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Development of Endovascular Vibrating Polymer Actuator Probe for Mechanical Thrombolysis: A Phantom Study

Choi, Seung Hong*; Yoon, Bye-Ri; Oh, Jin Sun; Han, Moon Hee*; Lee, Jang Yeol; Cho, Hye Rim*; Kim, Moon June; Rhee, Kyehan; Jho, Jae Young

doi: 10.1097/MAT.0b013e31822188ce
Clinical Cardiovascular/Cardiopulmonary Bypass
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In this study, we propose a new method for enhancement of intraarterial thrombolysis using an ionic polymer-metal composite (IPMC) actuator. The purpose of this study was to test the mechanical thrombolysis efficiency of IPMC actuators and evaluate the endovascular vibrating polymer actuator probe for mechanical thrombolysis in a phantom model; 2 × 1 × 15 mm (2 mm in width, 1 mm in thickness, and 15 mm in length) and 0.8 × 0.8 × 10 mm (0.8 mm in width, 0.8 mm in thickness, and 10 mm in length) IPMC actuators were fabricated by stacking five and four Nafion-117 films, respectively. We manufactured the endovascular vibrating polymer actuator probe, for which thrombolysis efficiency was tested in a vascular phantom. The phantom study using 2 × 1 × 15 mm IPMC actuators showed that 5 Hz actuation is the optimal frequency for thrombolysis under both 2 and 3 V, when blood clot was not treated with rtPA, and when exposed to rtPA, IPMC actuators under the optimized condition (3 V, 5 Hz, and 5 min) significantly increased the thrombolysis degree compared with control and other experimental groups (p < 0.05). In addition, 0.8 × 0.8 × 10 mm IPMC actuators also revealed a significantly higher thrombolysis degree under the optimized condition than the control and rtPA only groups (p < 0.05). Finally, the fabricated probe using 0.8 × 0.8 × 10 mm IPMC actuators also incurred higher thrombolysis degree under the optimized condition than the control and rtPA only groups (p < 0.05). A vibrating polymer actuator probe is a feasible device for intravascular thrombolysis, and further study in an animal model is warranted.

From the *Department of Radiology, Seoul National University College of Medicine, Chongno-gu; †School of Chemical and Biological Engineering, Seoul National University; and ‡Department of Mechanical Engineering, Myoungji University, Seoul, Korea.

Submitted for consideration November 2010; accepted for publication in revised form April 2011.

Reprint Requests: Moon Hee Han, MD, Department of Radiology, Seoul National University College of Medicine, 28, Yongon-dong, Chongno-gu, Seoul 110-744, Korea. Email: hanmh@snuh.org.

The first two authors contributed equally to this work.

Stroke remains the third most common cause of death in industrialized nations, after myocardial infarction and cancer, and the single most common reason for permanent disability.1 Intraarterial thrombolysis (IAT) has several theoretic advantages over intravenous (IV) thrombolysis. For instance, with coaxial microcatheter techniques, the occluded intracranial vessel is directly accessible, and the fibrinolytic agent can be infused directly into the thrombus.2 With a smaller dose, complications from systemic fibrinolytic effects, including intracranial hemorrhage, can theoretically be reduced, and IA techniques have led to higher recanalization rates than IV thrombolysis.2,3

Even though the Food and Drug Administration has now approved the endovascular thrombectomy (Merci retriever, Concentric Medical, Mountain View, CA) and thromboaspiration (Penumbra system, Penumbra, Alameda, CA) methods,2 there have been reports of target vessel perforation or dissection, of which rates ranged from 0% to 7% with the MERCI retriever and 0%–5% with the Penumbra system.4 In theory, the mechanical thrombus disruption method still has potential for future application, which may facilitate pharmacological thrombolysis by fragmenting the nonthrombotic components of the clot and increasing the surface area of clot exposed to thrombolytics.5

In this study, we propose a new method for enhancement of IAT using an ionic polymer-metal composite (IPMC) actuator. IPMCs are regarded as one of the most promising smart materials because they are light weight and can make large bending deformations under low driving voltages.6 Thus, they are expected to be applied to soft robotic actuators and artificial muscles, as well as dynamic sensors in the micro-to-macro size range.6

In this study, we tested the mechanical thrombolysis efficiency of IPMC actuators in a phantom model. In addition, we developed the endovascular vibrating polymer actuator probe using IPMC for mechanical thrombolysis, for which feasibility was also evaluated in a vascular phantom model.

