Characterization, biocompatibility, and optimization of electrospun SF/PCL composite nanofiber films

Yanping Feng; Zhang Jupei; Zhihong Dong; Lu Tang

doi:10.1515/rams-2022-0333

Article Open Access

Characterization, biocompatibility, and optimization of electrospun SF/PCL composite nanofiber films

Yanping Feng , Zhang Jupei , Zhihong Dong and Lu Tang

Published/Copyright: July 11, 2023

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From the journal REVIEWS ON ADVANCED MATERIALS SCIENCE Volume 62 Issue 1

Abstract

In this study, composite nanofiber films for the wound dressing application were prepared with silk fibroin (SF) and polycaprolactone (PCL) by electrospinning techniques, and the SF/PCL composite nanofiber films were characterized by the combined techniques of scanning electron microscopy (SEM), the equilibrium water content, Fourier transform infrared spectrometer test, X-ray diffraction (XRD) and cell viability test. The results indicated several parameters, including the rotating roller speed, solution concentration, and SF/PCL ratio, affected SF/PCL composite nanofibers’ diameter size, distribution, and wettability. The SF/PCL composite nanofiber manifested a smaller fiber diameter and more uniform nanofibers than pure PCL nanofibers. The contact angle changed from 121 ± 2° of the neat pure PCL to full wetting of 40% SF/PCL composite nanofiber films at 2,000 rpm, indicating good hydrophilicity. Meanwhile, cells exhibit adhesion and proliferation on the composite nanofiber films. These results testified that SF/PCL composite nanofiber films may provide good wettability for cell adhesion and proliferation. It was suggested that optimized SF/PCL composite nanofiber films could be used as a potential biological dressing for skin wound healing.

Keywords: silk fibroin; polycaprolactone; hydrophilic; roller speed; fiber diameter

1 Introduction

The human body’s skin is a natural protective barrier against external pathogens but it is also fragile and easily injured leading to forming wounds to some degree [1]. Normal wound healing needs a long time, and exudation may be produced during the wound recovery period, which leads to adverse consequences such as wound inflammation and even partially purulent infection. So, it is particularly important to select appropriate wound dressings that are non-toxic and biocompatible for absorbing the exudation and accelerating wound healing [2,3]. In clinics, there are more types of wound dressings, such as hydrogels [4] and spinning films [5]. Compared with traditional gauze [6], these materials are antibacterial, hydrophilic, breathable, and biocompatible, and even some may be degradable to avoid secondary injury from multiple replacements [7]. In recent years, with the development of electrostatic spinning technology, electrospun nanofibers have been widely used in many fields such as environmental air filtration [8], biosensing [9], nanoelectronics [10], and biomedical engineering [11] due to their unique properties (e.g., large specific surface area and high porosity). Especially in biomedicine, some good biocompatible materials, such as natural SF [12], gelatin [13], and alginate [14] and synthetic polyethylene glycol [15], polylactic acid, and polycaprolactone (PCL) [16], are often used in wound healing [17], drug transport [18], tissue engineering [19], neural repair [20], and so on. By electrospinning technology, different types of composite nanofiber films were prepared according to the characteristics of the materials [21,22]. In particular, natural silk fibroin (SF) extracted from silk is a good biomaterial [23,24]. It exhibits properties such as good biocompatibility, biodegradability, mechanical properties and hydrophilicity, and non-toxicity, and may make cell proliferation, adhesion, and migration to promote wound healing as wound dressings [25,26]. Yet, high molecular weight PCL has excellent strength, elasticity, and controllable biodegradability, and therefore, was preferred as wound dressings [27]. However, hydrophobic PCL hindered wound exudate absorption and cell adhesion, and further limited the use [28]; while the special structure of pure SF (β-sheet secondary structure) may improve hydrophilicity for electrospinning [29]. So, it is optimal to prepare the PCL/SF composite to electrospun composite nanofibers due to good spinnability and non-toxicity [30,31]. Although the addition of SF will accelerate the degradation of PCL, it only degrades 1.44% after 90 days [32] and 8.08% after 2 weeks [33], and this slow degradation is conducive to structural stability and can effectively promote the long repair period of biological tissues. This composite nanofiber film with good hydrophilicity and biocompatibility can be used as a carrier for other antibacterial substances, such as chitosan [34], minocycline hydrochloride antibiotics [35], etc., which could provide more valuable reference for wound dressings.

