corresponding longitudinal growth stretch profiles. Overall, these results underscored the pronounced variation in longitudinal growth stretch for the PA and circumferential growth stretch for both the AA and PA.

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Fig. 9

Geometric parametric studies using a tapered cylinder and two toroid phantoms, with key dimensions taken from the PA measurements. For the tapered cylindrical phantom, heterogeneous change in λθ with growth is clearly evident. In contrast, the presence of curvature in the circular cross-section toroid phantom produced heterogeneous λs patterns. When both effects were combined in the tapered elliptical toroid, (which geometrically most closely represented PA geometry), the resulting phantom demonstrated both heterogeneous growth deformation patterns as estimated in the PA in vivo.

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