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. 2023 Jun 12;31(5):675–682. doi: 10.1177/15910199231182850

A novel method for preparing clot analogs under dynamic vortical flow for testing mechanical thrombectomy devices

Ronghui Liu 1,2, Bin Lv 3, Haoye Meng 4, Luo Zhang 2, Weijing Ma 5, Hongping He 2, Ren Wei 6, Na Ma 1,7, Yubo Fan 1, Jun Wang 3,✉, Xuewen Ren 8,✉, Weidong Wang 2,✉
PMCID: PMC12475351  PMID: 37309134

Abstract

Background

Clot analogs are essential in animal and in vitro experiments on mechanical thrombectomy devices for treating acute ischemic stroke. Clot analogs should be capable of reproducing a variety of arterial clots observed in clinical practice in terms of histological composition and mechanical properties.

Methods

Bovine blood with added thrombin was stirred in a beaker so that clots could be formed under the condition of dynamic vortical flow. Static clots were also prepared without stirring, and the properties of the static clots and dynamic clots were compared. Histological and scanning electron microscopy experiments were performed. Compression and relaxation tests were performed to evaluate the mechanical properties of the two types of clots. Thromboembolism and thrombectomy tests were conducted in an in vitro circulation model.

Results

Compared to the static clots, the dynamic clots prepared under vortical flow displayed a higher fibrin content, and their fibrin network was denser and sturdier than that of the static clots. The stiffness of the dynamic clots was significantly higher than that of the static clots. The stress of both types of clots could decay quickly under large sustained strain. The static clots could break at the bifurcation in the vascular model, while the dynamic clots could be firmly stuck in the vascular model.

Conclusions

Dynamic clots generated in dynamic vortical flow differ significantly from static clots in terms of their composition and mechanical properties, which may be beneficial information for preclinical research on mechanical thrombectomy devices.

Keywords: Clot analogs, acute ischemic stroke, mechanical thrombectomy, in vitro model

Introduction

In recent years, mechanical thrombectomy has emerged as an effective technique for treating acute ischemic stroke with large vessel occlusion. The recanalization rate can reach approximately 80–90% using mechanical thrombectomy devices, such as stent retrievers and aspiration catheters.1,2 Many novel devices and creative methods have appeared to improve the recanalization rate and reduce complications such as vascular injury and distal embolization. In vitro models and animal models play important roles in the preclinical evaluation of these novel devices and methods.

Blood clots are primarily composed of fibrin and blood cells. Clots can be hard or soft, and each type has different mechanical properties. It is generally believed that soft clots contain more red blood cells (RBCs), while hard clots are rich in fibrin. The mechanical properties of the thrombus can influence its interaction with the thrombectomy device and the recanalization rate. In several animal and in vitro studies, a decreased recanalization rate of thrombectomy devices for treating hard clots has been reported.3,4

The preparation of clot analogs is necessary for in vitro and animal experiments on mechanical thrombectomy devices. The most common technique for preparing clot analogs is to induce thrombus formation in whole blood by thrombin addition under static conditions. 5 Since the clot prepared by this method is soft, it cannot be used to evaluate the performance of thrombectomy devices interacting with hard fibrin-rich clots. Previous studies have applied various methods for preparing fibrin-rich hard clots. For example, Duffy et al. 6 successfully prepared clots with different compositions by centrifuging plasma and RBCs and mixing them in a specific ratio. Many in vitro experiments have prepared hard clots using similar methods.4,7,8 In the literature, the preparation of hard thrombi by the addition of fibrinogen has also been reported.9,10

The structural compositions and mechanical properties of biological tissues are significantly influenced by the mechanical environment they are exposed to. The arterial system has a fast flow velocity and high blood pressure and is a complex flow environment. Vortical flow occurs in the heart and swirling flow occurs in arteries.11,12 However, many of the aforementioned methods produce clots under static conditions, which is quite different from the arterial thrombosis that occurs in the mechanical environment of the body. The Chandler loop, which is a slowly rotating circular tube, can also be used to prepare thrombi under dynamic conditions. 13 Although the Chandler loop simulates the shear effect between blood flow and the vessel wall, it does not include a complex hemodynamic environment, such as that of vortical flow in the heart. Due to these different mechanical environments, the clot analogs prepared by the aforementioned methods may be different from real arterial thrombi in terms of composition and microstructure, which may affect the accuracy of the results of in vitro and animal experiments on mechanical thrombectomy devices.

