Natural Flavonoid-Functionalized Silk Fiber Presenting Antibacterial

Research Article Cite This: ACS Sustainable Chem. Eng. 2017, 5, 10518-10526

pubs.acs.org/journal/ascecg

Natural Flavonoid-Functionalized Silk Fiber Presenting Antibacterial, Antioxidant, and UV Protection Performance Yuyang Zhou and Ren-Cheng Tang* National Engineering Laboratory for Modern Silk, College of Textile and Clothing Engineering, Soochow University, 199 Renai Road, Suzhou 215123, China S Supporting Information *

ABSTRACT: Natural bioactive compounds as promising alternatives to synthetic finishing agents have recently gained increasing attention in the textile industry due to their eco-friendliness, low irritation, and biocompatibility. The present study reports a sustainable approach for preparing antibacterial, antioxidant, and UV-protective silk fiber using two natural flavonoids (quercetin and rutin) by an adsorption technique. The adsorption kinetics and isotherms of the two flavonoids were investigated, and their functionalities and the washing durability of their functionalities were discussed. The equilibrium adsorption isotherms fitted well to the Langmuir and Freundlich adsorption models, demonstrating that ion−ion interactions, hydrogen bonding, and van der Waals forces play major roles in the adsorption of quercetin and rutin on silk. The adsorption isotherm parameters of quercetin and rutin had a decisive effect on their adsorption kinetics, which fit well to the pseudo-second-order kinetic equation. Quercetin exhibited higher initial adsorption rate, shorter half adsorption time, and higher adsorption capability than those of rutin due to its higher affinity constant. Quercetin also imparted better antioxidant, antibacterial, and UV protection performance to silk than rutin at the same initial application concentration and provided better washing durability of functionalities. This study demonstrates that quercetin and rutin can be employed as promising multifunctional agents for the chemical processing of silk materials. KEYWORDS: Flavonoids, Adsorption, Silk, Antibacterial activity, Antioxidant activity, UV protection

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INTRODUCTION With the enhancement of environmental consciousness, bioactive extracts from plants as renewable and sustainable bioresource products have drawn increasing attention in the textile industry owing to their nontoxicity, degradability, and eco-friendliness.1 Many studies have also confirmed that natural bioactive extracts possess a diversity of functionalities such as antibacterial activity, antioxidant activity, anti-inflammatory activity, and so forth, which have promising prospects in the development of hygiene-related and medical textiles.2,3 In addition, the application of natural functional colors in textiles combines dyeing and finishing processes,4 which can be regarded as an efficient technique with low consumption of water and energy. Silk, because of its several outstanding properties including smooth and lustrous appearance, soft handle, hygroscopicity, and wearing comfortableness, has been regarded as a luxurious textile for thousands of years. Furthermore, the superior mechanical performance and bioavailability of silk enable it to © 2017 American Chemical Society

be an appropriate material that can be applied as a biomedical textile and as a scaffold for tissue engineering, surgical threads, and wound dressings.5 However, several obvious drawbacks of silk fiber, for instance, low antimicrobial and antioxidant activity, poor UV protection ability, and deterioration, greatly impede its practical application.5,6 Thus, efforts should be made to overcome these deficiencies and to provide silk with specific functionalities. In recent investigations, the antibacterial functionalization of silk by inorganic nanomaterials and natural bioactive extracts has become a hot issue.1−8 Flavonoids, accounting for the largest proportion in the family of natural bioactive extracts, are known to be produced by plants to defend against microbial invasions. Moreover, it has already been known for decades that flavonoids have potent antioxidant activity, which is able to reduce the amount of Received: July 24, 2017 Revised: October 6, 2017 Published: October 12, 2017 10518

DOI: 10.1021/acssuschemeng.7b02513 ACS Sustainable Chem. Eng. 2017, 5, 10518−10526

