Hemostatic Swabs Containing Polydopamine-like ... - ACS Publications

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Hemostatic Swabs Containing Polydopamine-like Catecholamine Chitosan-catechol for Normal and Coagulopathic Animal Models Mikyung Shin, Ji Hyun Ryu, Kyu ri Kim, Min Jun Kim, Seongyeon Jo, Moon Sue Lee, Dong Yun Lee, and Haeshin Lee ACS Biomater. Sci. Eng., Just Accepted Manuscript • DOI: 10.1021/acsbiomaterials.8b00451 • Publication Date (Web): 17 May 2018 Downloaded from http://pubs.acs.org on May 17, 2018

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ACS Biomaterials Science & Engineering

Hemostatic Swabs Containing Polydopamine-like Catecholamine Chitosan-catechol for Normal and Coagulopathic Animal Models Mikyung Shin,‡,1 Ji Hyun Ryu,‡,2 Kyuri Kim,3 Min Jun Kim,4 Seongyeon Jo,5 Moon Sue Lee,5 Dong Yun Lee,4 and Haeshin Lee*1,5 1

Department of Chemistry, Korea Advanced Institute of Science and Technology (KAIST),

University Rd. 291, Daejeon 34141, South Korea. 2

Department of Carbon Convergence Engineering, Wonkwang Univeristy, Iksan, Jeonbuk,

54538, South Korea. 3

Graduate School of Nanoscience and Technology, Korea Advanced Institute of Science and

Technology (KAIST), 291 University Rd., Daejeon 34141, South Korea. 4

Department of Bioengineering, College of Engineering, and BK21 PLUS Future

Biopharmaceutical Human Resources Training and Research Team Institute of Nano Science & Technology (INST), Hanyang University 222 Wangsimni-ro, Seong Dong-gu, Seoul 04763, South Korea. 5

InnoTherapy Inc. 97 Uisadang-daero, Yeongdeungpo-gu, Seoul 07327, South Korea.

*Correspondence to: [email protected].

ACS Paragon Plus Environment

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KEYWORDS. swabs, catecholamine polymers, hemostasis, coagulopathy

ABSTRACT: All animal experiments for evaluating drug efficacy or developing medical devices are unavoidably accompanied by bleedings that result in unreliable outcomes with large variations between individuals. Herein, we developed hemostatic swabs prepared by a musselinspired catecholamine polymer called chitosan-catechol, which was inspired by the chemical composition of the well-known material-independent coating material of polydopamine. The hemostatic ability of the swabs resulted from the formation of self-sealing membranes by rapid intermolecular interactions between whole blood proteins and the applied chitosan-catechol. The blood protein/chitosan-catechol composite sealing membrane resulted in dramatic decreases in bleedings for both normal and coagulopathic models, such as diabetes.

Nearly all animal experiments lead to bleedings due to syringe injections for administering drugs or surgical procedures. Examples include in vivo experiments for evaluating drug efficacy, developing treatment procedures for a certain disease or medical devices, and so on. For all such experiments, bleedings from animals are unavoidable, which critically affect the health status of post-operative subject animals. Importantly, most small mice and rats acting as a particular disease model often suffer from incessant bleedings such as delayed hemostasis resulting from impaired functions in platelets and/or thrombin related pathways.1-3 Uncontrolled massive bleedings or delayed hemostasis often results in i) slow health recovery after surgical procedures or drug administration, ii) failure to establish particular animal models or iii) significant experimental errors.


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The most significant problem with failure to control bleeding is for drug administration via blood vessels. Precise control of the amount of injected drugs is very important to determine the relationship between the therapeutic effect and the dosage dependency. However, a few hundred µL of blood loss due to disease-related impaired hemostasis often exceed 10 % or more of the total blood volume of mice. This unavoidably loses a certain portion of the administered drug, resulting in changes in the drug levels in blood. In the worst-case scenario, the subject animals are dead due to bleeding or its related complications. In practice, however, researchers have a limited toolkit to manage uncontrolled bleedings in animal models. Widespread materials such as gauzes, cotton balls or other biomaterials (i.e., polysaccharides)4 have routinely been used for hemostasis. Moreover, forceps and electrosurgery devices named ‘bovies’5 are the only available tools for bleeding control. These devices are often not effective in managing bleedings and thus cause further damage to tissues or have adverse effects on healing. Polydopamine, a well-known adhesive catecholamine compound, has been used to functionalize virtually all solid substrates,6 including a superhydrophobic surface,7 porous materials and membranes,8,9 fibrous scaffolds/hydrogels,10-12 and even air/water interfaces.13,14 The unprecedented, material-independent surface chemistry achieved using polydopamine originates from mussel adhesive proteins,15,16 in which catechols from 3,4dihydroxyphenylalnine and amine moieties from lysine are abundant. The chemical conjugation of a catechol-containing small molecule such as hydrocaffeic acid onto the amine-rich natural polymer chitosan, which is useful an adhesive catecholamine, enabled the development of a polydopamine-like material.17-19 Similar to marine mussels using their water-resistant adhesives to strongly attach their bodies to surfaces,20 the corresponding chitosan-catechol conjugates (CHI-C) have shown body fluid-resistant adhesive properties as well as hemostatic abilities. In


