Design of an electrospun polyvinyl alcohol (PVA)/chitosan/curcumin based- wound dressing containing titania nanotubes (TNT)

doi:10.21203/rs.3.rs-4081534/v1

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Design of an electrospun polyvinyl alcohol (PVA)/chitosan/curcumin based- wound dressing containing titania nanotubes (TNT)

https://doi.org/10.21203/rs.3.rs-4081534/v1

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Burn wounds are one of the most significant causes of morbidity around the world. Burn wound healing and skin tissue regeneration still have serious and considerable challenges. This study applies the electrospinning method to make PVA-chitosan-curcumin wound dressing containing titania nanotubes with 0.5, 1.5, and 3 wt%, following that their physicochemical properties were investigated using scanning electron microscopy (SEM), transmission electron microscopy (TEM), Fourier-transform infrared spectroscopy (FTIR), and mechanical test. Then, the in vivo effectiveness of the designed wound dressing in the wound healing process in the Wistar rat model was evaluated for two weeks. The most important result of applying the TiO₂ nanotube was the improved regeneration of damaged tissues with an appreciable decline in scar formation, skin color anomalies, and accelerated wound healing and contraction.

Electrospinning

Titania nanotube

wound dressing

Skin regeneration

Skin is a soft tissue that protects the whole body and internal tissues against heat, electrical balance, and physical damage [1]. Skin dressings prevent the entry of pathogens and microbes into the damaged area and the loss of body water, leading to the acceleration of wound closure and reduction of scar formation [2]. The wound healing process is complex, and in case of severe tissue damage, the tissue restoration may not lead to the return of the typical tissue structure, the connective tissue may be damaged, and a scar or wound may be formed [3]. The wound-healing process includes stages of hemostasis, inflammation, and granulation. Today, dressings of biological origin influence wound healing and scar reduction [4–7]. Also, extensive studies on topical ointments or new dressings are constantly being done. So far, various dressings have been made to treat and repair wounds. Still, most have problems such as incompatibility in the biological environment, lack of antibacterial properties, and proper degradability [8, 9]. A suitable wound dressing should have the following characteristics [7, 10–12]: Appropriate speed of water evaporation to prevent infection and bacterial accumulation in the wound, appropriate permeability, and the ability to absorb fluids and nutrients to prevent the growth of bacteria in the wound, creating a barrier to prevent the penetration of microorganisms and infection to the wound site, antibacterial properties to prevent the growth of microbes in the dressing area. Restoration or replacement of damaged tissue has always been one of the main concerns of biological scientists. Today, tissue engineering is an essential tool for scientists in producing replacement tissues and prostheses for repairing or replacing damaged tissue [13]. In this regard, electrospinning as a technology for producing nanofibers has attracted scientists' attention for the sake of the fabrication of a three-dimensional and porous nanoscale scaffold which is very similar to the extracellular matrix of natural tissue. Nanofibers, having unique properties, can create a suitable bed for dressing damaged tissues. In addition to this feature, nanofibers structures are very suitable for adhesion and cell proliferation [14–16].

Chitosan (Cs) is a semi-crystalline polysaccharide obtained by the deacetylation of chitin. This biomaterial has been widely used in medical and pharmaceutical fields due to its favorable properties. Dressings containing chitosan have desirable properties such as homeostasis, antibacterial, biocompatibility, and biodegradability [17]. It should be noted that chitosan hydrogel in dressings can increase the speed of healing, create a moist environment, and better protect the wound [18]. Also, the glucose amine in chitosan causes cytokine production, increases the secretion of macrophages, and stimulates the growth and proliferation of fibroblasts and collagen. Finally, the factors above accelerate wound healing.

Polyvinyl alcohol (PVA) comprises vinyl alcohol-co-vinyl acetate copolymers and is an inert synthetic polymer, bio-adhesive, biocompatible, and biodegradable [19]. It possesses outstanding properties such as mechanical resistance, solubility in water, gas permeability, and efficient electrospinning. Polymeric nanofibers materials have attracted much attention from the scientific community, especially for medical applications [20]. However, their mechanical properties limit their use in medical applications such as tissue engineering.