This study identifies a new method for preparing clot analogs under dynamic vortical flow and compares dynamic clot analogs with static clot analogs in terms of their histological compositions, microstructures, and mechanical properties. Thromboembolism and mechanical thrombectomy tests were performed on dynamic clots in an in vitro circulation model. We hope that this novel technique will be applied for thrombectomy devices in animal and in vitro research to support the testing and development of new devices and methods.

Materials and methods

Clot preparation

Fresh bovine whole blood (Beijing Bersee Science and Technology, China) with 3.8% sodium citrate was used to prepare clot analogs, which were preserved at 4 °C prior to use. Briefly, 5 ml of blood was poured into a 10 ml beaker in a water bath at 37 °C. Then, 2.27% calcium chloride was added to the blood at a 1:10 ratio. Thrombin was added at 2.5 NIHU/ml blood, followed by shaking for 5 s. For static thrombus preparation, the blood was injected with a syringe into a polytetrafluoroethylene (PTFE) tube with an inner diameter of 5 mm and placed at 37 °C for 1 h. To prepare dynamic clots, the blood in the beaker was stirred for 20 min in a 37 °C water bath using a blender. The stirring bar was made of PTFE. The rotation speed was 500 rpm. The clots formed under dynamic conditions could be seen attached around the stirring bar after the stirring was completed. The formed static and dynamic thrombi were removed, placed into saline, and cut into desired dimensions for further use.

Histological evaluation

The clots were washed in saline and immediately placed into 10% neutral buffered formalin for fixation for 48 h. After washing in phosphate-buffered saline (PBS), they were embedded in paraffin, cut into 4 μm slices, and stained with hematoxylin and eosin (H&E).

Scanning electron microscopy (SEM)

The thrombi were fixed in 2.5% glutaraldehyde for more than 4 h, rinsed in PBS, and dehydrated with an ethanol gradient (75%, 90%, and 100%). The samples were dried by a critical point dryer (EM CPD300, Leica Microsystems Gmbh, Vienna, Austria). Finally, samples were sprayed with platinum and observed with a scanning electron microscope (S-4800, Hitachi, Japan) at a resolution of 1 nm and magnification of 1500×. The operating voltage and current were 5 kV and 10 μA, respectively.

Compression test

The clots were cut into cylindrical specimens approximately 4 mm in diameter and 3 mm in height. Seven samples of each clot type were evaluated with an electromechanical system (MTS E43.104, USA) with a load sensor of 100 N. The maximum compression strain was 80%. The loading rate was 2 mm/min. The stress was expressed as σ = F/A, where F is the load, and A is the initial cross-sectional area of the clot. The strain was defined as ε = (L2–L)L2, with L0 representing the initial height of the clot and L denoting the height of the clot after deformation. The stress–strain curves of the loading process were recorded, and the tangent stiffness of the stress–strain curves at 60% and 80% strains was calculated.

The sample size and experimental equipment for the stress relaxation test were identical to those used for the compression test. The samples were rapidly compressed to 80% strain at a rate of 1 mm/s, and then the strain was held constant for 300 s. The stress variation during the process was recorded. Nine samples of each clot type were examined. The differences between the two clot groups were compared using the Mann–Whitney U test (GraphPad Prism 9.0).

In vitro thromboembolism test

The in vitro test model consisted of a liquid diaphragm pump (PLAB2001, Preclinic Medtech, Shanghai, China), a transparent cerebral vascular phantom (Preclinic Medtech, Shanghai, China), and a thermostatic water tank (PLAB3001, Preclinic Medtech, Shanghai, China) connected to silicon tubes filled with saline solution at 37 °C. The connection diagram of the test system was previously shown in the literature. 14 The vascular phantom included the internal carotid artery (ICA), the M1 and M2 segments of the middle cerebral artery (MCA), and the A1 segment of the anterior cerebral artery (ACA) (Figure 1F). Leptomeningeal collateral circulation was reproduced by the connection between the distal MCA branch and the terminal ACA branch. The flow state in the circuit remained constant and was measured by ultrasonic flow meters (Xunyin Technology, Shanghai, China). The pressures were measured by two invasive pressure sensors (JCR Medical Technology, Shenzhen, China) with an intensive care unit monitor (C80-V, Comen Medical Instrument, Shenzhen, China). Valves were placed behind the vascular model to regulate the flow resistance in the flow circuit. The flow rate and pressure in the model were maintained within physiological ranges by controlling the output rate of the pump and the valves in the flow circuit (Figure 1F). When no clot was injected, the ICA and MCA flows were 230 ml/min 15 and 130 ml/min, 16 respectively. The MCA branch had a proximal pressure of approximately 81 mmHg.