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particular, the immediate, self-sealing properties of one type of mussel-inspired hemostatic materials allow complete prevention of bleeding from punctured blood vessels, even after the removal of syringe needles.21 This invention provides an opportunity to develop a simple hemostatic device to manage uncontrolled bleedings from animals used in various disease models. Herein, we developed a hemostatic swab that considerably reduces blood loss from animal disease models. The hemostatic swab is simply prepared by dip coating with CHI-C, which includes all the chemical functional groups of mussel-inspired materials (i.e., the amine and catechol groups of polydopamine). Unlike conventional cotton-based swabs, which cause hemostasis passively by blood adsorption and compression, the CHI-C-coated swabs exhibit active hemostasis via formation of a self-sealing membrane through rapid complexation with blood proteins. This physico-chemical response of the CHI-C-coated swabs in the in vivo bloodrich, wet environment showed excellent hemostasis, even for the severely hemostatically impaired diabetic rat model, which bleeds nearly 90 % of the lethal-level bleeding volume (equivalent to ~ 10 % of total blood volume) when using typical cotton-ball swabs. Our study indicates that the self-sealing membrane of polydopamine-like hemostatic materials (i.e., CHI-C) and blood proteins can result in a prompt decrease in excessive bleedings and can potentially be utilized in a variety of both normal and coagulopathic mouse/rat models with uncontrolled bleeding in surgical or syringe injection situations as well as further clinical settings for humans such as hemophilia and diabetic patients. For preparation of the hemostatic swab, CHI-C was synthesized by an 1-ethyl-3-(3dimethylaminopropyl)carbodiimide (EDC) coupling reaction with 3,4-dihydroxyhydrocinnamic acid as previously reported.19,21 The degree of catechol conjugation (DOCcat) was determined


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using the absorbance of CHI-C at 280 nm (A280 = 0.90) by ultraviolet/visible (UV-vis) spectroscopy (Figure 1a). 3,4-Dihydroxyhydrocinnamic acid was used as a standard molecule. The tethered catechol contents in CHI-C were ~ 6.2 % of the amine groups in the chitosan backbone. Furthermore, the DOCcat was confirmed by the ratio of the relative integral value for the catechol protons (3H; 6.8 ppm) to those for all protons in the chitosan backbone (10H) detected by proton nuclear magnetic resonance (1H-NMR) spectroscopy (Figure 1b). The results show that ~10.6 % of the amine groups were conjugated to the 3,4-dihydroxyhydrocinnamic acid groups. The reaction solution was dialyzed and subsequently lyophilized, which resulted in a white sponge-like solid (Figure 1c, photo). The CHI-C sponge was dissolved in distilled water at a concentration of 1 wt% (i.e., 10 mg/mL), and commercial cotton-ball swabs were immersed in the resulting solution (200 µL) for 1 hour. During the coating procedure, the initial volume of chitosan solution (200 µL) was decreased down to 50 ± 14 µL, indicating that the absorption amount onto the swabs was 1.5 ± 0.1 mg considering the CHI-C concentration (10 mg/mL). After that, the CHI-C/cotton swabs were lyophilized. The overall appearance of the CHI-Ccoated swabs was almost the same as that before the CHI-C functionalization (Figure 1c). Importantly, the sizes and shapes of the coated swabs can easily be controlled by the shape and size of molds in which the unfunctionalized swabs were soaked (final photo, Figure 1c). Figure 1d shows the morphology of the CHI-C layers coated on the existing surface of cotton (white arrows), as imaged by scanning electron microscopy (SEM). The lyophilized thin CHI-C adlayer was clearly detected. In addition to the surface exposed CHI-C coating layer, we expected that CHI-C exists in inner pores as well because the high water solubility of CHI-C (~60 mg/mL)22 facilitates its facile penetration into the porous cotton microfibrils.