Curcumin is a yellow pigment extracted from the rhizome of turmeric root, which is widely used to treat various inflammatory diseases in traditional medicine. The role of curcumin in healing wounds and stimulating the secretion of growth factor (TGF-11) is a very influential factor in the trend of wound healing. Also, in the last two decades, extensive studies have been conducted on the topical antioxidant properties of curcumin for the treatment of wounds, and the results indicate that curcumin reduces oxidative stress in the wound site and ultimately heals the wound. However, despite the tremendous therapeutic potential of curcumin due to its low bioavailability, instability of curcumin in neutral and alkaline conditions, and low solubility in water and body fluids, it has yet to be used for many medical applications. Curcumin is classified as a biological drug in class four molecular drugs 2BCS. [18]

Titanium dioxide (TiO₂) is a metal oxide semiconductor material involved in various medical applications such as drug delivery, biosensors, and tissue engineering. It has good corrosion resistance and the high performance of functional groups on its surface which is one of its other features [21]. TiO₂ nanotubes (NTs) have a large surface-to-volume ratio and a high strength-to-weight ratio, which helps to increase the mechanical properties and bioactivity if combined [22, 23]. Polymer matrix composite and, specifically TiO₂ nanotubes in the form of powder have attracted the attention of many researchers because they can be obtained with controllable dimensions through hydrothermal technique [24]. This project applies the electrospinning method in making PVA-chitosan dressings with an antioxidant trait of curcumin, containing titanium nanotubes to accelerate wound healing and tissue restoration. The null hypothesis was the lack of effect of adding nanotubes on the properties of the PVA-chitosan-curcumin dressings, such as physical, mechanical, and biological as a burn wound dressing.

The materials used in this research (polyvinyl alcohol with molecular weight 72KDa, chitosan (low molecular weight), curcumin, acetic acid) were purchased from Merck company. Titanium nanotube (TNT) was produced by hydrothermal method, as reported by Eslami et al. [23]. Briefly, the TiO₂ nanoparticles (Degussa, 25nm) in a Teflon-lined autoclave were treated with 10N NaOH solution at 150°C for 2 days. The obtained precipitates were washed with both deionized water and 1M HCl aqueous solution until the pH value of the rinsing solution was less than 7. Then, they were dried at 80°C for 3 hours, and finally, nanotubes were calcined at 350°C to purify.

Chitosan is first added to acetic acid (98%, v/v) to prepare the polymer solution to achieve a final concentration of 30% (w/v). The above solution is stirred for 12 hours at room temperature. Then, to prepare the solution of polyvinyl alcohol, PVA is added to deionized water to obtain a solution with a concentration of 10% (w/v). The above solution is stirred at 80°C for 4 hours. After preparing both PVA and chitosan solutions, they are combined in a ratio of 1 to 1 to prepare the PC solution. The PC solution is stirred for 30 minutes at room temperature for a precise and uniform solution. Then curcumin is added to the PC solution in proportions of 0.5% (w/v). The solution containing curcumin is stirred for 1 hour at room temperature. Then TNT is added to each prepared solution containing curcumin in proportions of 0.5, 1.5, and 3% (w/v) and stirred for 2 hours at room temperature to obtain a homogeneous solution. Various groups of polymer solutions prepared for electrospinning are shown in Table 1. After preparing the polymer solution according to Table 1, each group’s solution is transferred to the electrospinning device. The settings applied to the device include an applied voltage of 20 kV, with a flow rate of 0.3 milliliters per hour. Also, the distance to the collector was 15 cm. Electrospinning was conducted under the same ambient temperature and 40% humidity conditions. After electrospinning, all fibers are exposed to UV radiation for 30 minutes to sterilize.

Table 1

Different groups of polymer solutions prepared for electrospinning
Groups Materials	Group 1	Group 2	Group 3	Group 4	Group 5
Chitosan-PVA solution ratio (w/v)	1:1	1:1	1:1	1:1	1:1
Curcumin (%w/v)	-	0.5	0.5	0.5	0.5
TNT (%w/v)	-	-	0.5	1.5	3

At first, the synthesized TiO₂ nanotube powder was characterized by using SEM and TEM microscopes to show tubular structure. Then, the following instruments were used to characterize the electrospun fibers.

