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Functionalized Antimicrobial Electrospun Poly

(vinyl alcohol) Nanowebs

Uday Turaga, PhD, Vinitkumar Singh, PhD, Anna Gibson, PhD, Shahrima Maharubin, Carol Korzeniewski, PhD, Steven Presley, PhD, Ernest Smith, PhD, Ronald J Kendall, PhD, Seshadri S. Ramkumar, Ph.D.

Texas Tech University – TIEHH, Lubbock, TX UNITED STATES

Correspondence to

Seshadri S. Ramkumar email: s.ramkumar@ttu.edu

ABSTRACT

Electrospun poly (vinyl alcohol) [PVA] nanowebs functionalized with a commercially available microbiocidal solution Reputex™ 20 were prepared. The active ingredient of Reputex™ 20 is polyhexamethylene biguanides, a safe antiseptic. Fourier Transform Infrared spectroscopy confirmed the functionalization of PVA nanowebs. Functionalized nanowebs were characterized by evaluating their antimicrobial properties, breathability characteristics and tensile properties. Functionalized nanowebs demonstrated significant antimicrobial activity against both Gram positive and Gram negative bacteria. Nanowebs developed from biocompatible polymers like PVA, and functionalized with safe antiseptics, could find many biomedical applications such as wound bandages.

Keywords: Poly (vinyl alcohol), Reputex™ 20, polyhexamethylene biguanides, Fourier transform infrared spectroscopy

INTRODUCTION

The technique of electrospinning has enabled the production of micron and sub-micron fibers with unique properties such as high surface area to volume ratio and high porosity. An external applied electric potential that draws fine fibers from a polymer solution is used in electrospinning. Electrospun fibers are increasingly finding applications in many different sectors such as filtration, life sciences, defense, etc. The aspect of functionalization imparts additional properties to electrospun nanofibers thereby enhancing their applicability [1-7].

One potential biomedical application of nanofibers that is being increasingly investigated is wound dressing materials. Wound dressings assist in the complex biological process of wound healing in vitro. Wound dressing materials are expected to serve the following functions to facilitate the effective healing of wounds: 1) absorb wound exudates; 2) suppress microbial activity near the vicinity of

wound interface and 4) be nontoxic, nonallergic and nonscaring [8]. The high porosity and pore-interconnectivity of electrospun nanofibers enable excellent gas/fluid exchange and efficient exudation of fluids from wound site. More importantly, the small size of pores in nanofibers inhibits the invasion of exogenous microorganisms [9].Nanofibers present themselves as ideal candidates for use in wound bandages by virtue of these important properties.

One of the crucial requirements of nanofibers for use in wound dressing materials is their antimicrobial property; they should prevent bacterial colonization and subsequent infections. Development of nanofibers with antimicrobial properties could be accomplished in the following ways: 1) using a blend of polymer solution and the active agent in electrospinning; 2) co-axial electrospinning that confines the active agent in the core of fibers; 3) use of a precursor during electrospinning that could later be activated; 4) post-electrospinning procedures that functionalize the fibers with active agent and 5) encapsulation of active agents in nanofibers prior or post electrospinning [10]. The first approach has been widely used and the incorporation of antibiotics such as rifampicin and paclitaxel [11], mefoxin [12], and metal oxide nanoparticles such as silver [13] has been discussed in literature. However, the possibility of microorganisms developing antibiotic resistance [14] and the ambiguity in using nanoparticles near open wounds where they may gain potential access in to human body [13] has resulted in a need for safe antiseptics for use in wound dressings.

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importantly, PHMBs are considered as non-toxic analogues of naturally occurring antimicrobial peptides (AMPs). AMPs are positively charged and low molecular weight proteins that bind to cell membrane of microorganisms and elicit their antimicrobial activity by compromising the membrane integrity [17]. Over the course of wound healing, growth factors induce the expression of AMPs as part of the host defense mechanism [18]. Additionally, PHMBs bind to the membrane in such a way that they settle on the surface of the membrane without integrating in to the lipid domains of the membrane. Efflux pumps that play a major role in removing drugs from the cytoplasm and cell membrane of bacteria are ineffective in removing PHMBs as they do not enter the lipid domains. Hence, the possibility of bacteria developing resistance towards PHMBs is negligible [14].