Research Article

ACS Sustainable Chemistry & Engineering

provided by Shanghai Zhengzhang Laundering and Dyeing Co. Ltd., China. Nutrient agar and nutrient broth were used in the antibacterial test and purchased from Sinopharm Chemical Reagent Co. Ltd., China and Shanghai Sincere Biotech Co. Ltd., China, respectively. Adsorption of Quercetin and Rutin. All of the treatment processes were implemented in conical flasks, which were shaken in an oscillated dyeing machine. A liquor ratio (liquor volume to fabric weight) of 50:1 was used. Citric acid-disodium hydrogen phosphate buffer was used for the adjustment of pH values. At the end of each treatment, the treated fabrics were rinsed with distilled water and then allowed to dry in open air. pH Dependence of Adsorption. In this section, 3% on the weight of fabric (owf) quercetin and rutin were used in the silk treatment with a pH range from 2.7 to 7.1. The temperature of the treatment bath was raised from 30 to 90 °C at a rate of 2 °C/min, and the treatment was carried out at 90 °C for 60 min. Adsorption Kinetics. The solutions containing 3% owf quercetin or rutin were used, and their pH values were adjusted to 2.75. The fabrics were treated at 90 °C for different time periods. Equilibrium Adsorption Isotherms. The explorations of adsorption isotherms for quercetin and rutin on silk were conducted at pH 2.75 and 90 °C using a series of flavonoid concentrations from 1 to 10% owf. According to the study of adsorption kinetics, the adsorption reached an equilibrium state in 90 min. Thus, the fabrics were treated for 90 min in this section. Building-Up Properties. A series of of quercetin and rutin concentrations (1−10% owf) were used. The pH values of the solutions were adjusted to 2.75. The temperature of the treatment bath was raised from 30 to 90 °C at a rate of 2 °C/min, and the treatment was continued at 90 °C for 60 min. The as-prepared samples were employed for the evaluation of functionalities. Measurements. Uptake of Quercetin and Rutin by Silk. The UV/vis absorption spectra were obtained by a Shimadzu UV-1800 UV/vis spectrophotometer (Shimadzu Co., Japan). Taking the low solubility of quercetin and rutin into account, their solutions were diluted 50-times with 80% ethanol prior to the measurement. The determination of exhaustion percentages of quercetin (λmax = 364 nm) and rutin (λmax = 351 nm) was based on the previously established standard working curves according to eq 1, where C0 and C1 are the concentrations of quercetin and rutin before and after adsorption, respectively. The concentrations of quercetin and rutin on silk were determined according to the difference in the concentrations of quercetin and rutin in solution before and after adsorption and the weight of the dried fabric.

active and harmful substances such as reactive oxygen free radicals through radical scavenging.9 In recent years, a small amount of available literature has been focused on the functionalization of textiles by flavonoids and the interactions between flavonoids and fiber materials.6,10,11 Altıok et al.10 innovatively adopted silk fibroin as an adsorbent for the recycling of the polyphenols including several flavonoids from the extracts of olive leaf, indicating the occurrence of the interactions between silk and flavonoids. Flavonoids were ascertained to be efficient for improving the UV protection ability of cellulosic fabrics.11 In our previous work,6 baicalin, which has one carboxyl group but no catechol moiety in the Bring, was successfully used to impart antibacterial, antioxidant, and UV protection functions to silk fiber, and the electrostatic interaction operating between the carboxyl group of baicalin and the amino group of silk was clarified. Quercetin and rutin (Figure 1) belong to the bioactive flavonoid compounds, existing widely in different sorts of fruits

Figure 1. Chemical structures of quercetin and rutin.

and vegetable tissues.12,13 In fact, the critical difference between their chemical structures is that rutin contains one disaccharide moiety at the C-3 position of the C-ring. It is widely known that glycosyl groups are very common in flavonoids and have been found to be responsible for the hydrophilicity and biological properties.14−17 So far, few reports have focused on the fabrication of multifunctional silk with flavonoids with different chemical structures. Furthermore, the relationships among the adsorption behaviors of flavonoids, functions of silk imparted by flavonoids, and chemical structures of flavonoids also remain to be explored. Both quercetin and rutin are faintly colored flavonoids; thus, they are very appropriate for the functional modification of silk due to the fact that they probably exert little influence on the color of silk materials. The aim of the present research was to prepare bioactive and UV-protective silk materials by the introduction of querectin and rutin. In the present work, the pH dependence of the uptake of quercetin and rutin by silk was explored, the adsorption mechanism and capability of quercetin and rutin on silk were discussed, and the antioxidant activity, antibacterial activity, and UV protection ability of the silk treated with quercetin and rutin were determined. The relations among the structures, adsorption mechanism and capability, and functions of quercetin and rutin were emphasized.