Some information obtained from Fourier transform spectroscopy (FTIR) includes quantitative and qualitative identification of organic compounds containing nanoparticles and determining the type of functional group and bonds in its molecules. For this purpose, the samples were powdered, and spectrometry was performed using an FTIR 410 device, OCSAJ, in the wave number range of 400–4000 cm^− 1.

To check the size of the pores and their morphology and the nanofibers, the SIA2100 device was used. The samples were sent for SEM analysis to check the morphological effect, and the samples were analyzed with x1000 magnification at a working distance of 3 mm at 10 kV.

A comparison of mechanical strength in different electro-spun scaffolds was made using an Instron model TM-SM machine made in England. First, the length and thickness of the samples were measured. Then, with a strain rate of 5 mm/min, a tensile force was applied to the samples in the direction of the nanofibers. After five repetitions for each sample, the stress-strain diagrams were obtained and compared.

The in vivo study used adult (male) Wistar rats weighing 200 to 250 grams. The animals were thoroughly examined to ensure the absence of any infection in the body. Rats were kept in separate aluminum cages in the animal room with appropriate conditions, 22 ± 2°C, relative humidity, temperature 40–60%, and a 12-hour light-dark cycle day and night. They were fed with pellets for laboratory animals and drinking water. Then 8 Wistar rats were randomly selected and divided into control groups (PVA-chitosan-curcumin) and treatment groups (PVA-chitosan-curcumin containing TNT). To create wounds, the rats were first anesthetized by intraperitoneal injection of ketamine 75 mg/kg and xylazine 10 mg/kg. Then the hair on the animal's back was cut short; then, a one-centimeter incision was made in non-infectious conditions after smearing the skin with betadine solution with the help of a scalpel. The percentage of wound contraction was measured by measuring the area of the wound immediately after wounding, during the two weeks of the study, and on days 3, 7, and 14. The measurement was expressed as the percentage of contraction, wound using the following formula (1):

$$\% Wound contraction=\frac{\text{W}\text{o}\text{u}\text{n}\text{d} \text{a}\text{r}\text{e}\text{a} \text{o}\text{n} \text{d}\text{a}\text{y} 1 - \text{W}\text{o}\text{u}\text{n}\text{d} \text{a}\text{r}\text{e}\text{a} \text{o}\text{n} \text{d}\text{a}\text{y} \text{n}}{\text{W}\text{o}\text{u}\text{n}\text{d} \text{a}\text{r}\text{e}\text{a} \text{o}\text{n} \text{d}\text{a}\text{y} 1}\times 100$$

At the end of the 14-day treatment period, after induction of anesthesia, the biopsy samples of repaired skin were separated and placed in 10% formalin for histopathological studies. The tissue samples were examined regarding fibroblastic cells and the thickness of the epidermal layer using hematoxylin and eosin staining. The stained sections were examined and studied under a light microscope (Olympus, Japan) with a magnification of 40.

Figure 1a displays the SEM micrograph of TiO₂ nanotube powders that have tubular morphology with a diameter of about 40 nm and a length of several hundred nanometers to several micrometers, unlike the spherical morphology of P25 nanoparticles. Also, TEM was utilized to show the tubular structure of TNT which was hollow and open-ended nanotubes with uniform inner and outer diameters (see Fig. 1b).