Studies have shown that smaller diameter and uniformity of fiber can provide high porosity and easier absorption of water molecules to promote hydrophilicity and cell adhesion and proliferation [34]. The spinning parameters like the fiber diameter, voltage, flow rate, roller speed, and spinning concentration were affected [36,37], but few studies testified SF/PCL composite nanofiber films as wound dressings by the combination of high roller speed and high solution concentration to explore lower fiber diameter and better hydrophilicity, as well as the impact on cell compatibility. In this study, SF/PCL composite nanofiber films were prepared by different roller rotation speeds and SF contents to explore better SF/PCL composite nanofiber films for skin tissue repair.

2 Experimental methods

2.1 Materials

SF powder was obtained from Senyuan Biotechnology Co. Ltd (Xi’an). PCL (average molecular weight: 40,000) was obtained from Shangpu Boyuan (Beijing) Biotechnology Co., Ltd. Hexafluoroisopropanol (HFIP, 99.5%) was obtained from Shanghai Aladdin Biochemical Technology Co., Ltd. Dichloromethane and other chemical reagents in this experiment were obtained from Chengdu Kolon Chemical Co. Ltd.

2.2 Preparation of the electrospinning solution and electrospinning parameter setting

About 0.8 g of PCL was dissolved in a mixed solvent of 10 mL HFIP and 5 mL DCM, and SF was added according to different SF/PCL weight percentages (0, 5, 20, and 40). Furthermore, the mixed solution was stirred for 12 h at room temperature to finally obtain a transparent spinning solution. The SF/PCL composite nanofibers were electrospun by an electrostatic spinning machine (model: TL-01, Tongli Micro-Nano Technology Co.), and the specific schematic diagram is shown in Figure 1. Briefly, the electrospun solution was loaded into a 10 mL syringe; the liquid was ejected from the catheter through a 22-gauge needle and extruded into nanofibers with a syringe pump at room temperature and an ambient relative humidity of 45–55%. The following optimized electrospinning parameters were kept in the whole experiment: applied electric field voltage, 15–18 kV; feeding rate, 1–1.2 mL·h⁻¹; and the tip to collector distance, 10 cm. During this process, the SF/PCL nanofibers were sprayed on a rotating cylindrical drum with aluminum foil, and different roller rotation speeds (250, 500, 1,000, and 2,000 rpm) were adjusted to prepare sample groups. Finally, the SF/PCL nanofiber films were obtained from the collector surface and dried at room temperature prior to use.

Figure 1

Schematic diagram of the electrospinning process.

2.3 Characterization of SF/PCL nanofiber films

The morphology of SF/PCL composite nanofiber films was observed by scanning electron microscopy (SEM; SU8010, Japan). The average diameter size and distribution of fibers of 50 fibers randomly selected from each sample were determined. The microstructure was analyzed by using a Fourier transform infrared (FTIR) spectrometer (Nicolet Co., USA) with a scan range of 4,000 to 400 cm⁻¹, and recorded with a resolution of 2 cm⁻¹ by 45 scans. The crystal structure was analyzed by X-ray diffraction (XRD; Bruker, Germany) with a scan range of 5–80 cm⁻¹. Wettability was evaluated by measuring the contact angle of the fiber films using a contact angle meter (WM2017013, Sweden Beolean Technology Co). All measured samples were tested three times, and the average value was obtained.

2.4 Biocompatibility of SF/PCL nanofiber films

In order to evaluate the biocompatibility of SF/PCL composite nanofiber films (soaked in 75% ethanol, dried overnight, and then sterilized with UV for 5 min), a cell viability test was performed using human umbilical vein endothelial cells (HUVECs) for 24 h, and cell morphology and distribution were observed by microscope. The specific process was as follows: first, the nanofiber films were put on the bottom of 48-well plates, and cells were seeded on them at a density of 3,000 cells per well; then HUVECs were cultured in Dulbecco's modified Eagle’s medium (10% fetal bovine serum). In all tests (blank, control, and sample groups), HUVECs were incubated at 37°C for 24 h, and then HUVECs were fixed with 4% paraformaldehyde for 10 min, stained with 0.014% methyl violet for 5 min, and observed and photographed using a microscope. In order to evaluate the cell viability of SF/PCL composite nanofiber films under different spinning conditions, a cell viability test was performed using HUVECs for 5 days, and cell viability was assayed with CCK-8 (Cell Counting Kit-8). The nanofiber films were put on the bottom of 96-well plates and cells were seeded on them at a density of 2,000 cells per well; other culture conditions were the same as above. Then, the medium was replaced with 100 μL of the CCK-8 solution and incubated at 37°C for another 1 h. Finally, the absorbance of each well was measured using a spectrophotometer to obtain the desired optical density (OD₄₅₀) values.

2.5 Statistical analysis

The data were expressed as mean ± standard deviation (SD) and analyzed using a one-way analysis of variance. Statistical analysis was performed using GraphPad Prism 9 software. A significant difference was considered with p < 0.05.