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exhaustion (%) =

C0 − C1 × 100 C0

(1)

Color Characteristics. The color parameters of each sample, which was folded twice, were measured by a Datacolor 600 (Datacolor Technology Co., USA) using D65 illumination and 10° observer. The lightness [L*], redness-greenness value [a*], and yellowness-blueness value [b*] were recorded. The color difference (DE) was determined by eq 2, where the subscripts “untr” and “tr” represent the silk fabrics untreated and treated with quercetin or rutin, respectively. * )2 + (a tr* − a untr * )2 + (btr* − buntr * )2 ]1/2 DE = [(Ltr* − Luntr

(2)

Antioxidant Activity. The antioxidant property of samples was determined by the ABTS radical decolorization assay using spectrophotometric analysis according to the previous method.18 More details regarding the antioxidant activity assessment were shown in our previous work.4,6 Antibacterial Activity. The antibacterial activity of samples was assessed according to GB/T 20944.3−2008. Escherichia coli (E. coli, ATCC 8099) and Staphylococcus aureus (S. aureus, ATCC 6538) were provided by the College of Life Science, Soochow University (China). More details regarding the antibacterial activity assessment were shown in our previous work.4,6 UV Protection Performance. The UV transmittance and UV protection factor (UPF) of samples were determined in a Labsphere

EXPERIMENTAL SECTION

Materials. The silk fabric of crepe de chine (specification code: 12103) was purchased from Suzhou Jiaduoli Silk Apparel Co. Ltd., China. Quercetin (purity 95%) and rutin (purity 95%) were obtained from Xi’an Qing Yue Biotechnology Co. Ltd., China. 2,2′-Azino-bis(3ethylbenzothiazoline-6-sulfonic acid) diammonium salt (ABTS), citric acid, disodium hydrogen phosphate, monopotassium phosphate, and potassium peroxodisulfate were analytical grade reagents. A commercial detergent specially used for the laundering of silk was 10519


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ACS Sustainable Chemistry & Engineering UV-1000F UV transmittance analyzer (Labsphere Inc., USA) according to GB/T 18830-2009. Four different positions of each sample were measured to give an average result. Durability of Functionalities. The functionalities of the silk fabrics subjected to 1, 5, and 10 washing cycles were evaluated. The washing was carried out at 40 °C according to our previously reported method.19 Test of the Desorption of Flavonoids from the Treated Silk. The desorption of flavonoids from the treated silk in water was investigated at 30 °C. The liquor ratio was adjusted to 200:1. The silk fabrics treated with 3% owf flavonoids according to the method described in Building-Up Properties were used in the test. The change of the desorption rate over time was determined by the difference in the concentrations of flavonoids on silk before and after desorption. Surface Morphology, Thermal Stability, and Mechanical Performance. The untreated silk and 2% owf flavonoid-treated silk obtained in Building-Up Properties were used for the investigation of surface morphology, thermal stability, and mechanical performance. The surface morphologies of silk fabrics were observed using a TM3030 tabletop scanning electron microscope (Hitachi High Technologies America Inc., USA). The thermal stability of the fabrics was studied using a TG/DTA 6300 (Seiko Instruments, Inc., Japan) from 50 to 600 °C with a heating rate of 10 °C/min in nitrogen (20 mL/min). The tensile strength of the samples was tested by an Instron 3365 tester (Illinois Tool Works Inc., UK) according to ISO 139341:2013. Prior to the measurement, all the samples were conditioned in standard atmospheric conditions for 24 h. Finally, the average results of six specimens were reported for each sample.