In the following, the results of evaluating the properties of each electrospun sample will be examined. FTIR spectroscopy was utilized to characterize the presence of chemical compounds and monitor the molecular interactions between ingredients. According to Fig. 2a, the chitosan/PVA blend illustrates the absorption peaks of both chitosan and PVA, the chemical formula of PVA and chitosan is (C₂H₄O) n and C₆H₁₁NO₄, respectively. The broadband at 3200–3550 cm^− 1 is related to O-H stretching or –H bands. The C-H is stretched at 2940.46 cm^− 1. The wavelength of 1255–1265 cm^− 1 indicates the -CH₃ wagging. The broad absorption bands at 1083.86 cm^− 1 are attributed to the C-O stretching mode. The peaks at 849.64 cm^− 1 were assigned C-C vibrations of PVA. The chitosan vibration situates in the broadband at 3360 cm^− 1 which is owing to the OH stretching. The bands at 1432.92 and 1728.11 cm^− 1 are assigned for NH bending (NH₂) and $\text{C}=\text{O}$ stretching (amid I) [24]. These results might differ slightly from the obtained results by others which is due to that when two or more polymers are blends, the characteristics spectra peaks could change, as a result of the reflection of physical blends and chemical interactions. These observations show a good miscibility between chitosan and PVA which is most likely owing to the formation of intermolecular hydrogen groups between the amino and hydroxyl groups that belong to chitosan and hydroxyl groups in PVA. Adding the curcumin to the chitosan-PVA blend (see Fig. 2b), led to a slight shift which could be caused by interactions between the polymer matrix and the phenolic compounds present in the curcumin powder. Peak displacement for NH₂ was observed at wavenumbers of 1432 cm⁻¹ (mixed polymers) and 1428 cm^− 1 (blend with curcumin) [25]. Siripatrawan et al. [26] have similar findings about the formation of covalent bonds between chitosan and green tea extract. Figure 2c, d, and e show the blend of chitosan/PVA/curcumin with various TNT powders. The broadband around 440 to 700 cm^− 1 is attributed to both the Ti-O-Ti band and the vibrations of Ti-O bonds in the TiO₂ lattice. In addition, the peaks at about 1630 and 3400 cm^− 1 have been assigned from the adsorbed water, and a large amount of hydroxyl groups appear on the surface of the TNTs [23]. It is noteworthy that the addition of TNTs into the chitosan/PVA/curcumin blend shifted a peak at 443 cm^− 1 to a higher wavenumber while the quantity of TNTs increased in the polymeric blend.

The structure of scaffolds was examined by scanning electron microscope. Figure 3 shows completely uniform fibers and interrelated porosity. All investigated samples collected the fibers without tangling on aluminum foil. The diameter of fibers was also calculated by the Image J software. Figure 3A is related to the PVA-chitosan sample; the average fiber diameter in this structure is 53 nm. In another study, PVA/Chitosan nanofibers were made, and the average fiber diameter in this structure was calculated to be 53 nm [25]. Figure 3B is related to PVA-Chitosan-Curcumin. Compared to sample A, the fiber diameter has increased slightly and reached 57 nm. The structure of the PVA-Chitosan-Curcumin-TNT scaffolds can be seen in Fig. 3C, D, and E which compared to A and B, their dimensions of the pores decrease. Also, the diameter of the fibers increases significantly, so that in the structure containing 0.5% TNT (Fig. 3C), the average diameter of the fibers is 65 nm, and in 1.5% TNT (Fig. 3D) is 66 nanometers. However, the structure containing 3% TNT (Fig. 3E) shows a significant increase in the fibers' diameter, and the fibers' diameter reaches 74 nm, and the dimensions of the porosity are significantly reduced.