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The hemostatic capability of the CHI-C/cotton swabs was evaluated using a liver hemorrhaging model (Figure 2). In general, the liver is blood vessel-rich organ. Thus, the puncture using a needle (21 G) on a mouse or a punch (the diameter of 6 mm) to a rat liver caused severe bleedings. Figure 2a shows an illustration of the experimental design for a mouse model. The needle injection (21 G) resulted in bleeding from the mouse liver. Then, the blood loss was measured by the weight changes in either a CHI-C/cotton swab or a bare one. In general, 10 % blood loss of total blood volume (TBV) is deadly for mouse individuals, which is approximately 200 µL for a mouse (25 g) and 1.5 mL for a rat (250 g).23 Thus, all blood loss (%) was calculated at a ratio of measured blood loss to 10 % TBV (Figure 2b and 2c). For all hemorrhaging models, the CHI-C/cotton swabs exhibited an excellent hemostatic effect compared to that observed using the unmodified commercial swabs, resulting in mitigation of the blood loss by the CHI-C-coated swabs. In a mouse model, the use of commercial cotton swabs showed complete hemostasis after 60 µL bleeding, which corresponds to 29.7 ± 3.7 % blood loss to the lethal level of 10 % TBV (Figure 2b, right bar). In contrast, the blood loss dramatically decreased down to 8.8 ± 0.3 % when using CHI-coated swabs (Figure 2b, left bar). The aforementioned hemostatic results were also consistent in a rat model (Figure 2c). The blood loss was only 3.0 ± 1.0 % for CHI-C-coated swabs (left bar) but increased to 12.7 ± 4.1 % for the bare swabs (right bar). In Figure 2c, the inset photos represent CHI-coated (left) or unfunctionalized swabs (right) after contact with the liver bleeding sites. Comparative SEM morphological studies between the CHI-C/cotton swabs and commercial ones suggest mechanisms for the observed effective hemostasis. We found that a number of microscale aggregates were formed and adhered onto the CHI-C/cotton composite microfibrils after blood contact (Figure 2d). The aggregates were visibly perceptible (red arrows, SEM image), and when


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they were imaged by SEM, they were thoroughly spread over the entire surface. However, for the bare swabs, no aggregates were observed; instead, they showed simple absorption of blood without any notable characteristics (Figure 2e). We hypothesized that CHI-C coated/cotton composite layers of the swabs spontaneously forms a complex with a variety of blood components, such as serum proteins and other blood cells (i.e., erythrocytes, white blood cells, or platelets), which is the primary mechanism of hemostasis. Our previous study clearly showed that the insoluble thin membrane-like aggregates were generated by the intermolecular interaction between CHI-C and serum proteins, decreasing total amount of blood serum proteins.24 Previously, we demonstrated that the ability of CHI-C to induce hemostasis of CHI-C originated from rapid and physical complexation with virtually all blood components.21 The applicability of the CHI-C-coated composite swabs extends even to coagulopathic animal bleeding models. To demonstrate hemostasis in the case of coagulopathic bleedings, we chose diabetic rat models. In practice, liver hemorrhage in normal rat models resulted in 12.7 ± 4.1 % blood loss at most (Figure 3a, black bar). In contrast, liver hemorrhage in diabetic rat models caused a lethal level of bleeding, i.e., up to 90.6 ± 31.0 % blood loss (red bar). Thus, hemostasis of a diabetic liver can be more important than that of normal bleeding. Figure 3b shows the amount of blood loss (%) for diabetic liver bleeding after utilizing the CHI-C-coated swabs or commercial cotton swabs. As expected, the swabs functionalized with CHI-C effectively decreased the overall blood loss down to 21.0 ± 1.5 % (blue bar) compared to 90.6 ± 31.0 % when using the commercial cotton swabs (cyan bar). We further demonstrated the hemostatic capability in another coagulopathy setting, in which we introduced an incision to a femoral artery to cause hemorrhage. The CHI-C-coated swabs decreased the blood loss to 4.3 ± 1.3 % (blue bar) compared 18.6 ± 12.2 % for the bare swabs (cyan bar). These results indicate the significant


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hemostatic effect of the CHI-C-coated swabs, demonstrating that the CHI-C-coated swabs might be useful as hemostatic formulations for coagulopathic animals. As mentioned above, the CHIC-coated layers on the swab surface formed microaggregates with the blood components (Figure 2d). Thus, the CHI-C/blood aggregates can also be generated and adhered onto the tissue incision sites, thereby functioning as a physical barrier against the bleeding. Histological analysis was performed to evaluate the CHI-C/blood component adhered onto the incision/defect sites (Figure 3d). As a result, with Safranin-O/Fast Green and iron-hematoxylin staining,25 CHI-C stained with a brilliant green color was observed on the defect sites of both the femoral artery and liver (red asterisk, right panel, Figure 3d). This result indicates that CHI-C has generated a physical barrier on the interface between the CHI-C-coated swabs and the bleeding sites. The physical barrier induced by CHI-C has a hemostatic effect regardless of the biochemical coagulation pathway. Thus, the hemostatic swabs developed in this report are effective in preventing blood loss for both normal and impaired bleedings. Furthermore, a simple ease of use for the hemostatic swabs might be potentially applicable for clinical settings to decrease uncontrollable bleedings for warfarin or heparin treated surgical procedures. In conclusion, we developed a hemostatic CHI-C-coated cotton swab that effectively prevents bleedings in both normal and coagulopathic animal models. CHI-C is a hemostatic polymer inspired by the mechanism of the wet-resistant adhesive behavior of mussels. By simple dip coating of CHI-C onto a conventional cotton swabs, exterior/internal CHI-C absorbed layers were observed, which resulted in complexation with various blood components upon blood contact at the hemorrhaging site. In particular, the hemostatic swab is very effective for diabetic bleeding models, as it decreased the blood loss from a lethal level (10% TBV) down to a safe level . Considering the easy preparation of the hemostatic swab, our findings on the self-


