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Research Papers

Local Versus Global Mechanical Effects of Intramural Swelling in Carotid Arteries

[+] Author and Article Information
T. A. Sorrentino, L. Fourman, J. Ferruzzi, K. S. Miller

Department of Biomedical Engineering,
Yale University,
New Haven, CT 06511

J. D. Humphrey

Department of Biomedical Engineering,
Yale University,
New Haven, CT 06511
Vascular Biology and Therapeutics Program,
Yale School of Medicine,
New Haven, CT 06511

S. Roccabianca

Department of Biomedical Engineering,
Yale University,
New Haven, CT 06511
e-mail: roccabis@egr.msu.edu

1Present address: Department of Mechanical Engineering, Michigan State University, East Lansing, MI 48823.

2Corresponding author.

Manuscript received July 18, 2014; final manuscript received December 1, 2014; published online February 16, 2015. Assoc. Editor: Hai-Chao Han.

J Biomech Eng 137(4), 041008 (Apr 01, 2015) (8 pages) Paper No: BIO-14-1330; doi: 10.1115/1.4029303 History: Received July 18, 2014; Revised December 01, 2014; Online February 16, 2015

Glycosaminoglycans (GAGs) are increasingly thought to play important roles in arterial mechanics and mechanobiology. We recently suggested that these highly negatively charged molecules, well known for their important contributions to cartilage mechanics, can pressurize intralamellar units in elastic arteries via a localized swelling process and thereby impact both smooth muscle mechanosensing and structural integrity. In this paper, we report osmotic loading experiments on murine common carotid arteries that revealed different degrees and extents of transmural swelling. Overall geometry changed significantly with exposure to hypo-osmotic solutions, as expected, yet mean pressure-outer diameter behaviors remained largely the same. Histological analyses revealed further that the swelling was not always distributed uniformly despite being confined primarily to the media. This unexpected finding guided a theoretical study of effects of different distributions of swelling on the wall stress. Results suggested that intramural swelling can introduce highly localized changes in the wall mechanics that could induce differential mechanobiological responses across the wall. There is, therefore, a need to focus on local, not global, mechanics when examining issues such as swelling-induced mechanosensing.

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Figures

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Fig. 1

(Top) Schematic representation of the four configurations of interest: an overall unswollen traction-free configuration κtf, an osmotically loaded and mechanically preconditioned configuration κprec*, an axially stretched and pressurized configuration κP*, and an osmotically loaded only (not preconditioned) configuration κol*. (Middle and bottom) Swelling ν*measured experimentally between configurations defined in the top panel, evaluated for each solution of interest: control HBSS (i.e., 270 mOsm/l, light gray) and hypo-osmotic HBSS at 33% (i.e., 90 mOsm/l, dark gray) or 3.3% (i.e., 9 mOsm/l, black) content of sodium chloride. In particular, the middle panel shows on the left the swelling due to both the osmotic loading and the mechanical preconditioning, between configurations κtf and κprec*, and on the right the swelling associated with axial extension and pressurization of the vessel, between configurations κprec*and κP*. The bottom panel shows on the left the swelling due to the osmotic loading alone, between configurations κtf and κol*, and on the right the swelling associated with mechanical preconditioning alone, between configurations κol* and κprec*. The asterisks represent statistically significant differences (one way ANOVA, p < 0.05).

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Fig. 2

Averaged experimental data for pressure–diameter responses of mouse common carotid arteries exposed to three different testing solutions: control iso-osmotic solution (i.e., 270 mOsm/l, triangle), and hypo-osmotic solutions with a reduced content of NaCl of 33% (i.e., 90 mOsm/l, square) and 3.3% (i.e., 9 mOsm/l, diamond)

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Fig. 8

Linearized circumferential stiffness for the hypo-osmotic solutions (90 mOsm/l and 9 mOsm/l) for an axial stretch of λziv*~1.60 and λziv*~1.40, respectively, and an internal pressure of 93.3 mmHg. The thick lines correspond to the distributions of swelling, as shown in Fig. 4: a sigmoidal distribution concentrating the swelling within the medial layer (dashed line) and a peak distribution concentrating the swelling in one intralamellar space within the media (solid line). The dotted line represents the unswollen, homeostatic (control) case. The arrows on the left represent the integral averages of stiffness within the wall.

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Fig. 7

Axial stress distribution for the hypo-osmotic solutions (90 mOsm/l and 9 mOsm/l) for an axial stretch of λziv*~1.60 and λziv*~1.40, respectively, and an internal pressure of 93.3 mmHg. The lines correspond to the distributions of swelling, as shown in Fig. 4: a sigmoidal distribution concentrating the swelling within the medial layer (dashed line) and a peak distribution concentrating the swelling in one intralamellar space within the media (solid line). The dotted line represents the circumferential stress for the homeostatic, unswollen, control case.

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Fig. 6

Circumferential (hoop) stress distribution for the hypo-osmotic solutions (90 mOsm/l and 9 mOsm/l) for an axial stretch of λziv*~1.60 and λziv*~1.40, respectively, and an internal pressure of 93.3 mmHg. The lines correspond to the distributions of swelling, as shown in Fig. 4: a sigmoidal distribution concentrating the swelling within the medial layer (dashed line) and a peak distribution concentrating the swelling in one intralamellar space within the media (solid line). The dotted line represents the circumferential stress for the homeostatic, unswollen, control case.

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Fig. 5

Simulated (solid and dashed lines) and experimental (symbols) pressure–diameter behavior for mouse carotid arteries. The top panel represents the iso-osmotic solution (270 mOsm/l), the middle panel the hypo-osmotic solution at 33% (90 mOsm/l), and the bottom panel the hypo-osmotic solution at 3.3% (9 mOsm/l), respectively. Recall that the baseline model was based on independent biaxial data [10]. The gray area shows the interval of confidence due to the standard error affecting all the geometrical quantities recorded experimentally (e.g., outer diameter and axial stretch in the homeostatic configuration, amount of swelling due to the different osmolarity of the solutions). Goodness of prediction is provided in terms of root mean square error RMSE. Note that the simulations for the sigmoidal (dashed line) and concentrated (solid line) swelling were essentially superimposed; only at the lowest pressure in the bottom panel can they be delineated.

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Fig. 4

Swelling ν* for two hypo-osmotic solutions considered in this study. Shown are two possible distributions of swelling motivated by the histological images shown in Fig. 3: a sigmoidal distribution concentrating the swelling uniformly within the medial layer (dashed line) and a peak distribution concentrating the swelling mainly within one intralamellar space within the media (solid line). Also noted in each panel is the average normalized change in volume (i.e., det(F*) = ν*, with ν* = 1.09 or ν* = 1.33), namely, the amount of swelling due to each hypo-osmotic solution and preconditioning (Fig. 1, middle left) normalized by the preconditioning related swelling in control vessels only (Fig. 1, bottom right). The dotted, vertical lines represent the medial–adventitial border in the traction-free intact unloaded configuration.

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Fig. 3

Histological cross sections of osmotically swollen arteries (i.e., Verhoeff-Van Gieson stain). Carotid arteries mechanically tested in (a) iso-osmotic HBSS with no apparent intralamellar swelling, (b) 3.3% hypo-osmotic HBSS displaying a uniform swelling within the medial layer, and (c) 3.3% hypo-osmotic HBSS displaying a swelling concentrated in the outermost intralamellar space.

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