Owing to the advantages of using PHMBs in treating wounds, the functionalization of electrospun nanofibers with PHMBs for biomedical applications has been recently investigated. Dilamian et al. (2013) have studied the influence of PHMBs on electrospun chitosan/polyethylene oxide nanofibers. The authors have inferred that the addition of PHMBs increases the conductivity of electrospinning dope resulting in a decrease in diameter of nanofibers [19]. Liu et al. (2012) have developed and characterized blends of cellulose acetate and polyester urethane nanofibers functionalized with PHMBs for their use as potential wound dressings [20]. However, the aforementioned studies have employed harmful organic solvents like dimethylformamide and tetrahydrofuran, a concern from an environmental perspective. More importantly, both the studies have investigated the applicability of pure PHMBs, which may not always be readily available. The present study investigates the possibility of functionalizing a hydrophilic polymer, poly (vinyl alcohol) (PVA) with a commercially available microbiocidal solution Reputex™ 20 from Lonza, Inc. Reputex™ 20 is a 20% poly(hexamethylene biguanide)hydrochloride solution [21]. The objective of this study is to fabricate and characterize PVA nanofibers functionalized with Reputex™ 20 for use in various biomedical applications such as wound dressing materials. PVA is chosen because of its proven biocompatibility [22] and Reputex™ 20 is a special grade of PHMB available from Lonza, Inc. predominantly for textile treatments [21]. Preparation and characterization of PVA nanofibers functionalized quaternary ammonium compounds such as benzyl triethylammonium chloride has recently been discussed by Park and Kim 2015 [23].

However, the use of a commercial PHMB based product like Reputex™ 20 for functionalizing nanofibers has heretofore not been discussed in literature. More importantly, as PVA is a hydrophilic polymer, functionalized PVA nanowebs are heat cross-linked [22] to increase their stability in aqueous conditions. The effect of heat cross-linking on antimicrobial properties of functionalized PVA nanowebs is also studied.

EXPERIMENTAL SECTION Materials

PVA (MW: 89,000-98,000 and 99+% hydrolyzed) was obtained from Sigma-Aldrich. Mueller Hinton agar and Mueller Hinton broth were procured from Sigma-Aldrich. Escherichia coli ATCC® 25922™ (E. coli) and Staphylococcus aureus ATCC® 29213™ (S. aureus) were purchased from American Type Culture Collection (ATCC®). Reputex™ 20 microbiocidal solution was obtained from Lonza, Inc.

Preparation of Electrospinning Solution

A 12% PVA solution in 90:10 deionized water and Reputex™ 20 used as electrospinnig dope was prepared in the following fashion. Initially, 12 gms. of PVA were dissolved in 15 ml of DI water at 800C for 3 hours with intermittent stirring. 2ml of Reputex™ 20 was mixed with 3 ml of DI water separately. Finally, both the solutions were mixed using a magnetic stirrer after bringing the PVA solution to room temperature.

Electrospinning Set-Up

A syringe equipped with a 20 gauge needle and containing the PVA solution was loaded onto a Harvard Apparatus PHD 2000 infuse/withdraw pump. A flow rate of 0.02 ml/min was maintained. Nanofibers were drawn by charging the needle of the syringe to a voltage of 25kV using a Gamma High Voltage Power Supply unit (ES 30P-5W, Gamma High Voltage Research, FL). An aluminum collector was placed at a distance of 15 cm from the tip of the syringe.

Henceforth in this paper, Reputex™ 20 functionalized PVA nanowebs will be referred to as functionalized PVA nanowebs.

Heat Cross-linking of PVA Nanowebs

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Scanning Electron Microscopy (SEM) Characterization of PVA Nanowebs

Morphology of PVA nanwebs was characterized using a Hitachi S-4300SE/N SEM. An accelerating voltage of 2 kV was used with no coating on nanowebs. Average fiber diameter was calculated by measuring the diameters of 80 fibers from various locations of the web.

Fourier Transform Infrared (FTIR) Spectroscopy Measurements

The attenuated total internal reflection (ATR) mode FTIR spectra of all the samples were obtained using a Bruker Vertex 70 spectrophotometer (Bruker, Billerica, MA). The spectrophotometer was equipped with a liquid nitrogen cooled mercury-cadmium-telluride (MCT) detector. Spectra were recorded in the range of 4000-800 cm-1. The spectra were computed using an average of 128 interferograms measured at a resolution of 4 cm-1 and apodized with a Blackman-Harris 3-Term function. Dry air from a purge gas generator (Parker-Hannifin Corporation, Parker Balston Model 75-52, Haverhill, MA, USA) was used to continuously purge the spectrophotometer bench and sample compartment. All measurements were carried out at 23oC.

