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. 2021 Mar 31;73(3):423–431. doi: 10.1007/s10616-021-00467-2

Antimicrobial and wound healing properties of cotton fabrics functionalized with oil‐in‐water emulsions containing Pinus brutia bark extract and Pycnogenol® for biomedical applications

Pelin Secim-Karakaya 1,✉, Pelin Saglam-Metiner 2, Ozlem Yesil-Celiktas 2,✉
PMCID: PMC8167011  PMID: 34149175

Abstract

Topical formulations containing 1–2% of Pinus brutia bark extract and Pycnogenol® have been prepared to investigate the effect of flavonoids on the stability of O/W emulsions, which were subjected to physicochemical and thermal stability tests. The formulations have been applied to cotton fabrics to evaluate antimicrobial properties against Staphylococcus aureus, Escherichia coli, Candida albicans and Aspergillus brasiliensis. Furthermore, prepared cotton fabrics have been tested on keratinocytes seeded in cell culture inserts for wound healing. Results of freeze thaw cycle test indicated enhanced thermo-stability with no major changes in pH and viscosity, likewise the results of centrifugation assay. However, the addition of Pycnogenol® has tremendously decreased the viscosity of the topical formulation (10,900 cp.). In terms of antimicrobial activity, 2% P. brutia treated cotton fabrics decreased the proliferation of Aspergillus brasiliensis 78.8%, which were more effective than that of Pycnogenol® formulation (62.9%). As for wound healing, 2% P. brutia treated cotton fabrics increased HaCaT keratinocyte cell proliferation and accelerated the cell-free gap closure compared to Pycnogenol® and untreated control groups. The obtained results indicate the utilization of pine bark for developing an eco-friendly natural antifungal finish for medical textiles.

Keywords: Topical formulation, Wound healing, Cell proliferation, Antifungal, Pinus brutia, Pycnogenol®

Introduction

The research and development efforts in biomedical textiles have shifted towards functionalization of fabrics to design products with advanced properties such as ultraviolet protection (Salama et al. 2015), antibacterial activity (Gressier et al. 2019) and flame retardancy (Dong et al. 2018). With the advances in emulsion technology, topical formulations have been applied to textiles for biomedical purposes. The ultimate aim in formulating a topical formulation is to provide high protection to the skin, which is susceptible to oxidative stress (Wang et al. 2019). Therefore, researchers have focused on the potential use of some secondary metabolites of higher plants as free radical scavengers to prevent oxidative skin damage (Casagrande et al. 2006), and their topical applications have been of considerable interest (Reszko et al. 2010). Among the natural compounds, anthocyanins, flavonoids, such as catechin, epicatechin and taxifolin draw attention due to their broad biological activities. For instance, catechin, epicatechin and taxifolin have been reported to exert antioxidant (Xu et al. 2021; Santos et al. 2021) and anticancer activities (Kuban-Jankowska et al. 2020; Li et al. 2019). Furthermore, neuroprotective effect of catechin has been highlighted in a study, suggesting that administration of catechin might be a potential adjuvant therapy for the amelioration of DOX-induced cognitive impairment, which may improve the quality of life of cancer survivors (Cheruku et al. 2018). These compounds are reported in some natural resources such as green tea (Er and Dikmen, 2017), pine bark (Shen et al. 2010; Yesil-Celiktas et al. 2009a), black carrot (Yesil-Celiktas et al. 2017) and blueberry (Kazan et al. 2017).

The most common commercially available pine bark extract is Pycnogenol®, a standardised extract of French maritime pine bark (Pinus maritima), which is probably the most studied phenolic tree extract containing proanthocyanidins. Pycnogenol® and bark extracts from various pine species have been reported to accelerate wound healing (Cetin et al. 2013), reduce scar formation (Blazso et al. 2004), exhibit anti-inflammatory activity (Lichota et al. 2019; Ince et al. 2009), have cardiovascular benefits, the ability to enhance microcirculation by increasing capillary permeability, strong free radical scavenging activity (Yesil-Celiktas 2009) against reactive oxygen and nitrogen species, the potential to regenerate the ascorbyl radical and to protect endogenous vitamin E and glutathione from oxidative stress. P. brutia extracts were reported to contain procyanidins, (+)-catechin and considerably high amounts of taxifolin (Yesil-Celiktas et al. 2009a).