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Materials and Methods

This experiment was approved by the animal care committee at Seoul National University Hospital.

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Fabrication of IPMC Actuators

Nafion-117 film from Dupont (Wilmington, DE) with a thickness of 0.18 mm was used as the ionic polymer membrane. IPMCs of 0.8- and 1-mm thickness were manufactured by stacking four and five films, respectively. For hot pressing, Nafion films were placed between the presses (Model M, #9372, Fred S Carver, Inc.; Wabash, IN), heated up, and pressed with medium pressure. The detailed steps followed the previous study.6 To improve the performance of the IPMC actuators, the platinum electroless-plating cycle was repeated twice. Platinum electrodes were created on both surfaces of stacked IPMC by chemical reduction process described in the literature.7

Finally, IPMC actuators of 2 mm in width, 1 mm in thickness, and 15 mm in length (2 × 1 × 15 mm IPMC actuator), and 0.8 mm in width, 0.8 mm in thickness, and 10 mm in length (0.8 × 0.8 × 10 mm IPMC actuator) by stacking five and four films, respectively, were fabricated for this study. The IPMC actuators were designed to have the tip move in one plane. All IPMC actuators were prepared by one author (B.Y.).

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Hemocompatability Test for IPMC Actuators

For in vitro hemocompatibility test of IPMC actuators, extract hemolysis test was performed according to the ISO 10993-4,8 which manufacturers of medical devices need to use as guidance to register their products, lists five categories of testing (thrombosis, coagulation, hematology, platelets, and immunology) in which tests should be done. For the test, whole blood of a New Zealand White Rabbit mixed with citrate (3.8%) was used. The IPMCs of 4 g are extracted with saline of 20 ml for 60 minutes. A portion of the saline extract is removed and added to a standard aliquot of diluted rabbit blood cells, and the two are mixed gently. The percent hemolysis induced by IPMC leachables is determined by spectrophotometric measurement of hemoglobin release. Distilled water and normal saline were used as positive and negative controls, respectively. This test was performed in Korea Testing Laboratory (Seoul, Korea).

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Measurement of IPMC Actuator Force and Displacement

The tip force and displacement of the IPMC actuators were evaluated in the atmosphere. The tip force of the specimen under 3 V direct current (DC) was measured using the load cell with zero displacement condition. Under 3 V alternating current (AC) at 1, 5, and 10 Hz, displacement of the actuator was measured using laser displacement sensor. The actuation motion of IPMCs was also captured by a video camera.

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Clot Preparation and In Vitro Phantom

Venous whole blood was drawn from healthy mongrel dogs (n = 3), collected in Falcon 50 ml conical tubes (BD Biosciences), and cured overnight at 37°C (12–16 hours). The blood of dogs was chosen because of the future in vivo application of the IPMC actuators. Before overnight incubation, hematocrit, hemoglobin, platelet (PT), and activated partial thromboplastin time (aPTT) were measured for each animal and ranged from 45% to 50%, 14.5–16 g/dL, 287–322 × 103/μl, 1–1.10 international normalized ratio (INR), and 25.6–27.5 seconds, respectively.

The in vitro phantom was fabricated by attachment of an acryl tube of 1.5 cm in length and 3.5 mm in inner diameter to a glass plate (76 × 26 mm, 1 mm thickness) using glue. Blood clot of 100 mg was placed in the individual phantom; 50 μl normal saline was then added on the top of the blood clot to prevent evaporation of liquid in the blood clot. Clot size was measured using an electrical balance (AT200, Mettler Toledo; Seoul, South Korea). The clot was gently swiped on gauze before weighing to remove residues. Finally, an IPMC actuator was inserted into the phantom, and the lower portion of the actuator was put into the blood clot. The upper portion of an actuator was connected with a 5 MHz digital synthesized function generator (Potek-9305, Seoul, Korea) (Figure 1). This process was performed by two authors (S.H.C. and H.R.C.).

Figure 1.

Figure 1.