To investigate mechanical properties, fabricated scaffolds were subjected to 5 mm/min tension in the direction of parallel nanofibers. After five repetitions for each sample, the results were analyzed as a stress-strain diagram for each sample (Fig. 4). The results of the stress-strain diagram (Fig. 4a) show that the PVA-chitosan scaffold has the lowest and PVA-chitosan-curcumin-TNT 3% has the highest mechanical strength. Tensile strength obtained from the stress-strain diagram shows that the PVA-chitosan scaffold has tensile strength of 1.99 MPa. In another study, PVA/Chitosan nanofibers have a tensile strength of 0.89 MPa [26]. The incorporation of chitosan into the PVA network could lead to a less efficient crosslinking rate between PVA and chitosan, consequently, the mechanical properties improve becoming the most rigid. Stress-strain curve of PVA-CS was extremely dependent on the strain rate, which means the viscoelastic behavior, is generally observed in tensile tests of synthetic fibers, tendons, and ligaments. Therefore, the blend of PVA and chitosan can mechanically replace non-mineralized tissues, such as skin and muscle [29]. The PVA-chitosan-curcumin scaffold has a tensile strength of 2.54 MPa. In another study, PVA/Chitosan/Curcumin nanofibers have a tensile strength of 2.2 MPa [27] which is almost similar to the result obtained by our group. Another point that should be stated is that the distribution of curcumin in the polymeric matrix increases the strength by 20% compared to the pure PVA/chitosan sample which could make productive stress transfer at the interface. The increase in tensile strength at break means more strength. The intermolecular interaction between OH and NH₂ groups of cyclic chain in chitosan molecules between chitosan and curcumin led to an improvement of the mechanical properties of the polymeric matrix. Adding curcumin, due to high-energy intermolecular interactions in which Cur acts as the CS molecules’ interface coupling agents, aids in the crosslinking between chitosan and curcumin, consequently, tensile strength increases [31]. An insignificant increase in the tensile strength of PVA/chitosan due to curcumin loading was noted which could be attributed to the hydrophobic nature of curcumin and its effect on the integration of two polymers [32]. By adding TNT to the scaffold structure, it can be seen that the strength increases. The tensile strength of PVA-chitosan-curcumin scaffolds containing 0.5, 1.5, and 3% of TNT was 2.81, 3.95, and 7.4 MPa, respectively (Fig. 4b). Thus, the addition of TNT into the polymeric matrix led to increased resistance to the deformation of PVA-CS material. This high enhancement is similar to that observed by Sharma et al. [33], where they showed that the addition of 2% carbon nanofiber in a polypropylene matrix caused a 748% increase. Interestingly, at a higher percent of TNT content, scaffolds did not experience a decrease in strength, which was contrary to the results shown by Eslami et al. [34], they obtained the optimal percent of TNT, 0.5 wt. % and believed due to high surface to volume ratio of nanotubes, resulting in, nanotubes accumulated which leads to the lack of TNTs proper dispersion. However, we obtain the higher strength, when the TNT percent reached 3 wt. %, which is more likely owing to the appropriate distribution of nanotubes in the polymeric matrix. This will provide more uniform stress distribution, minimizing the formation of the stress-concentration centers, finally, the increase in interfacial area for stress transfer from polymeric matrix to the nanotubes as a filler [35] as well as, because TNTs described as a continuous fiber, therefore, they can release stress in the composite without breaking and will increase the toughness of the composite for the sake of energy absorption of nanotubes [34], which led to good mechanical properties. As a result, they possessed acceptable tensile strengths for application in soft tissue engineering.

To investigate the ability of TiO₂ nanotubes incorporated polymer blende on the wound healing, the PVA-chitosan-curcumin as well as that containing 3 wt% TNTs were sutured in the full thickness wound in the rats. On the day of implantation and each day after the implantation, the wound size was checked in each group and until the wound was completely healed, photographs were taken. Figure 5 shows the photographs of the wound with both neat and nanotube- containing wound dressings on the first day (Fig. 4a and e), on the 3rd day (Fig. 5b and f), on the 7th day (Fig. 5c and g), and on the 14th day (Fig. 5d and h) of implantation. In the initial days after implantation, it was difficult to get a clear idea about wound healing. However, it was obvious that the surface area property diminished over time during fourteen days in all treatments so that, the treatment group with nanotube was able to create a more restored surface area compared to the PVA-chitosan-curcumin group. Between the 3rd and 7th day of implantation, a region of both control wound dressing and nanotube-incorporated wound dressing is expelled from the healing wound along with the debris. After this, the wound surface was observable and there was a remarkable difference in healing between groups (Fig. 5.d and h). TiO₂ nanotube-containing wound dressings were healed entirely within this period. It is also worth noting that on the 14th day, the wounds were entirely healed without any sign of scar formation in the case of nanotube-incorporated electrospun wound dressing. During the wound healing process, these fibrotic scars are usually formed, which can damage the normal tissue organization and have an effect on regeneration [36]. In this study, we could not perceive such a fibrotic scar after the entire wound healing which indicates regeneration. In the control sample of implanted wounds, hair formation in the healed area was less than in other regions. However, the sample containing TiO₂ nanotube has normal skin with hairs as in other areas has been observed. Because there are no hair follicles which are the stem cells that produce hair as well as the lack of other components of the skin containing sebaceous glands and the epidermis [37]. From the point of view of inflammation in the wound areas, a minor inflammation was observed in the case of 3wt% TiO₂ nanotube-containing wound dressing which could be due to the release of TiO₂ nanotubes after implantation. This is attributed to release faster into the implantation site due to the agglomeration of nanotubes and, as a result, inflammation. This systemic inflammation is produced by higher levels of reactive oxygen [35].