The present study was designed to evaluate the physicochemical and thermo-stability of topical formulations enriched with Pycnogenol® and Pinus brutia bark extracts. Then cotton fabrics treated with topical formulations were investigated in terms of antimicrobial and wound healing properties using an in vitro model with human skin keratinocytes for medical applications.

Materials and methods

Plant material and Pycnogenol®

Pinus brutia Ten. has spread out in eastern Mediterranean countries and is distributed widely in several regions in Turkey. Pine bark specimen (P. brutia) was collected from Izmir-Deliomer (N: 38° 10′ 17.0″, E: 27° 03′ 46.7″, altitude: 120 m) in August 2006. The specimen was dried at room temperature, ground by using a conventional grinder, passed through a 1 mm mesh and stored at + 4 °C. Voucher specimen is kept at IZEF Herbarium (IZEF 5762). Pycnogenol® was gently donated by Horphag Research Ltd., UK.

Preparation of solvent extracts

About 100 g of ground pine bark were extracted with 1000 mL of ethanol (Merck) for three cycles (about 6 h) using a soxhlet (500 mL) apparatus. The extracts were concentrated to dryness at 60 °C in vacuum by Laborato 4001, Heidolph rotary evaporator and subsequently lyophilized.

Topical O/W formulations

Topical O/W formulations were prepared by dissolving oil phase (18%) at 70–80 °C. Oil and water phases were mixed together at the same temperature without vortexing to avoid the entrapment of air. After cooling to 30–40 °C, 1–2% P. brutia bark extract and 2% Pycnogenol® were added to the O/W emulsions, totaling up to four different formulations including control.

Physicochemical properties of topical O/W formulations

The viscosities of the topical O/W formulations were measured using a Brookfield LVDV-II + Viscosimeter at 10 rpm and pH at 20 °C with a Forlab pHmeter (Carlo Erba).

Stability tests of topical O/W formulations

Freeze thaw cycle test

The topical formulations were subjected to three freeze/thaw cycles, each with temperature swinging from 48 °C, to room temperature, to − 15 °C and then back to room temperature, with a duration of 24 h at each temperature. A number of rheological tests were performed with samples by measuring viscosity at 10 rpm and pH at 20 °C after each cycle.

Centrifugation assay

Cream formulations were centrifuged at 3000 rpm for 30 min. Phase separation rates were reported as percentages referred to the graduated measuring tube (10 mL), i.e. 100 = stable; 0 = total instability (Anchisi et al. 2001).

Functionalization of cotton fabrics

Cotton fabrics (10 × 10 cm) have been treated with three different formulations at a ratio of 1 g fabric:1 g formulation. Subsequently, the fabrics were dried at room temperature and sterilized.

Antimicrobial activity of treated cotton fabrics

The antimicrobial activities of treated fabrics were quantitatively evaluated against Staphylococcus aureus, Escherichia coli, Candida albicans and Aspergillus brasiliensis according to the test method AATCC 100 (AATCC 100 2014) (Fig. 1). The cotton fabrics were sterilized in an autoclave. Counts of 105 cfu (colony-forming unit)/mL suspensions were prepared and mixed homogeneously. Then 1 mL of suspension was transferred to cotton fabrics and incubated at 37 °C for 18–24 h. Subsequently, 100 mL of sterile neutralizing agent was transferred into the vial. After 5 min, serial dilutions were prepared by mixing homogeneously. 1 mL of prepared dilutions were transferred to petri dishes and 15 mL of Malt Extract Agar is added. After incubation at 37 °C for 48 h, the colonies were counted. An untreated cotton fabric was used to calculate the recovery. The % reductions of bacteria and fungi on the fabrics were calculated using the following formula:

R=100B-A/B

R is percent reduction, A is the number of microorganisms recovered from the inoculated treated test specimen incubated over desired contact period, whereas B is the number of bacteria recovered from the inoculated treated test specimen immediately after inoculation (at “0” contact time).

Fig. 1.