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Optimization Study for Thrombolysis Using 2 × 1 × 15 mm IPMC Actuators

First, the degree of clot disruption under no actuation of IPMC was measured for 5 or 10 minutes as the control groups. The effect of electrical currency in an IPMC actuator to thrombolysis was observed under the condition of 3 V, 20 Hz, and no actuation for 10 minutes. The thrombolysis efficiency of IPMC actuators was measured under input voltages of 1, 2, or 3 V AC, thrombolysis time of 5 or 10 minutes, and actuation frequency of 1, 5, or 10 Hz; experimental groups were labeled as input voltage (V)-thrombolysis time (min)-actuation frequency (Hz) group (e.g., 1V-5 min-5 Hz group). The additive effect of actuators to recombinant tissue plasminogen activator (rtPA) (Actylase, Boeringer, Ingelheim, Germany) was also investigated, and 50 μl of rtPA solution in 0.1 μg/ml concentration (total 5 μg) was added on the top of each blood clot. In each group, experiments were repeated 10 times. Experiments were performed at room temperature. After exposure of the clots to actuation, the clots were gently extracted from phantoms and placed on cotton gauze. After removal of disrupted clots, the clots were then weighed to determine the final size. Thrombolysis (T), expressed as a percentage, was defined as the relative reduction in the mass of the clot:

Where Win is the initial weight of the clot, and Wfi is the final weight of the clot. Finally, for each experimental group thrombolysis, efficiency was recorded as a ratio compared with the control group, which was not exposed to actuation. These processes were performed by two authors (B.Y. and J.S.O.).

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Fabrication of Vibrating Polymer Actuator Probe Using IPMC and Test in a Vascular Phantom

To manufacture the endovascular polymer actuator probe for mechanical thrombolysis, 0.8 × 0.8 × 10 mm IPMC actuators were used, of which thrombolysis efficiency was tested with rtPA and then compared with the control group and clots treated with rtPA only. For this experiment, an in vitro phantom using an acryl tube of 7.5 mm in length and 3.5 mm in inner diameter was used, in which a 50-mg clot was placed.

We manufactured the endovascular vibrating polymer actuator probe using IPMC, for which thrombolysis efficiency was tested in a vascular phantom. The endovascular vibrating polymer actuator probe was fabricated as follows: a) copper wires (0.22 mm in a diameter and 50 cm in a length) were attached to the 0.8 × 0.8 × 10 mm IPMC actuator by lead soldering, b) the soldered portion of an IPMC actuator was fixed by silicon glue at one end of a Teflon tube (Dongsung Science, Seoul, Korea) of 1 mm in inner diameter, 1.5 mm in outer diameter, and 40 cm in length, and the other end of the Teflon tube was an outlet of copper wires (Figure 2).

Figure 2.

Figure 2.

The vascular phantom was modified from the previously reported experiment (Figure 3).9 The dynamic flow model using the vascular phantom aimed at duplicating some of the physioanatomical conditions related to a single artery embolic occlusion in humans. The dynamic flow was made by normal saline. Individual blood clots weighing 100 mg were placed within a 1-cm-long acryl tube of 3.5 mm in inner diameter, and distal end of the clot was fixed by cotton gauze with 0.5-mm-sized pores. The acryl tubes with blood clot were connected to the vascular phantom system using silicon tubes before experiments and were disconnected to measure residual clot. A fluid pressure gradient was formed using a gravity dependent flow system simulating a physiological volume rate of 2.1 ml/s such as that present in larger human arteries. Different treatments such as no actuation, rtPA only, and actuation with rtPA (1 mg in 1 L normal saline) were introduced into the flow system. In each experiment, tests were performed for 5 minutes and repeated 10 times. Dissolution of the clot among the different treatment groups before and after treatment was measured for determination of thrombolysis efficiency (T).

Figure 3.

Figure 3.

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Statistical Analysis

For all statistical analyses, a two-tailed p value of less than 0.05 was considered to indicate a statistically significant difference. Statistical analyses were performed using commercially available softwares (MedCalc, version 11.1.1.0, MedCalc software, Mariakerke, Belgium). The data were presented as mean ± standard deviation in terms of thrombolysis efficiency. Repeated measurements analysis of variance (ANOVA) with post hoc comparisons was used for multiple comparisons. In terms of thrombolytic difference between in vivo phantom experimental groups and control groups or groups treated with rtPA only, the unpaired Student's test was used.

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Results

Hemocompatability Test for IPMC Actuators

The percentage hemolysis of eluate from IPMCs was 0% and confirmed as nonhemolytic.