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RESULTS AND DISCUSSION UV−Vis Absorption Spectroscopy. The UV−Vis absorption spectroscopy of quercetin and rutin provides an amount of detail about their water solubility, stability, and spectral features, which are in close relationship with their application properties. Moreover, the multiple hydroxyl groups of flavonoid compounds are inclined to ionize or to be oxidized at different pH values, leading to variation in the physical and chemical behaviors of flavonoids.20,21 Therefore, it is essential to study the UV−Vis absorption spectra of quercetin and rutin at different pH values before their application to silk. As seen in Figure 2, quercetin showed very low absorption intensity below pH 7, and the deposition of the particles was found at the container bottom, indicating its low solubility. The absorption intensity of rutin was higher than that of quercetin at pH 7, which manifests that rutin has better solubility than quercetin as a result of the presence of a hydrophilic glycosidic moiety in its chemical structure.17,22 When the pH value increased above pH 7, the absorbance of quercetin and rutin solutions became higher, less deposition was observed at the bottom of the container, and the color of the solution also changed. These phenomena are associated with the deprotonation of hydroxyl groups in their structures at both the 7 and 4′ positions.23−25 Additionally, two major absorption bands (bands I and II) were observed in the UV−Vis absorption spectra of quercetin and rutin.26 Band I in the 300−400 nm range represents the absorption of the cinnamoyl system (Band C-rings), whereas band II in the 240−280 nm range is attributed to the benzoyl system (A- and C-rings). When the pH was increased to 9, a new peak at a longer wavelength (about 395 nm) appeared. Then, the new peak underwent a red shift as the pH further increased. These complex variations in basic conditions indicate that the species at high pH are not just a consequence of the deprotonation of hydroxyl groups in flavonoids.27 Taking the unstability of flavonoids in basic conditions into consideration, quercetin and rutin were applied in acidic conditions in the following experiments.

Figure 2. UV−Vis absorption spectra of quercetin (a) and rutin (b) in water at different pH values (concentration: 0.01 g/L).

Adsorption Properties. pH Dependence of Adsorption. The pH value can significantly influence the uptake of flavonoids by silk owing to the fact that the pH can change the ionization extent of flavonoids and the net charge of silk fiber. In addition, the pH value of solution can also lead to color changes of quercetin and rutin according to the aforementioned results. As shown in Figure 3a, the uptake of quercetin by silk had almost no change in the pH range of 2.8 to 5.1 and then was reduced dramatically. Additionally, quercetin showed much better adsorption capacity on silk than rutin, which can be explained by the fact that rutin has better water solubility than quercetin as it contains the hydrophilic glycosidic moiety, leading to its great tendency toward distribution in water. The color variations of silk fabrics induced by treatment of quercetin and rutin in a pH range of 2.75−7.08 are depicted in Figure 3b. The silk fabrics treated with quercetin displayed more yellow appearance with high b* values than those treated with rutin. However, the silk fabrics treated with rutin at different pH values displayed marginal color variations. These phenomena are consistent with the color changes of quercetin and rutin in water (Figure 2). Considering the high utilization of quercetin and rutin, pH 2.75 was used in the following studies. Adsorption Kinetics. The adsorption kinetics, which play a significant role during the treatment process, can provide very useful information in the design of adsorption systems. In this work, the adsorption rates of quercetin and rutin were investigated in terms of their adsorption amount (Ct) as a function of time (t). As depicted in Figure 4, the adsorption quantity of quercetin and rutin showed a dramatic increase in the first 30 min. Moreover, quercetin showed a higher adsorption rate than rutin. After approximately 90 min, the 10520


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ACS Sustainable Chemistry & Engineering t1/2 =

1 kCe

(4)

ri = kCe2

(5) 2

The correlation coefficients (R ) of the kinetic model are listed in Table 1. Clearly, the R2 values for the linear plots of Table 1. Adsorption Kinetic Parameters of Quercetin and Rutin for Silk sample

ri (mg g−1 min−1)

t1/2 (min)

k (10−3 g mg−1 min−1)