Fig. 1

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A schematic depicting the assessment of antimicrobial activities of treated cotton fabrics

Wound healing properties of treated cotton fabrics

A human skin keratinocyte HaCaT cell line was obtained from American Cell Culture Collection (ATCC, Mannassas, VA, USA). Cells were maintained in Dulbecco's Modified Eagle Medium (DMEM) supplemented with high glucose (4500 mg/L), 10% fetal bovine serum, 2 mM l-glutamine, 100 U/mL penicillin/100 μg/mL streptomycin and 0.1% 10 mg/mL gentamicin. Cells were cultured in 75-cm2 cell culture flasks at 37 °C in a 5% CO2 atmosphere, received fresh medium every 2 days and subcultured every 5–7 days. All cell culture reagents were supplied by Sigma-Aldrich.

In order to determine wound healing properties, 2% P. brutia bark extract and 2% Pycnogenol formulation treated cotton fabrics were cultured on HaCaT cells, whereas only growth medium was added to the control group. The migration test was performed using Culture-Insert 2 Well in µ-Dish 35 mm (Ibidi, 81176, Germany). For this, cells were seeded into the culture-insert 2 well (5 × 104 cells/70 µL/each well) and incubated for 24 h in growth medium until 95–100% cell density was reached. After cell attachment and proliferation, the biocompatible silicone gasket was removed and a cell-free gap was created in which the cell migration could be visualized. Then, the culture-dish was filled with 3 mL growth medium and treated cotton fabrics were covered over cells. The time-dependent cell migration and wound healing on a cell-free gap was monitored under inverted microscope with × 10 magnification (Motic AE31E Trinocular, Spain) every 3 h (the fabrics were taken out for monitoring, and then covered again) for about 24 h, and open areas were measured using Moticam 1080 camera software.

Statistical analysis

Statistical analyses of the data were performed by Student’s t-test and one-way ANOVA with Tukey’s Multiple Comparison test with a confidence interval of ± 95% and p < 0.05 using Prism 5.0 (Graphpad, San Diego, CA, USA) programme. All experiments were carried out as 3 replicates. Data are presented as mean values ± SEM (standard error of the mean).

Results and discussion

Physicochemical properties and stabilities of topical O/W formulations

The physicochemical properties of the control without the incorporation of extract and with the incorporation of P. brutia bark extract and Pycnogenol® were evaluated based on pH (Table 1), viscosity (Table 2) values and data of the centrifugation assay, whereas freeze thaw cycle test was used to study the thermo-stability. The mentioned parameters were screened throughout the freeze thaw cycle test and at the end of 12 months of storage. The results of the freeze thaw cycle test indicated enhanced thermo-stability properties with no major changes in pH and viscosity, likewise the results of centrifugation assay, where no phase separations were observed. The optimum pH range is reported to be around 5.5 for topical formulations to ensure effective application with less skin irritation (Elmataeeshy et al. 2018). The pH of developed formulations were between 6.10 and 5.54, which is suitable to the human skin (Lee et al. 2016). However, the addition of Pycnogenol® has tremendously decreased the viscosity of the topical formulation (10,900 cp), whereas P. brutia bark extract incorporated formulation showed a similar rheological behavior to the control.

Table 1.

The pH values (± SEM) of topical O/W formulations during freeze thaw cycle test and at the end of 12 months of storage

Initial Cycle 1 Cycle 2 Cycle 3 12 months
Control 6.03 ± 0.00 6.00 ± 0.00 6.03 ± 0.00 6.02 ± 0.00 5.97 ± 0.04
%1 P. brutia 5.91 ± 0.00 5.86 ± 0.04 5.85 ± 0.01 5.83 ± 0.00 5.80 ± 0.06
%2 P. brutia 5.80 ± 0.00 5.76 ± 0.01 5.71 ± 0.01 5.71 ± 0.00 5.54 ± 0.03
%2 Pycnogenol 6.10 ± 0.06 5.95 ± 0.04 5.94 ± 0.06 5.91 ± 0.06 5.74 ± 0.01
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Table 2.