3 Results and discussion

3.1 Effect of roller speed on the structure and hydrophilicity of pure PCL nanofiber films

Uniform and order nanofibers can provide higher surface area and interconnected pores to facilitate cell adhesion and proliferation as wound dressings [38]. The roller speed was one of the key factors to affect the diameter of pure PCL nanofibers. The SEM results showed that with the increase of the roller speed, the diameter size of nanofibers became more uniform and the nanofibers were orderly arranged toward particular directions (Figure 2a). At lower roller speeds (250 and 500 rpm), the electrospun nanofibers were in disorder, and at higher roller speeds (1,000 and 2,000 rpm), the nanofibers tended to be in order. Moreover, the nanofibers’ diameter decreased gradually as the roller speed increased. The average diameter of the nanofibers was in the range of 350–200 nm (Figure 2c) and the distribution was more uniform. It was because the fibers were stretched quickly from the electrospinning needles ejecting rapidly when the roller was accelerated, making the fibers finer. At the same time, acceleration can reduce the number of fibers that are randomly dropped on the roller. Under similar conditions, the fiber diameter distribution at a 150 rpm roller speed was uneven, showing micro-nanometer levels, which was different from our results [39]. Pure PCL is a kind of hydrophobic material, and no matter how the nanofibers are arranged, the contact angle was around 120°, which showed that PCL nanofiber films had good hydrophobicity (Figure 2b). These results indicated that it was feasible to increase the electrospun roller speed to improve the size and uniformity of nanofibers.

Figure 2

SEM micrographs of PCL electrospun films at different roller speeds. The second column shows the high-magnification images corresponding to the first column (a) and the corresponding wettability (b). The diameter size distribution (c).

3.2 Effect of SF content on the structure and hydrophilicity of SF/PCL composite nanofiber films

In the electrospinning process, the spinning solution concentration was considered to be an important parameter to affect the fiber structure [40]. Different contents of SF were used to prepare SF/PCL composite nanofibers at a 250 rpm roller rotation speed (Figure 3). Figure 3a shows that some small beads were formed at lower concentrations (5–10%), which may be the lower viscosity spinning fluid leading to an unstable jet flow. When the SF content was in the range of 0–40%, the fiber size gradually decreased from 330 to 90 nm, and the fiber diameter size distribution was more uniform (Figure 3c). When the roller rotation speed was constant, the viscosity of the solution affected the uniformity and diameter size of the fiber formation. Research showed that the increase of SF content was beneficial to shorten the fiber diameter; however, it did not shorten the fiber diameter below 100 nm [22,33]. Meanwhile, SF may improve the wettability of the fiber film. When SF was added to the PCL solution, the concentration changed from 0 to 40 wt%, the contact angle decreased from 121° to 56°, which showed better hydrophilicity (Figure 3b). Compared with the study by Lee et al. [27], this experiment can reach the contact angle of SF/PCL nanofiber films below 98° after the addition of SF. It has been proved that the increase of SF content may decrease the contact angle of the SF/PCL fiber film; meanwhile, this composite nanofiber film may provide a better moist environment for tissue regeneration. Of course, under the same conditions, the hydrophilicity of 40% SF/PCL films was greater than that of the films, and the contact angle was less than 75° [41]. These results indicated that SF can improve the hydrophilicity and the order of SF/PLC composite nanofiber film, and they have great potential for skin wound healing [42].

Figure 3

SEM micrographs of PCL electrospun films with different SF contents at 250 rpm roller speeds. The second column shows the images at high magnification corresponding to the first column (a) and the corresponding wettability (b). The diameter size distribution at a 250 rpm roller speed (c).

Under the above conditions, the effect of different concentrations of SF solution on the uniformity of nanofiber films was determined when the roller rotation speed was increased to 2,000 rpm. The results are shown in Figure 4: as the SF content increased, the nanofiber remained well organized (Figure 4a) and the average diameter size decreased gradually from 193.4 to 50 nm (Figure 4c). The higher roller rotation speed (2,000 rpm) resulted in a smaller fiber diameter and more uniformity and compacted diameter distribution compared to that of the 250 rpm roller rotation speed. The wettability of SF/PCL composite films also improved gradually with the increase of SF content, especially the 40% SF/PCL fiber, which can achieve complete wetting (Figure 4b). Undoubtedly, it was more advantageous for cell adhesion and proliferation. These results showed that an increase of both SF content and roller speeds may spin finer and more uniform diameter nanofiber, which was beneficial to improve the wettability of SF/PCL composite nanofiber films. It has been shown that the contact angle of SF/PCL nanofiber fibers can be reduced by adding SF [43], after UV-ozone irradiation and acrylic acid treatment [44], or by adding PEO[45]. The last two methods are too complicated, and in both methods, complete wetting cannot be achieved. In comparison, it is more beneficial to the application of biocompatible composite fiber membranes by controlling the SF content and roller rotation speed to achieve complete wetting.