Figure 1.

Figure 1.

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Preparation process of static and dynamic clots (A); static clot (B); dynamic clot (C); blood stirring with a stirrer in the beaker (D); compression test (E); fluid circuits in the in vitro test platform (F).

The thromboembolism test was performed on static and dynamic clots. The static and dynamic clots were cut to 15 mm in length and 4 mm in diameter. Eight tests were administered to each group. The flow pump was turned on when the clots were placed at the entry of the vascular model. The procedure was recorded by a video imaging system (DSC-HX90, Sony, Japan).

In vitro thrombectomy test

The thrombectomy test for dynamic clots was performed in vitro in the same model. The size of dynamic clots was the same as that in the thromboembolism test. A 6 Fr intermediate catheter (Navien, ev3, Irvine, CA, USA) was inserted near the clot through a 6 Fr guiding sheath (Cook Medical, Bloomington, IN, USA). A stent retriever (Solitaire FR 6*30, ev3, Irvine, CA, USA) was delivered to the embolization site and released through a microcatheter (rebar-18, ev3, Irvine, CA, USA). The stent retriever was carefully pulled back to the intermediate catheter with aspiration after waiting for 3–5 min. The above procedures were repeated if clots remained in the vascular model, but the total number of passes was limited to three. A total of eight tests were performed to assess the recanalization rate.

Results

The H&E stained the RBCs in red and fibrin in pink. Nearly all the static clots were homogeneous (Figure 2A) with sparse fibrin (Figure 2C). A significant amount of fibrin could be seen in the dynamic clots, with fibers oriented in various directions and patterns (Figures 2B and 2D). The dynamic clots exhibited more pronounced heterogeneity, with regions with more RBCs and regions with more fibrin. Scanning electron microscopy (SEM) revealed that the fibrin network of the static clots was sparse (Figure 2E), while the fibrin network of the dynamic clots was dense. The fiber bundles of the dynamic clots were thicker and directional in some areas (Figure 2F).

Figure 2.

Figure 2.

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H&E staining results of static (A) and dynamic clots (B) at 5× magnification; H&E staining results of static (C) and dynamic clots (D) at 20× magnification; scanning electron microscopy images showing the microstructures of static (E) and dynamic clots (F).

Figure 3A shows the stress–strain curves of the two clots under compression. The dynamic clots showed significantly higher stiffness than the static clots. The median value of stiffness was 13.96 kPa for the static clots and 65.06 kPa for the dynamic clots under a strain of 60%, showing a significant difference (P < 0.001, confidence interval [CI] = 95%) (Figure 3B). The median stiffness values of the static and dynamic clots were 92.6 kPa and 636.5 kPa at 80% strain, respectively (P < 0.001, CI = 95%) (Figure 3C).

Figure 3.

Figure 3.

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Stress–strain curves measured during the compression test (A); comparison of the stiffness of static and dynamic clots at 60% and 80% strains (B and C); stress relaxation curve (D); comparison of time required for 80% attenuation from the peak stress (E); stress value comparison after relaxation for 300 s (F). “d” indicates dynamic clots and “s” indicates static clots.

Figure 3D shows the stress–time curves of the thrombus relaxation process for both groups. The stress of the clots in both groups decayed rapidly under 80% strain, but the stress of the dynamic clots decayed even faster. The time required to decay 80% of the peak stress was significantly different between the static and dynamic clots (median: 10.5 vs. 4.41; P < 0.0001, CI = 95%) (Figure 3E). After 300 s, the median value of the final stress was 1.876 kPa for the static clots and −2.914 kPa for the dynamic clots, which indicated a significant difference (P < 0.0001, CI = 95%) (Figure 3F).