Antimicrobial Activity Tests

The antibacterial activity of functionalized nanofiber webs was evaluated against a Gram positive (S. aureus) and a Gram negative (E. coli) bacterium. The sensitivity or resistance of the aerobic bacteria to functionalized PVA nanowebs was determined using a Kirby-Bauer disk diffusion susceptibility test-like method. A 6-mm disk of nanofiber was cut and sterilized under UV light (15 minutes on each side) to avoid any contamination. Mueller Hinton agar plates were inoculated with 0.5 McFarland equivalent suspensions of fresh, 24 hour growth bacteria prior to the placing of disks on the agar surface. Native (non-functionalized) PVA nanowebs were used as negative control and 10% Reputex™ 20 in water was used as a positive control. For the sake of antimicrobial studies, functionalized PVA nanowebs were run in triplicate on each plate along with a positive (10% Reputex™ 20 in water) and a negative control (native PVA nanowebs). Inoculated plates were incubated at 370C for 24 hours. Following incubation, a ruler was used to measure the diameter (including the disk) of the zone of inhibited bacterial growth. All measurements are made with the unaided eye while viewing the back of the Petri dish.

Evaluation of Moisture Vapor Transmission Rate (MVTR) of Nanowebs

British Standard Evaporative Dish method (BS 7209:1990) was used to measure the water vapor permeability functionalized PVA nanowebs. The breathability of the webs, measured in terms of MVTR (g/m2/day), was calculated using Eq. (1):

MVTR=24M/At (1)

where M is the loss in mass of the assembly over a given time period t (g),

t is the time between the successive weighings of the assembly (h),

and A is the apparent area of the exposed test specimen (0.005413 m2).

Determination of Tensile Properties of Nanowebs Tensile properties of nanowebs were measured using an Instron 5569 tensile tester. A modified version of ASTM D638-10 (Standard test method for tensile properties of plastics) was used to carry out the measurements. A 2.5 Newton load cell at a crosshead speed of 10 mm/min was used for all the measurements. The maximum load (N), extension at maximum load (mm), and the modulus (MPa) were determined for the purpose of the study. A gauge length of 2 cm was used. The samples were cut into 1 cm × 3 cm pieces to carry out the tests.

Statistical Analysis

Statistical analysis of all the results was performed using R software (version 2.13.1, R Core Development Team 2011). A Students’ t-test was performed at a confidence interval of 95% (p=0.05) to analyze the significant difference in the means of the variables.

RESULTS AND DISCUSSION Morphology of PVA Nanowebs

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FIGURE 1. SEM images of functionalized/heat cross-linked PVA nanowebs and fiber diameter distribution histogram.

The average fiber diameter of pure PVA nanofibers electrospun and heat cross-linked under similar conditions was found to be 247±75 nm [24]. Hence, it can be inferred that functionalization with Reputex™ 20 resulted in a decrease in the diameter of PVA nanofibers. Studies from Dilamian et al. (2013) have suggested that addition of PHMBs increase the conductivity of electrospinning dope [19]. Also, it was observed in the present study that addition of PHMBs significantly decreased the surface tension of electrospinning dope (n=3, p<0.05). The addition of Reputex™ 20 to the electrospinning dope has decreased the surface tension of dope from 64.85 ± 0.15 mN/m to 59.16 ± 0.17 mN/m. The increase in the conductivity and decrease in surface tension of electrospinning dope would explain the overall decrease in average fiber diameter of functionalized PVA nanowebs.

FTIR of PVA Nanowebs

Results of infrared spectroscopy measurements comparing native, functionalized and functionalized/heat cross-linked PVA nanowebs are presented in Figures 2 and 3.

FIGURE 2. ATR Spectra of Reputex™ 20 and PVA Nanowebs in the low energy region of 800-1700 cm-1. (A) Native PVA Nanoweb (black). (B) Functionalized PVA Nanoweb (green). (C) Functionalized and Heat Cross-linked PVA Nanowebs (red). (D) Pure Reputex™ 20 solution.

FIGURE 3. ATR Spectra of Reputex™ 20 and PVA Nanowebs in the high energy region of 1000-3500 cm-1. (A) Native PVA Nanoweb (black). (B) Functionalized PVA Nanoweb (green). (C) Functionalized and Heat Cross-linked PVA Nanoweb (red). (D) Pure Reputex™ 20 solution. The insets in B and C expand the y-axis scales across the wavenumber regions indicated by a factor of 5.