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mitigating blood loss property of catechol-conjugated polymers could be very useful for future developments of other hemostatic formulations.


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Figure 1. Preparation of mussel-inspired adhesive CHI-C/cotton composite hemostatic swabs. (a) UV-vis and (b) 1H-NMR spectra of catechol-conjugated chitosan (CHI-C). (c) Experimental description for preparing of the CHI/cotton composite swab: CHI-C sponge generation by lyophilization, dissolution of the CHI-C sponge, immersion of a commercial cotton swab, and additional lyophilization. The right photo shows functionalized swabs with a variety of size and shapes. (d) SEM image of the morphology of the CHI-C-coated layer on the swab.


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Figure 2. Hemostatic capabilities of the CHI-C-coated swabs for normal liver hemorrhaging models. (a) Experimental design for evaluating the hemostatic effect of the CHI-C-coated or the commercial cotton swab after mouse liver puncture using 21 G needles. Quantitative analysis of blood loss (%) from the punctured (b) mouse or (c) rat liver after gentle compression of the CHIC-coated (left gray bar) or commercial cotton swabs (right gray bar). The inset photos in Figure 2C exhibited the blood-absorbed CHI-C-coated (1st photo) and cotton swabs (2nd one) Data are expressed as the mean ± SD (n = 3). An unpaired t-test, *P < 0.05 and **P < 0.01. Comparison of the surface morphology (SEM images) of (d) the CHI-C-coated swabs to (e) the cotton swabs after in vivo blood contact. The photos show the lyophilized samples.


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Figure 3. Hemostatic capabilities of the CHI-C-coated swabs for coagulopathic hemorrhaging of the liver in diabetic rat models. (a) Comparison of blood loss (%) between a normal liver and a diabetic one. The red box represents the ranges of a lethal bleeding level (i.e., 10 % of total blood volume (TBV)). Quantitative analysis of blood loss for diabetic (b) liver and (c) femoral artery bleedings. (d) Histology of the incision sites, femoral artery (top column) or liver (bottom column), after compression of the commercial cotton swabs (left row) or CHIC-coated ones (right row). Statistical analysis using an unpaired t-test, *P < 0.05 and **P < 0.01, and F test to compare variances, #P < 0.05.


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ASSOCIATED CONTENT

AUTHOR INFORMATION Corresponding Author *E-mail: [email protected]

Author Contributions The manuscript was written through contributions of all authors. All authors have given approval to the final version of the manuscript. ‡These authors contributed equally.

ACKNOWLEDGMENT This study was supported by a grant from the National R&D Program for Cancer Control, Ministry for Health and Welfare, Republic of Korea (1631060 (H. L.)) and the National Research Foundation of Republic of Korea (NRF) Grant funded by the Ministry of Science, ICT & Future Planning for convergent research: Development program for convergence R&D over traditional culture and current technology (NRF-2016M3C1B5906485 (H. L.)), Basic Science Research Program funded by the Ministry of Education (NRF-2016R1A6A3A11933589 (M. S.)), and Creative Materials Discovery Program (NRF-2017M3D1A1039289 (D. Y. L.)). This research was also financially supported by the Ministry of SMEs and Startups (MSS), Republic of Korea, under the “Regional Specialized Industry Development Program (R&D, R0006544 (M. S.))” supervised by the Korea Institute for Advancement of Technology (KIAT).


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Supporting Information. The supporting information is available free of charge. Experimental section (PDF)

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For Table of Contents Use Only

Hemostatic Swabs Containing Polydopamine-like Catecholamine Chitosan-catechol for Normal and Coagulopathic Animal Models Mikyung Shin,‡,1 Ji Hyun Ryu,‡,2 Kyuri Kim,3 Min Jun Kim,4 Seongyeon Jo,5 Moon Sue Lee,5 Dong Yun Lee,4 and Haeshin Lee*1,5


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Hemostatic Swabs Containing Polydopamine-like ... - ACS Publications

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