The thromboembolism experimental results are shown in Table 1. Interestingly, all static clots broke off at the T-shaped bifurcation and flowed to the MCA and ACA. The difference was that 37.5% of the cases were nonruptured clots that could be embolized in both the MCA and ACA branches. In 50% of the cases, after breaking at the T-branch, the clots flowing to the MCA could be stuck in the M2 segment (Figure 4A-C). In 12.5% of the cases, after the clots broke at the T bifurcation, they broke again at the M2 segment bifurcation, and some of the clot fragment flowed to the distal MCA. In contrast, none of the dynamic clots fractured, and all of them could be firmly embolized in vessel branches; specifically, 62.5% of the clots were embolized at the T bifurcation. Twenty-five percent of them were embolized in the proximal M1 and A1 segments, and 12.5% of them were embolized in the A1 segment.

Table 1.

Thromboembolism test.

Situation Result Percentage
Static clot
Broke at the T-shaped bifurcation, and none of the clot fragments were stuck in the ACA and MCA branches (3/8) 37.5%
Broke at the T-shaped bifurcation, and the clots flowing to the MCA were stuck in the M2 segment. The clot fragments flowing to the ACA were not stuck in the A1 segment (4/8) 50%
Broke at the T-shaped bifurcation and again at the M2 segment bifurcation, and some of the clot fragments could flow to the distal MCA. The clot fragments flowing to the ACA were not stuck (1/8) 12.5%
Dynamic clot
Stuck at T-shaped bifurcation (5/8) 62.5%
Stuck at the proximal M1 and A1 branches (2/8) 25%
Stuck at the proximal A1 branch (1/8) 12.5%
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Figure 4.

Figure 4.

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In the thromboembolism test, the static clot broke at the T-shaped bifurcation and did not stick at the anterior cerebral artery branch, while partial clot fragments stuck in the branch of the M2 segment (A–C). Dynamic clots were firmly stuck at the T-shaped bifurcation (D and E). The mechanical thrombectomy test was performed with dynamic clots (F).

In the in vitro mechanical thrombectomy test, the recanalization rate was 87.5%. The average pass number was 1.75. The first-pass recanalization rate was 50%.

Discussion

Clot analogs are essential for the research and testing of thrombectomy devices and other new stroke-treatment devices.17,18 Clot analogs should be similar to the real clots formed in the body in terms of composition and mechanical properties. In this research, a method for creating clot analogs under dynamic vortical flows was proposed, and the histological, microstructural, and mechanical properties of the clot analogs were investigated. Thromboembolism and thrombectomy tests were performed in an in vitro circulation model.

The structure and strength of biological tissues are closely related to the mechanical environment to which they are exposed. Arterial systems are characterized by high flow rates, high pressures, and complex flow conditions. The flow conditions in this study were close to some of the flow characteristics in the heart and artery. The velocity of blood in the churning beaker was also in the range of the arterial flow velocity. There are vortices in the left atrium and left atrial appendage. 11 Abnormal vortices in the left atrial appendage may induce thrombosis and ischemic stroke during atrial fibrillation. 12 In addition to having high blood pressure and flow rate, swirling flow can be exhibited by the aorta. Therefore, clot analogs formed under dynamic vortical flow may be more similar to arterial thrombi than those formed under static conditions.

Although the relationship between thrombus histological composition and stroke etiology is controversial according to the literature, 19 both cardioembolic and noncardioembolic clots have a relatively high fibrin content. 20 In our histological examination, it was found that dynamic clots had higher fibrin contents than static clots. The SEM experiments also demonstrated that the fibrin network of dynamic clots was dense, while that of static clots was sparse. Liu et al. 21 analyzed the heterogeneity of clots removed during mechanical thrombectomy. Our histological examination showed that, compared to the static clots, the dynamic clots had heterogeneity that was more comparable to that of human arterial thrombi. Thus, dynamic clot analogs are closer to arterial thrombi in terms of fibrin content and thrombus heterogeneity.

The compression test results of static clots were similar to those observed by Malone et al. 22 and represented slightly smaller values than those observed by Johnson et al. 23 The stiffness of the dynamic clots in our study was comparable to that of the thrombi retrieved from the human body in the study by Chueh et al. 24 Moreover, Johnson et al. 23 showed that there is no difference in the stiffness between whole blood thrombi and thrombi formed under static conditions with 0% hematocrit. However, we found that the dynamic clots were more rigid than the static clots under moderate and large strains. Considering the histological and SEM results, we speculated that although the ratio of fibrin to erythrocytes is important, the fibrin network density and the robustness of network fibers are also important factors affecting clot stiffness.