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Measurement of IPMC Actuator Force and Displacement

Under 3 V DC, 2 × 1 × 15 mm and 0.8 × 0.8 × 10 mm IPMC actuators showed 1.38 and 1.13 g force (gf) for 6 seconds, respectively. Under 3 V AC, 2 × 1 × 15 mm IPMC actuators had displacements of 0.95, 0.35, and 0.2 mm at 1, 5, and 10 Hz (Figure 4A and Video, Supplemental Digital Content 1, http://links.lww.com/ASAIO/A6), respectively, and displacements of 0.8 × 0.8 × 10 mm IPMC actuators were 0.90, 0.35, and 0.14 mm at 1, 5, and 10 Hz, respectively (Figure 4B and Video, Supplemental Digital Content 2, http://links.lww.com/ASAIO/A7).

Figure 4.

Figure 4.

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Optimization Study for Thrombolysis Using 2 × 1 × 15 mm IPMC Actuators

Degrees of thrombolysis in control groups for 5 minutes and 10 minutes were 31% ± 6% (standard deviation) and 30% ± 5%, respectively (p = 0.5272). In addition, the currency had no thrombolytic effect under the condition of 3 V and 20 Hz for 10 minutes compared with 10 minutes control group (32% ± 4%, p = 0.2080).

Table 1 summarizes the thrombolysis efficiencies of IPMC actuators under voltage of 1, 2, and 3 V, thrombolysis time of 5 and 10 minutes, and actuation frequency of 1, 5, and 10 Hz. IPMC actuators have no additional thrombolytic effect under 1 V; however, 5 Hz actuation at both 2 and 3 V showed significantly higher thrombolysis compared with the control groups (p < 0.05). There was no significant difference (p = 0.6653) among 2 V-5 min-5 Hz, 2 V-10 min-5 Hz, 3 V-5 min-5 Hz, and 3 V-10 min-5 Hz groups, even though 3 V-5 min-5 Hz group showed the highest thrombolysis efficiency (138% ± 16%) among the groups (Figure 5A).

Table 1

Table 1

Figure 5.

Figure 5.

Clots treated only with rtPA for 5 and 10 minutes incurred 132% ± 14% (p = 0.0009) and 127% ± 29% (p = 0.0175) degrees of thrombolysis, respectively, which were compared with the control groups. All experimental groups treated with IPMC actuators plus rtPA showed significantly increased efficiency of thrombolysis than control groups (Table 2). However, significant differences were found only in 2 V-5 min-5 Hz, 2 V-5 min-10 Hz, 2 V-10 min-5 Hz, 3 V-5 min-1 Hz, 3 V-5 min-5 Hz, and 3 V-10 min-5 Hz groups with rtPA comparing with clots treated with rtPA only (p < 0.05), where there were significant differences among the groups (p = 0.0019), and 3 V-5 min-5 Hz group with rtPA showed a the significantly higher degree of thrombolysis than other groups (Figure 5B).

Table 2

Table 2

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Fabrication of Vibrating Polymer Actuator Probe Using IPMC and Test in a Vascular Phantom

According to the results described earlier, the optimal condition of IPMC actuators for thrombolysis was considered as follows: input voltage of 3 V, thrombolysis time of 5 minutes, and actuation frequency of 5 Hz. Thus, in vitro experiments with 0.8 × 0.8 × 10 mm IPMC actuators were performed under those conditions and compared with the control group for the 50 μg clot and clots treated with rtPA, which resulted in significant difference between groups (p < 0.0001) and IPMC actuators significantly increased the degree of thrombolysis (48% ± 5%) compared with the control (25% ± 5%, p < 0.001) and rtPA only (31% ± 5%, p < 0.001) groups (Figure 6A).

Figure 6.

Figure 6.

Vibrating polymer actuator probes also showed higher efficiency of thrombolysis (55% ± 10%) under the optimized condition of input voltage of 3 V, thrombolysis time of 5 minutes, and actuation frequency of 5 Hz with rtPA than control (32% ± 4%, p < 0.001) and rtPA only (43% ± 9%, p < 0.05) groups (Figure 6B).

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Discussion

We fabricated a new device using an IPMC actuator for mechanical thrombolysis; the IPMC is an electrically activated polymer actuator. The actuator can be made using a Nafion membrane after chemical deposition of platinum as the source of electrodes.10–12 When an electric field is prescribed through the thickness of an IPMC, cations inside the membrane carry solvent molecules toward the cathode, and the movement creates bending providing a source of actuation force.13,14 Even though IPMCs can be used to make an embedded system for providing great advantages for the integration of sensors and actuators, IPMCs generate low actuating force, which limits its application to actuators. In this study, thus, we used the hot-pressing method to fabricate the stacked IPMC actuators, by which the tip force of the actuators could be increased as in the previous report.6 Under 3 V DC, the tip forces of 2 × 1 × 15 mm and 0.8 × 0.8 × 10 mm IPMC actuators reached up to 1.38 and 1.13 gf, respectively, and finally, we fabricated vibrating polymer actuator probes of less than human middle cerebral artery (MCA) diameter.15 Our hypothesis was that the actuation force of the IPMC was enough to increase the degree of thrombolysis by blood clot disruption compared with the control groups.