The viscosities of topical O/W formulations during freeze thaw cycle test and after 12 months of storage

Initial Cycle 1 Cycle 2 Cycle 3 12 months
Control 49900 ± 0.10 56600 ± 0.13 57660 ± 0.11 57560 ± 0.10 59120 ± 0.14
%1 P. brutia 57480 ± 0.15 57200 ± 0.11 58580 ± 0.14 58620 ± 0.13 55180 ± 0.15
%2 P. brutia 58240 ± 0.13 57980 ± 0.14 58000 ± 0.12 58260 ± 0.16 57540 ± 0.14
%2 Pycnogenol 9560 ± 0.12 8350 ± 0.11 9633 ± 0.14 11116 ± 0.15 10613 ± 0.14
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Antimicrobial activity of treated cotton fabrics

The antimicrobial activities of cotton fabrics tretaed with topical O/W formulations have been tested against bacteria and fungi (Fig. 2). Formulations with both P.brutia bark extract and Pycnogenol have not exerted any activity against E. coli and C. albicans, whereas a moderate activity (p < 0.001) of 2% P. brutia bark extract was noted against S. aureus. However, 84.2% and 78.8% reduction in A. brasiliensis was observed in cotton fabrics treated with topical formulations containing 1% and 2% P. brutia bark extract (p > 0.05), respectively. The sample containing 2% Pycnogenol formulation, exhibited the lowest reduction as 62.9% (p < 0.01 and p < 0.05). Although Pycnogenol has antifungal property, better results were obtained by using 1% and 2% Pinus brutia formulations. Taxifolin, a polyphenol present in various pine bark extracts was reported to be effective in fungal infections (Shevelev et al. 2020). Therefore, this finding might be associated with the amount of taxifolin content of Pinus brutia, which is greater than that of the Pycnogenol. Indeed, Romani et al. (2006) reported polyphenol composition of Pycnogenol, where the amount of taxifolin was determined to be 33.1 mg g−1, whereas P. brutia extract showed a much higher value (186 mg g−1) in an another study (Yesil-Celiktas et al. 2009b). Polyphenols inhibit the oxidation reaction of free radicals and prevent growth of microbes as well (Qudsia et al. 2010).

Fig. 2.

Fig. 2

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The reduction in microorganism counts (% ± SEM) of cotton fabrics treated with topical O/W formulations against a S. aureus, b E. coli, c C. albicans and d A. brasiliensis (one-way ANOVA Tukey’s Multiple Comparison test, ns:p > 0.05 non-significant, *:p < 0.05, **:p < 0.01 and ***:p < 0.001)

