Research Papers

In Vitro Quantification of Time Dependent Thrombus Size Using Magnetic Resonance Imaging and Computational Simulations of Thrombus Surface Shear Stresses

[+] Author and Article Information
Joshua O. Taylor

Department of Bioengineering,
The Pennsylvania State University,
University Park, PA 16802;
Applied Research Laboratory,
The Pennsylvania State University,
State College, PA 16803

Kory P. Witmer

Department of Bioengineering,
The Pennsylvania State University,
University Park, PA 16802

Thomas Neuberger

Huck Institutes of the Life Sciences,
The Pennsylvania State University,
University Park, PA 16802;
Department of Bioengineering,
The Pennsylvania State University,
University Park, PA 16802

Brent A. Craven

Applied Research Laboratory,
The Pennsylvania State University,
State College, PA 16803;
Department of Bioengineering,
The Pennsylvania State University,
University Park, PA 16802

Richard S. Meyer, Steven Deutsch

Applied Research Laboratory,
The Pennsylvania State University,
State College, PA 16803

Keefe B. Manning

Department of Bioengineering,
The Pennsylvania State University,
University Park, PA 16802;
Department of Surgery,
The Penn State College of Medicine,
Hershey, PA 17033
e-mail: kbm10@psu.edu

1Corresponding author.

Manuscript received November 12, 2013; final manuscript received April 25, 2014; accepted manuscript posted May 8, 2014; published online May 23, 2014. Assoc. Editor: Ender A. Finol.

J Biomech Eng 136(7), 071012 (May 23, 2014) (11 pages) Paper No: BIO-13-1526; doi: 10.1115/1.4027613 History: Received November 12, 2013; Revised April 25, 2014; Accepted May 08, 2014

Thrombosis and thromboembolization remain large obstacles in the design of cardiovascular devices. In this study, the temporal behavior of thrombus size within a backward-facing step (BFS) model is investigated, as this geometry can mimic the flow separation which has been found to contribute to thrombosis in cardiac devices. Magnetic resonance imaging (MRI) is used to quantify thrombus size and collect topographic data of thrombi formed by circulating bovine blood through a BFS model for times ranging between 10 and 90 min at a constant upstream Reynolds number of 490. Thrombus height, length, exposed surface area, and volume are measured, and asymptotic behavior is observed for each as the blood circulation time is increased. Velocity patterns near, and wall shear stress (WSS) distributions on, the exposed thrombus surfaces are calculated using computational fluid dynamics (CFD). Both the mean and maximum WSS on the exposed thrombus surfaces are much more dependent on thrombus topography than thrombus size, and the best predictors for asymptotic thrombus length and volume are the reattachment length and volume of reversed flow, respectively, from the region of separated flow downstream of the BFS.

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Grahic Jump Location
Fig. 1

(a) A schematic of the flow loop containing the acrylic BFS model used for MRI experiments. The inlet and outlet tubes were only used for filling/draining the loop and were clamped during blood circulation. Arrows indicate the direction of flow. (b) A cross-sectional view of both segments of the BFS model at the seam.

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Fig. 2

(a) Inlet, (b) outlet, (c) acrylic, and (d) thrombus STL files exported from Avizo for a thrombus formed after 10 min of blood circulation

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Fig. 3

An image obtained from histology sectioning displaying a magnified view of a thrombus surface that was exposed to blood flow. The primary components of the thrombus, red blood cells, and fibrin have been stained a pinkish-red color by H&E. A purple stained nucleus of a white blood cell can also be observed in the slice. Black circles illustrate two surface features (one valley and one protrusion) that are too small to be resolved in this study.

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Fig. 4

Velocity map and contours presented for the empty BFS model. The recirculation region can clearly be observed downstream of the step, with the site of initial thrombus formation indicated with a white “X.” The reattachment length measures 16.9 mm (6.76 S) and flow is from left to right.

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Fig. 5

Reconstructions of thrombi formed after all blood circulation times considered in this study (one representative thrombus for each time). The blood circulation time is displayed in the left column, a side view of the thrombus is presented in the middle column, and a top view of the thrombus is presented in the right column. The asymptotic behavior of both thrombus height and length can be observed qualitatively. The scale bar represents a distance of 5 mm, and the thrombi were formed in flow moving from left to right.

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Fig. 6

(a) Changes in normalized thrombus height (measured at the step) and length with increasing blood circulation time are presented. These values were normalized with the BFS height, 2.5 mm. The reattachment length of the initial recirculation region was normalized by the step height and marked on the right vertical axis. Error bars represent the SEM and n = 3 for all blood circulation times. (b) The changes in thrombus volume and exposed surface area (SA) with increasing blood circulation time are presented. Error bars represent the SEM and n = 3 for all blood circulation times.

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Fig. 7

Both the mean and maximum WSS and WSR calculated on the thrombus surfaces are presented with increasing blood circulation time. Error bars represent the SEM and n = 3 for all blood circulation times.

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Fig. 8

WSS distributions and corresponding histograms for all three thrombi imaged after 30 min of blood circulation. For panels (a)–(c), the mean/maximum WSS values are 0.13/2.2, 1.45/11.0, and 0.35/5.1 dyn/cm2, respectively.

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Fig. 9

Three axial slices of the lumen through a representative thrombus after (a) 10, (b) 30, and (c) 60 min of blood circulation. Velocity contours are shown to illustrate recirculation regions, and the acrylic model has been outlined in white after the BFS to show the thrombus boundaries. The positions of the slices are indicated with white lines across the WSS distribution on the thrombus surface. A white arrow on each velocity plot denotes the location of the step, and flow is from left to right in all plots. The length scales are different for the velocity and WSS plots. (a) Regions of high WSS are predicted on protrusions from the thrombus surface, even though the entire thrombus is contained within a recirculation region. (b) Location 1 in the velocity plot indicates a portion of the thrombus protruding into the lumen which causes a small recirculation region to develop downstream. This same location in the WSS plot has heightened WSS on the peak followed by a region of very low WSS. Location 2 indicates a recirculation region extending nearly the length of the thrombus, and this corresponds to a strip of low WSS. An example recirculation region has been magnified to provide a better view. (c) Location 3 in the velocity plots indicates a small recirculation region immediately downstream of the step which is reflected as a low WSS region on the upstream portion of the thrombus surface. Location 4 indicates a protrusion that extends far into the lumen of the model. This corresponds to the highest WSS calculated on any of the thrombus surfaces in this study. Location 5 indicates a small recirculation region that forms after this peak and the low WSS region that the CFD predicted at the same location.

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Fig. 10

Histograms of the WSS magnitude for the representative thrombi shown in Figs. 9(a)9(c). (a) Corresponds to the 10 min thrombus in Fig. 9(a), 9(b) corresponds to the 30 min thrombus in Fig. 9(b), and 9(c) corresponds to the 60 min thrombus in Fig. 9(c).




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