The rate of wound healing was calculated from the area of healing wound to complete wound healing and expressed as the percentage of wound healing can be seen in Fig. 6. Up to 3rd day of healing, there was a negligible variation in the area of wound in both control and nanotube incorporated samples. But after that nanotube incorporated wound dressings showed a higher rate of wound healing so that 93% of wound healing was achieved on the 14th day of implantation whereas control wound dressing was still not entirely healed which was only 73% of wound healing. It seems that TiO₂ nanotube containing wound dressing can not only improve wound treatment but also decline the elements against wound healing.

The influence of PVA-chitosan-curcumin including TiO2 nanotubes on the induction of fibroblast cell proliferation in in vivo is illustrated in Fig. 6. In the semi-quantitative evaluation section, histopathological indicators, it is obvious that the treatment specimen with 3 wt% of TiO₂ nanotubes increased the fibroblast proliferation compared to the control wound dressing (Fig. 7). After 14 days of implantation, attachment of fibroblast cells enhanced and grown through the treatment wound dressing with 3 wt% TiO₂ nanotubes. Fibroblast cells have displayed their trait elongated spindle-shaped morphology on PVA-chitosan-curcumin wound dressings that include TiO₂ nanotubes whereas in the control wound dressing the cells had spherical morphology. The epidermis layer is fully formed in the treatment group and has a greater thickness than in the control group. Epidermis formation in the treatment subgroup was more complete and faster than in the control group. There was no significant difference between the epidermis thicknesses in the two groups (Table 2). The wound covered with a specimen containing TiO₂ nanotube did not have a substantial increment in granulation tissue spot compared to the control. Angiogenesis was relatively high in the wound dressing contacting TNTs on day 14 when compared to the control group. Generally, the proliferation phase includes four stages: reepithelization, angiogenesis, tissue granulation formation, and collagen deposition [38]. As can be seen in Table 2, these four indices for wound dressing treated with TiO₂ nanotubes were relatively higher than the control specimen. Another reason that could be stated is related to the anti-bacterial and anti-inflammatory characteristics of TiO₂ nanotubes. A number of researchers utilized an effective approach to speed up wound healing, for example. Razali et al. [393] used TiO₂ nanotubes incorporated gellan gum bio-nanocomposite to accelerate wound healing. Moreover, TiO₂ nanotubes regulate the progression of wound healing through enhancement of skin moisture (hydrophilic activity) [40].

Table 2

Effect of TNT on investigated traits
group	Epithelial gap (µ)	Granulation tissue (µ)2	Angiogenesis (n)	Collagen fiber thickness (µ)	Fibroblast cells (n)	Collagen density (%)	Epithelialization (µ)	inflammation	Hyperemia
Control	0	2.25 x 10⁶	480	37.5	12550	61	70	-	-
Treated With TNTs	0	3.75 x 10⁶	504	86	21450	89	102	-	-

In this research, it was aimed to design impressive wound dressing for burn wounds by supporting the influence of PVA and chitosan with curcumin and TiO₂ nanotubes. According to the obtained results, nanofiber formulation possesses high chemical stability, mechanical resistance, and along with faster wound healing. In addition, it was shown that covering wounds with PVA-chitosan-curcumin containing TiO₂ nanotube improved considerably wound healing, accelerated angiogenesis, epidermal regeneration, and stimulated granulation, without any inflammation response. In conclusion, using PVA-chitosan containing curcumin and TNT as a wound dressing material will contribute to the wound healing process.

Acknowledgements

The authors are very pleased for the support of the Faculty of Engineering, Meybod University, Meybod, Iran.

Authors’ contribution

All authors have actively contributed to this project. HS contributed to martial synthesis and managed the project. NK did martial synthesis and experimental section. MA contributed to martial synthesis and data analysis. HZZ managed and supervised the project. HRP contributed to martial synthesis and data analysis.

Funding

There is no funding source.

Availability of data and materials

The data and materials are available.

Ethical Approval

The animal study was approved by ethic committee of Meybod University, Iran.

Conflict of interest

The authors declare that they have no conflict of interest.

Consent to participate

All authors have been personally and actively involved in substantial work leading to the paper and consent to participate.

Consent for publication

The paper is not currently being considered for publication elsewhere and all authors are consent for publication.

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Design of an electrospun polyvinyl alcohol (PVA)/chitosan/curcumin based- wound dressing containing titania nanotubes (TNT)

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