Figure 4

SEM micrographs of PCL electrospun films with different SF contents at 2,000 rpm roller speeds. The second column shows the high-magnification images corresponding to the first column (a) and the corresponding wettability (b). The particle size distribution at 2,000 rpm roller speed (c).

3.3 FTIR analysis

The FTIR spectra of the nanofibers are shown in Figure 5. For the pure SF, PCL, and SF/PCL composite nanofiber films, the peak characteristics of PCL can be observed clearly by comparing the spectra of other samples. The stretching band C═O of carbonyl esters was located at 1,719 cm⁻¹ in pure PCL nanofibers. The strong band of PCL crystalline phase at 1,240 cm⁻¹ was assigned to C−O and C−C stretching, the peak at 1,173 cm⁻¹ was attributed to vibrations in COC, C–O, and C–C, and the peak at 732 cm⁻¹ represented CH₂ bending of the caprolactone chain [46]. All characteristic bands of PCL were presented in SF/PCL composite nanofiber films; amide I, amide II and amide III bands appeared in pure SF, and further were more obvious in SF/PCL. These results testified that SF and PCL obtained a good molecular bonding.

Figure 5

FTIR patterns of SF/PCL nanofiber films.

3.4 XRD analysis

The XRD patterns of SF, pure PCL, and 40% SF/PCL composite nanofibers are shown in Figure 6. SF was an amorphous substance, and pure PCL showed a semi-crystalline state with three obvious diffraction peaks at 21.5° (110), 22.2° (111), and 23.9° (200) [47]. After the addition of the SF/PCL composite, the characteristic reflection peak became weaker and wider. Obviously, the crystallinity of PCL decreased while its crystalline structure did not change with the addition of SF.

Figure 6

XRD patterns of SF/PCL nanofiber films.

3.5 Biocompatibility evaluation of SF/PCL composite nanofiber films

The cell viability of HUVECs grown on SF/PCL composite nanofiber films within 24 h was evaluated (Figure 7a). The cell viability of HUVECs grown on SF/PCL composite nanofiber films was continually monitored for 5 days by the CCK-8 assay technique (Figure 7b and c). The results indicated that at lower 250 rpm, higher 2,000 rpm, or with added SF content, there was no significant difference compared with the blank group over 24 h, showing that composite nanofibers were nontoxic. At a high roller rotation speed, the average OD value was 7% higher than that at a low speed, which showed good cell viability. These results indicated that the structure and wettability of SF/PCL affected the cells’ proliferation and differentiation, and it also provided a better research idea for wound healing and skin engineering repair.

Figure 7

Fluorescence images of HUVECs grown on SF/PCL composite nanofiber films within 24 h at 250 and 2,000 rpm roller rotation speeds (a). HUVECs viability was cultured on various specimens for 5 days at 250 and 2,000 rpm roller rotation speeds (b and c). Data represent mean ± standard deviation (n = 5). The bar scale is 200 μm. *p < 0.5, **p < 0.01, ***p < 0.001 vs blank; ^# p < 0.5, ^## p < 0.01, ^### p < 0.001 vs 0%.

4 Conclusion

Different contents of SF were mixed with PCL to prepare SF/PCL composite nanofiber films by electrospinning technology. The process parameter of roller rotation speeds affected the diameters and diameter distributions of nanofibers, and SF contents affected the hydrophilicity/hydrophobicity of SF/PCL composite films. The diameter of the 40 wt% SF/PCL composite nanofiber was the smallest and more uniformly distributed at a higher 2,000 rpm roller rotation speed and could be completely wetted to improve cell proliferation and adhesion. SF/PCL composite nanofibers had better cell viability. It was concluded that the SF/PCL composite nanofiber films were valuable for application as a dressing to promote wound healing.

Funding information: This research was supported by the Key Project of Sichuan Medical Association (Q17002), Chengdu Municipal Technological Innovation R&D Project (2021-YF05-01871-SN), and Project of Chengdu Municipal Health Commission (2021059).
Author contributions: All authors have accepted responsibility for the entire content of this manuscript and approved its submission.
Conflict of interest: The authors state no conflict of interest.

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Received: 2022-09-12

Revised: 2023-02-16

Accepted: 2023-06-11

Published Online: 2023-07-11

This work is licensed under the Creative Commons Attribution 4.0 International License.

Articles in the same Issue

https://doi.org/10.1515/rams-2022-0333

Keywords for this article

silk fibroin; polycaprolactone; hydrophilic; roller speed; fiber diameter

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