Thus, the principal rationale for this study was to investigate whether IPMC actuators can be useful adjuvants to currently existing rtPA-induced thrombolysis and further enhance clot lysis results. The phantom study using 2 × 1 × 15 mm IPMC actuators showed that 5 Hz actuation is the optimal frequency for thrombolysis under both 2 and 3 V, when the blood clot was not treated with rtPA, and in terms of blood clots exposed to rtPA, IPMC actuators under the optimized condition (input voltage of 3 V, thrombolysis time of 5 minutes, and actuation frequency of 5 Hz) significantly increased the thrombolysis degree compared with the control and other experimental groups (p < 0.05). In addition, the 0.8 × 0.8 × 10 mm IPMC actuators also revealed a significantly higher degree of thrombolysis under the optimized condition than the control and rtPA only groups (p < 0.05). Finally, the fabricated vibrating polymer actuator probe using the 0.8 × 0.8 × 10 mm IPMC actuators also incurred higher thrombolysis degree under the optimized condition than the control and rtPA only groups (p < 0.05).

For mechanical thrombolysis, the optimal actuation frequency was 5 Hz compared with 1 and 10 Hz frequency. Even though higher frequency actuation seems to be more beneficial for mechanical clot disruption and increase of rtPA penetration to blood clots than that of lower frequency, the tip displacements of IPMC actuators at 10-Hz frequency were 0.20 and 0.14 mm in 2 × 1 × 15 mm and 0.8 × 0.8 × 10 mm IPMC actuators, respectively, which was not enough to increase mechanical thrombolysis. In terms of input voltage of IPMCs, actuation under 3 V increased the thrombolysis degree more than that under 1 and 2 V, which might be due to greater displacement and tip force of IPMC actuators than with lower input voltage. The previous study also reported that the displacement and tip force of IPMCs increase according to the rise in input voltage.6

Of particular interest, actuation for 5 minutes showed a higher degree of thrombolysis than that for 10 minutes. In this study, in vitro phantom studies were performed in the air. Conventional water-based IPMCs used in our study tend to significantly lose their solvent content when operated by higher than 1.22 input voltages in the air.16 Thus, actuation for more than 5 minutes seems to have no additional thrombolysis effect in the air, and the experimental blood is thought to reclot after 5 minutes, because of the absence of actuation. However, under water-rich in vivo environments, we believe that IPMC actuators can be used for longer than 5 minutes.

This study has several drawbacks other than the lack of an in vivo animal study. First, we developed the actuating model of IPMC, of which the main mechanism for thrombolysis is mechanical disruption; however, we did not evaluate the characteristics of the disrupted clot, which has a potential for secondary occlusion in small branches distal to treated vessels. Second, another aspect to be considered is the variable consistency of occlusive clots.17 The effectiveness of the recanalization method should be equivalent for “red” and “white” thrombi as well as for debris coming from a proximal atherosclerotic plaque. In this study, we investigated the thrombolysis effect for red thrombi, and further study of various thrombi is warranted. The other promising aspect of the IPMC is the flexibility, which can provide a myriad of motions such as clot capture or retrieval. Third, we applied up to 3 V AC to vibrate the IPMC actuators, which have the possibility of delivery of AC current to vessel lumen in the future in vivo application. However, voltages below 15 V AC are known to be relatively safe for wet contact areas, and these levels come from established standards and take into consideration the wide range of body impedance values and the various effects of current flows through the body.18

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Conclusion

In conclusion, we believe that the IPMC actuator is a feasible device for use in thrombolysis, as it is simple, allows rapid recanalization, and works with little or no interference with the coagulation system. In addition, we expect the IPMC actuators to be applied to various thrombolysis treatments for disruption of large clots such as thrombosed dialysis grafts and fistulas, because the IPMC actuators can be increased in size and actuation force.

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Acknowledgment

Supported by a grant of the Korea Healthcare technology R&D Project, Ministry for Health, Welfare & Family Affairs, Republic of Korea (A090406). The authors thank Yoon Kyeong Choi for the illustrations.

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