Stress relaxation reflects the viscoelastic phenomenon of clots. Both clots could relax quickly, and the stress of the dynamic clots decayed faster. At 300 s, the stress of the static clots was still maintained at a positive value, while the relaxation stress of the dynamic clots was already negative, implying that the clots were exerting a slight tension on the indenter at this time. This phenomenon was also observed by Malone et al., 22 possibly due to the stronger viscosity of dynamic clots. Johnson et al. 23 measured stress relaxation in clots with several hematocrit ratios and found a larger relaxation range in clots with a higher fibrin content. In our experiment, the dynamic clots had a higher fibrin content and a greater stress relaxation range, which is consistent with Johnson's results. The clinical requirement is that the stent retriever should be left for 3–5 min after capturing the clots but before retrieval. In our test, it was found that the relaxation stress of both types of clots could decay towards stable values during this time.

Erythrocyte-rich thrombi have been found to be more likely to migrate in clinical studies. 25 Malone et al. 22 found that static clots were easily torn during tensile testing. To our knowledge, we are the first to report the easy fracture property of static clots in an in vitro model. In contrast, dynamic clots could be easily stuck in the vascular model, and none of them broke, which was consistent with the finding from the compression test of the dynamic clots showing higher stiffness. The high coefficient of friction of fibrin-rich thrombi may also be a determining factor. 26 Based on the performance of static and dynamic clots in thromboembolism testing, we hypothesized that dynamic clots might closely resemble emboli at the onset of acute ischemic stroke and that static clots might be more similar to thrombi that form secondary to poor blood flow after embolization. Since static clots could not be firmly embolized in the vascular model, only dynamic clots were tested for thrombectomy. The recanalization rate and the number of passes of dynamic clots are similar to those in the literature.15,27,28

Interestingly, beakers with identical volumes (10 ml) and diameters (20 cm) to those of the left atrial appendage were used in this study. Furthermore, at a stirring rate of 500 r/min, the flow velocity in the beaker (maximum value of 52.3 cm/s) was also similar to that in the left atrial appendage. 29 Therefore, the device used to prepare dynamic clots has application potential in investigating thrombosis in the left atrial appendage. Preliminary experiments found that similar dynamic clots could be formed with lower stirring rate using the blender (200 rpm) or with manual stirring using a glass rod (approximately 100 rpm), but with lower stiffness than at 500 rpm. The median values of tangential stiffness at 80% strain were 469.5 kPa and 333.5 kPa, respectively.

Dynamic clots prepared by the Chandler loop device have also been used for testing thrombectomy devices.27,30 Histological examination of these clots showed a high fibrin content with distinct areas of RBCs and white blood cells,6,31,32 which is similar to the dynamic thrombi we prepared. Shao et al. 31 found that thrombi formed in a modified Chandler Loop had greater maximum tensile length in the manual elongation test and lower fracture rates in the catheter injection test. However, to our knowledge, the compression mechanical response of clots prepared by the Chandler loop has not been reported. In addition, dynamic clots prepared by vertical rotator also exhibited heterogeneity and large stiffness. 33 In the future, the properties of dynamic clots prepared by these different methods need to be further compared.

There are some limitations in this study. First, bovine blood was used for clot preparation. Chueh et al. 24 reported that bovine thrombi are more rigid than human thrombi. Future research should assess the characteristics of human thrombi generated by our approach. Second, the formation mechanism of the dense fibrin network of dynamic clots under vortex conditions was not deeply investigated. In the future, we will further evaluate the performance of dynamic clot analogs through a mechanical thrombectomy test in animal models.

Conclusion

The clot analogs formed under dynamic vortical flows are more similar to real arterial thrombi in terms of histological and mechanical properties. They can be used as a supplement to the current static clot analogs for the in vitro testing of mechanical thrombectomy devices for treating acute ischemic stroke.

Footnotes

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding: The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This work was supported by the National Key Research and Development Program of China, PLA key project, (grant number 2020YFC0862903, BHJ20J002).

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