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region between 1700-1500 cm-1 in the spectrum of the native PVA web (Figure 2A) is featureless, indicating the sample is free of absorbed water [25, 27]. The spectrum of the Reputex™ 20 solution (Figure 2D), in contrast, has dominant bands at 1633 cm-1 and 1555 cm-1 and is relatively featureless in the region near 1090 cm-1. The 1555 cm-1 band in the Reputex™ 20 (poly(hexamethylene biguanide)) spectrum is a signature for N-H bend vibrations [19]. The 1633 cm-1 peak probably arises from water (see below), although there may be a contribution from imine C=N stretching vibrations [19]. The spectrum of functionalized PVA nanoweb (Figure 2B) contains features common to the Reputex™ 20 solution and the native PVA web, demonstrating incorporation of active ingredient of Reputex™ 20 into PVA nanoweb during the electrospinning process. In the higher energy spectral region, a weak band near 2176 cm-1, which can be attributed to C≡N stretching of nitrile groups, appears in spectra of both the Reputex™ 20 solution (Figure 3D) and functionalized PVA nanoweb (Figure 3B, inset). The band provides additional evidence for functionalization of PVA nanoweb. Near 3300 cm-1, amine N-H stretching vibrations are expected. For the Reputex™ 20 solution, the broad O-H stretching features for water in the solution likely obscure the N-H stretching vibrations. In the functionalized PVA nanoweb, the O-H stretches of the PVA can similarly interfere. It is notable, however, that the O-H stretching band centered at 3329 cm-1 in the native PVA (Figure 3A) is downshifted in the functionalized PVA, possibly reflecting the effects of hydrogen bonding interactions with Reputex™ 20 N-H groups.

It is worth pointing out the sharp k at 1143 cm-1 in the spectrum of functionalized PVA nanoweb (Figure 2B). The intensity and sharpness of the band are characteristic of increasing PVA crystallinity [24-26]. Following heat treatment (Figure 2C), the 1143 cm-1 band sharpens further and grows in intensity, becoming even more distinct. Such heat treatment is understood to promote the formation of crystalline domains within a PVA matrix [24-26]. Growth of the feature following the thermal treatment suggests these regions become a greater fraction of the polymer structure. The Reputex™ 20 signature band at 1555 cm-1 band is also present in Figure 2C, indicating the incorporated Reputex™ 20 remains stable through the thermal treatment. Figure 3C shows the higher energy spectral region for this sample. Interestingly, the nitrile feature near 2176 cm-1 is shifted to lower energy (Figure 3C, inset), which may reflect changes in the PVA-Reputex

interaction induced by the thermal treatment. A downshift in the -C≡N stretching of nitrile groups can indicate non-covalent interactions that affect the π -electrons in the bond [28].

Antimicrobial Activity of Reputex™ 20 Functionalized PVA Nanowebs

The results on antibacterial activity of functionalized PVA nanowebs are presented in Figure 4.

FIGURE 4. Antimicrobial Activity of Reputex™ 20

Functionalized PVA Nanowebs. (A) Activity of Functionalized PVA Nanowebs on S. aureus. (B) Activity of Functionalized PVA Nanowebs on E. coli. (C) Activity of Functionalized/Heat Cross-linked PVA Nanowebs on S. aureus. (D) Activity of Functionalized/Heat Cross-linked Nanowebs on E. coli.

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with the negatively charged acidic phospholipids, phosphatidylglycerol (PG) and di phosphatidylglycerol (DPG). These electrostatic interactions result in the formation of PG/PHMB and DPG/PHMB domains eventually compromising the permeability of the phospholipid bilayer. The length of the polymer chain was observed to play a crucial role in determining the activity of PHMBs. Longer the polymer chains, larger the PG/PHMB and DPG/PHMB domains and hence greater the activity [29-31].

One of the biggest limitations of PVA nanowebs that hinder their application in biomedical sector is their water solubility. PVA is a hydrophilic polymer [22] and hence PVA nanowebs are soluble in water. Despite the number of chemical cross-linking treatments available to render electrospun PVA nanowebs insoluble in water [32-34], heat cross-linking [22] has emerged as a viable environmental friendly option that eradicates the use of harmful organic solvents. Hence, functionalized PVA nanowebs have been heat cross-linked to improve their stability in aqueous conditions. Figures 4C and 4D indicate that functionalized PVA nanowebs have retained their antimicrobial activity even after heat crosslinking (H1, H2 and H3 represent functionalized/heat cross-linked PVA nanowebs in Figure 4D. R1, R2 and R3 represent functionalized PVA nanowebs). More importantly, the size of the zones of inhibition for S. aureus and E. coli was found out to be 16 mm and 14mm (n=3), respectively. The active ingredient in Reputex™ 20 is heat stable and non-volatile [21]. The heat stability of active ingredient in Reputex™ 20 also is supported by the FTIR measurements, as the Reputex™ 20 signature band at 1555 cm-1 was observed even after heat cross-linking (Figure 2C).