Wound healing properties of treated cotton fabrics

Wound healing is a natural process consisting of multisystemic molecular responses and aims to repair and restore the functional status of injured living tissues. This phenomenon consists of three major consecutive phases (Lopez et al. 2018). Inflammation phase eliminates wound debris, releases growth factors and pro-inflammatory cytokines such as TNF-α (Shah and Amini-Nik 2017). Followed by proliferation phase, which is characterized by reepithelialization, neovascularization and granulation tissue formation that includes fibroblast migration and collagen synthesis (Er and Dikmen 2017; Coger et al. 2019). Finally, remodeling phase is the transformation phase into mature and stronger type I collagen (Landen et al. 2016). The natural compounds have been used in traditional medicine for wound healing due to less toxicity, fewer side effects, minimal costs, effective anti-inflammatory, antioxidant and antimicrobial activity, compared with conventional medicines (Anlas et al. 2019). In this respect, it has been reported in various studies that P. brutia extracts possess these mentioned properties (Ince et al. 2009; Yesil-Celiktas, 2009; Yesil-Celiktas et al. 2009a; Lichota et al. 2019). For this, the wound healing proporties of 2% P. brutia bark extract as the most effective antimicrobial formulation in this study and commercial 2% Pycnogenol formulation treated cotton fabrics have been tested on HaCaT cells. The time-dependent inverted microscope images of HaCaT cell-free gaps are shown in Fig. 3. The open area graphs and a schematic representation of the applied processes are depicted in Fig. 4a and b, respectively. The cell-free gap areas of each groups were approximately between 250.000 and 300.000 µm2, similar to the control at 0 h. Referring to the inflammation phase of wound healing process, the cells treated with formulatin soaked cotton fabric groups were observed to adjust to the conditions, while the cells in the control group slowly started to migrate at the 6th hour. The 12th hour has been an important time slot for proliferation phase as the cells in P. brutia formulation group exhibited a rapid attack for migration due to anti-inflammatory activity, while the control group progressed in its own path. Despite the attacks of the cells in Pycnogenol formulation group during the wound closure process at 18th hours, it was observed that the P. brutia formulation treated cells crawled, leading to an almost complete closure of the cell-free gap in the 21st hours at first, even before the control group. Finally, complete gap closure was observed for control and P. brutia formulation groups at the 24th hour, while an open area of about 48.000 µm2 remained in Pycnogenol formulation group. Cotton fabrics treated with O/W formulation containing 2% P. brutia bark extract accelerated the wound healing process due to an enhanced cell-free gap closure of HaCaT keratinocyte cells compared to cotton fabrics treated with O/W formulation containing 2% Pycnogenol® and untreated control group. In a recent study, (+)-catechin was reported to achieve the highest cell migration using human dermal fibroblasts, resulting in 100% wound closure at day 2 (Chaniad et al. 2020). Indeed, the amount of (+)-catechin in P. brutia extract used in this study is 70.4 mg/g, whereas only 1.5 mg/g in Pycnogenol® (Yesil-Celiktas et al. 2009b). Suntar et al. (2012) reported that Pinus species have been used for wound healing due to anti-hyaluronidase activity that promotes proliferation and migration of fibroblasts and endothelial cells into the wound site, as well as against rheumatic pain. In another study, a high wound healing activity of P. brutia bark extract in an incision wound model in rats with increased vascularization and a decrease in necrotic area (Cetin et al. 2013), as was confirmed with our in vitro wound healing model.

Fig. 3.

Fig. 3

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The time-dependent inverted microscope images of HaCaT cell-free gaps after treatment with 2% P. brutia bark extract and 2% Pycnogenol formulation treated cotton fabrics and growth medium control (Motic AE31E, 10X, bar scale at 100 μm)

Fig. 4.

Fig. 4

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a The time-dependent open area (µm2) graphs of HaCaT cell-free gaps after treatment cotton fabrics containing O/W formulations with 2% P. brutia bark extract, 2% Pycnogenol and control only treated with growth medium, b Representetive image of wound healing process of formulation treated cotton fabrics on HaCaT cell-free gaps

Conclusion

Bacteria and fungi can easily grow in textile materials used in hospitals and social areas and are harmful to human health. For protection purposes, medical textiles have been playing an important role in the healthcare industry (Said et al. 2021). For this reason, new antimicrobial and antifungal materials have drawn attention. This study was aimed at functionalization of cotton fabrics by treating with topical O/W formulations containing P. brutia bark extract and a commercial bark extract. Functionalization was achieved by adding features of antimicrobial and wound healing properties. In terms of antimicrobial activity, the proliferation of Aspergillus brasiliensis was decreased by 78.8%, when administered with 2% P. brutia treated cotton fabrics, whereas only 62.9% reduction was achieved with Pycnogenol® formulation. As for wound healing, 2% P. brutia treated cotton fabrics increased HaCaT keratinocyte cell proliferation and accelerated the cell-free gap closure compared to Pycnogenol® and untreated control groups. Thus, cotton fabrics functionalized with O/W formulation containing 2% P. brutia bark extract can be a viable alternative to synthetic antimicrobial agents used in medical textiles. Considering production at industrial scale, utilization of pine bark as a forestry waste can reduce the costs and provide sustainability, thereby offering potential for commercialization.

Acknowledgements

The financial support provided by the Research fund of Ege University (15MUH051) is highly appreciated.

Data availability

All data generated or analysed during this study are included in this published article.

Declarations

Conflict of interest

The authors declare no conflicts of interest.

Footnotes

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Contributor Information

Pelin Secim-Karakaya, Email: pelinsecim@mail.ege.edu.tr.

Ozlem Yesil-Celiktas, Email: ozlem.yesil.celiktas@ege.edu.tr.

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