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Research Papers

Regional Structural and Biomechanical Alterations of the Ovine Main Pulmonary Artery During Postnatal Growth

[+] Author and Article Information
Christopher A. Carruthers

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

Simon C. Watkins

Center for Biologic Imaging,
University of Pittsburgh,
Pittsburgh, PA 15219

John E. Mayer

Department of Cardiac Surgery,
Boston Children's Hospital and Harvard Medical School,
Boston, MA 02481

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

1 For this work, Dr. Fata won second place in the Ph.D. student paper competition in the “Cardiovascular solid mechanics” category at the 2012 summer bioengineering conference.

2Corresponding author. Present 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.

Contributed by the Bioengineering Division of ASME for publication in the JOURNAL OF BIOMECHANICAL ENGINEERING. Manuscript received December 1, 2012; final manuscript received December 27, 2012; accepted manuscript posted January 18, 2013; published online February 7, 2013. Editor: Victor H. Barocas.

J Biomech Eng 135(2), 021022 (Feb 07, 2013) (11 pages) Paper No: BIO-12-1591; doi: 10.1115/1.4023389 History: Received December 01, 2012; Accepted December 27, 2012; Revised December 27, 2012

The engineering foundation for novel approaches for the repair of congenital defects that involve the main pulmonary artery (PA) must rest on an understanding of changes in the structure-function relationship that occur during postnatal maturation. In the present study, we quantified the postnatal growth patterns in structural and biomechanical behavior in the ovine PA in the juvenile and adult stages. The biaxial mechanical properties and collagen and elastin fiber architecture were studied in four regions of the PA wall, with the collagen recruitment of the medial region analyzed using a custom biaxial mechanical-multiphoton microscopy system. Circumferential residual strain was also quantified at the sinotubular junction and bifurcation locations, which delimit the PA. The PA wall demonstrated significant mechanical anisotropy, except in the posterior region where it was nearly isotropic. Overall, we observed only moderate changes in regional mechanical properties with growth. We did observe that the medial and lateral locations experience a moderate increase in anisotropy. There was an average of about 24% circumferential residual stain present at the luminal surface in the juvenile stage that decreased to 16% in the adult stage with a significant decrease at the bifurcation, implying that the PA wall remodels toward the bifurcation with growth. There were no measurable changes in collagen and elastin content of the tunica media with growth. On average, the collagen fiber recruited more rapidly with strain in the adult compared to the juvenile. Interestingly, the PA thickness remained constant with growth. When this fact is combined with the observed stable overall mechanical behavior and increase in vessel diameter with growth, a simple Laplace Law wall stress estimate suggests an increase in effective PA wall stress with postnatal maturation. This observation is contrary to the accepted theory of maintenance of homeostatic stress levels in the regulation of vascular function and suggests alternative mechanisms regulate postnatal somatic growth. Understanding the underlying mechanisms, incorporating important structural features during growth, 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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Figures

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Fig. 1

(a) Anterior view of the ascending aorta (AA) and pulmonary trunk (PT) with medial aspect outlined (dashed square), showing the sinotubular junction (STJ) and bifurcation (BFN), which define the main pulmonary artery (PA). (b) Locations of biaxial testing samples excised from the PA's anterior (A), medial (M), posterior (P), and lateral (L) walls. Also shown are the estimated change in the PA circumference with growth (circumferential growth stretch, λθ) from Ref. [26], highlighting regions of large and small growth deformations, used to guide the specimen selection locations. (c) Sample unloaded ring (top) and stress-free (bottom) states shown for circumferential luminal and abluminal residual strain measurements at the STJ and BFN.

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Fig. 2

(a) Collagen (red) and elastin (green) of a proximal section of tunica media shown on left with each fiber population individually displayed in middle. (b) A depiction of orientation analysis of elastin fibers is demonstrated through superimposed regional fiber orientation vectors (white arrows) with corresponding normalized fiber orientation distribution graph.

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Fig. 3

The miniature biaxial stretching device combined with MPM system. Specimen's reflection in mirror captured by camera underneath the device stage (bottom).

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Fig. 4

Results from the equibiaxial stress protocol for each of four regions displayed for juvenile (circles) and adult (triangles) groups. Responses demonstrated mild nonlinearity and were circumferentially stiffer than longitudinally in all regions except the posterior wall, which was nearly isotropic in both age groups. The longitudinal compliance (maximum measured deformation) of lateral wall increased significantly with growth.

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Fig. 5

(a) Ratio of maximum longitudinal to circumferential stretch of equi-biaxial stress protocol in four regions of PA with growth. Here, the anisotropy of the medial wall increased substantially during postnatal growth while it was maintained in the other regions. (b) Circumferential residual strains at the luminal and abluminal surfaces in juvenile and adult ovine PA. Larger residual strain values were measured on abluminal surface than luminal surface in both age groups; BFN residual strain decreased considerably over time while it was maintained at STJ.

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Fig. 6

MPM image set showing different layer structures of PA. The top image is a montage of a transverse image sections of PA anterior wall with each layer labeled. MPM images of representative en-face sections of intimal, medial, and adventitial layers (bottom) displaying collagen (red) and elastin (green) structure and content in each layer: Collagen was relatively thin and had fine crimp structure in media and formed into thicker fiber bundles in adventitia; relative elastin content of media (62 ± 1%) was significantly larger than collagen while collagen was dominant fiber in adventitia (63 ± 2%).

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Fig. 7

(a) Thicknesses (in mm) of excised specimens of adult and juvenile PA. Anterior and posterior samples were consistently thicker than the medial and lateral samples. (b) Relative thickness of each arterial layer in transverse section of PA wall: media is substantially thicker than the intima and adventitia.

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Fig. 8

Regional variations in mean elastin fiber orientation and NOI from the PA wall with growth. (a) Elastin alignment in medial wall did not change significantly with growth, whereas the anterior and medial wall elastin fiber alignment was significantly closer to circumferential direction than posterior wall. (b) NOI of lateral wall was less than other regions in juvenile stage. In lateral wall, significant increase in circumferential mean orientation of elastin fibers with growth (from 23 ± 6 deg to 1 ± 7 deg) was associated with a significant drop in NOI from 60 ± 3% to 46 ± 4%. Overall, only the lateral region demonstrated statistically significant growth changes in both mean fiber direction and NOI.

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Fig. 9

The mean collagen (red) and elastin (green) fiber orientation histograms at peak physiological stretch in the juvenile and adult medial PA wall quantified in the MPM-biaxial-deformation experiments. Also shown for the elastin are the histogram results at low stretch, which were similar to the peak stretch results, supporting the assumption that equi-biaxial stretch induced no change in fiber alignment.

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Fig. 10

Growth adaptations in collagen fiber (a) tortuosity and (b) recruitment behavior of medial aspect of PA wall measured at different equibiaxial deformation levels. Overall, the adult group demonstrated greater initial tortuosity and recruitment rate compared to the juvenile state. (c) Biaxial stress-stretch behavior of medial aspect of adult PA wall near physiological biaxial stress levels demonstrated near equibiaxial deformation.

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