Breathability of Reputex™ 20 Functionalized PVA Nanowebs

Breathability of wound dressings is an important consideration in their development as it governs the loss of water from an open and wet wound. A wound dressing material is required to prevent not only the excessive dehydration of the wound, but also the build-up of wound exudates. Breathability of normal skin was found out to be 204 g/m2/day. In the case of an injured skin, it was observed to be in the range of 279-5138 g/m2/day depending on the severity of injury. Hence, studies have determined that the breathability of wound dressings should be in the range of 2000-2500 g/m2/day for them to function appropriately [8, 35]. In the present study, breathability of functionalized PVA nanowebs was found out to be 880.1 g/m2/day (n=4, se=4.24). Our

previous studies have indicated that breathability of native PVA nanowebs electrospun under similar conditions is 1209.5 g/m2/day [24]. Hence, it can be inferred that the functionalization of PVA nanowebs with Reputex™ 20 has resulted in a decrease in their breathability.

The decrease in breathability of functionalized PVA nanowebs can possibly be explained by the FTIR spectra. As discussed in Section 3.1, growth of the 1143 cm-1 peak in the functionalized nanowebs may be the result of intermolecular interactions between amine and imine groups on Reputex™ 20 and O-H groups in the PVA polymer. By tying up the polar functional groups, these interactions make them less available to interact with water, effectively lowering the breathability of functionalized PVA nanowebs. More importantly, the decrease in breathability could also be attributed to the composition of Reputex™ 20, which is 20% active ingredient and may contain other inert ingredients [21]. Aside from water, any additional inert ingredient in Reputex™ 20 may potentially interfere with the water vapor permeability characteristics of functionalized nanowebs as breathability of a substrate is strongly influenced by surface functional groups [36].

Tensile Properties of Reputex™ 20 Functionalized PVA Nanowebs

The tensile properties of functionalized and functionalized/heat cross-linked PVA nanowebs are depicted in Figure 5.

FIGURE 5. Tensile Properties of Functionalized and Heat Cross-linked/Functionalized PVA nanowebs, cross bars represent standard error of means, n=5, *p<0.05, and n.s., not significant.

As is evident from Figure 5, the process of heat crosslinking has resulted in a significant increase in the maximum load characteristics of functionalized PVA nanowebs (p<0.05). No significant difference in the extension at maximum load and the modulus of

*

n.s

.

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functionalized PVA nanowebs was observed after heat cross-linking. Hence, it can be inferred that the process of heat cross-linking has not compromised the tensile properties and antimicrobial activity of functionalized PVA nanowebs.

CONCLUSION

Antimicrobial nanowebs were fabricated by functionalizing PVA nanowebs with a commercially available microbiocidal solution Reputex™ 20. The active ingredient in Reputex™ 20 is PHMB, a safe antiseptic. Functionalized PVA nanowebs demonstrated excellent antimicrobial activity. Breathability of functionalized PVA nanowebs was compromised due to the inert ingredients present in Reputex™ 20. Functionalized PVA nanowebs were heat cross-linked to enhance their stability in aqueous conditions. The process of heat cross-linking compromised neither the antimicrobial activity nor the tensile properties of functionalized nanowebs. Nanowebs developed from biocompatible polymers and functionalized with safe antiseptics could find potential applications in wound dressings.

ACKNOWLEDGMENT

Dr. Seshadri Ramkumar gratefully acknowledges the financial support from The CH Foundation, Lubbock. Also, the authors gratefully acknowledge Dr. Bo Zhao, College of Arts and Sciences, Texas Tech University for all her help with SEM imaging of nanowebs. Thanks to The University A&S EOX Imaging Facility, Texas Tech University, instrument funded by NSF MRI 04-511.

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AUTHORS’ ADDRESSES Uday Turaga, PhD Vinitkumar Singh, PhD Anna Gibson, PhD Steven Presley, PhD Ernest Smith, PhD Ronald J Kendall, PhD Seshadri S. Ramkumar, PhD Texas Tech University - TIEHH P.O. Box 41163

Lubbock, TX 79409-1163 UNITED STATES

Shahrima Maharubin, MS Carol Korzeniewski, PhD Texas Tech University

Department of Chemistry and Biochemistry Lubbock TX 79409-1061

Figure

FIGURE 2. ATR Spectra of Reputex™ 20 and PVA Nanowebs in  the low energy region of 800-1700 cm-1
Figure 4Dfunctionalized/heat cross-linked PVA nanowebs in . R1, R2 and R3 represent functionalized PVA nanowebs)

References

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