Ce (mg/g)

R2

quercetin rutin

4.57 0.60

5.68 16.16

6.8 6.4

25.97 9.65

0.9998 0.9992

quercetin and rutin were very high, proving the validity of the pseudo-second-order kinetic equation in describing the adsorption process of quercetin and rutin. Quercetin exhibited higher initial adsorption rate, shorter half adsorption time, and slightly higher adsorption rate constant than rutin. Moreover, quercetin exhibited remarkably higher equilibrium adsorption quantity than rutin. All these results indicate that the affinity of quercetin to silk is higher than that of rutin, which enables us to further explore the equilibrium adsorption behaviors of quercetin and rutin onto silk. Adsorption Isotherms. The equilibrium adsorption isotherms are fundamental in describing the interactions between flavonoids and silk fiber, which can provide the most important information for analyzing and designing the adsorption process. The adsorption isotherms of quercetin and rutin on silk at pH 2.75 are depicted in Figure 5.

Figure 3. pH dependence of the uptake of quercetin and rutin by silk (a) and the color characteristics of the treated silk (b).

Figure 4. Adsorption rates of quercetin and rutin for silk.

Figure 5. Equilibrium adsorption isotherms of quercetin and rutin for silk.

adsorption quantity of quercetin and rutin onto silk became constant, indicating that the adsorption equilibrium was reached. For obtaining the parameters of adsorption kinetics, the pseudo second-order kinetic equation was used to fit the experiment data. Eq 3 represents the pseudo-second-order kinetic equation,28 where k is the adsorption rate constant, and Ct and Ce are the adsorption quantities of flavonoids at time t and at equilibrium, respectively. 1 1 t = + t 2 Ct C kCe (3) e

Langmuir and Freundlich adsorption models were used to describe the experimental isotherm points. For the Langmuir adsorption model, it is assumed that once one solute molecule is adsorbed by one reactive site of adsorbent, further adsorption at this site is impossible. In theory, when all reactive sites of adsorbent are occupied by solute molecules, no further adsorption can occur. The Langmuir isotherm has a pronounced plateau of the complete monolayer fulfillment, which is quite common in chemisorption processes. The expression of Langmuir adsorption is shown in eq 6, where Cf (mg/g) and Cs (mg/L) represent the concentrations of quercetin or rutin on silk and in solution at equilibrium, respectively; S is the saturation concentration of quercetin or rutin on silk, and KL is the Langmuir affinity constant.

If the adsorption complies with the pseudo-second-order kinetic equation, t/Ct would have a linear relationship with t. The slope and intercept of the relative linear regression line were employed to calculate the k and Ce values. In addition, the half adsorption time (t1/2) as well as the initial adsorption rate (ri) were calculated according to eqs 4 and 5, respectively. 10521


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ACS Sustainable Chemistry & Engineering Cf =

SKLCs 1 + SKLCs

Building-Up Property. The building-up ability of plant extracts have received particular attention in the textile industry owing to its close relationship with the utilization and ecoenvironmental impacts, which is related to the chemical structure, affinity to fiber, and adsorption mechanism and capability of natural substances. Thus, the building-up ability of quercetin and rutin on silk were also explored. As shown in Figure 6a, the adsorption amount of quercetin on silk

(6)

The Freundlich isotherm is also a widely accepted adsorption model. This model describes the equilibrium adsorption of solute on the heterogeneous surfaces of adsorbent and thus does not assume a monolayer capacity.29 The Freundlich equation is given as eq 7, where KF is the Freundlich affinity constant and n is an indicator of surface heterogeneity or adsorption intensity. Cf = KFCsn

(7)

The Langmuir and Freundlich adsorption parameters were obtained from the linear plots of 1/Cf versus 1/Cs and lnCf versus lnCs, respectively, and listed in Table 2. From Table 2, it Table 2. Langmuir and Freundlich Adsorption Parameters of Quercetin and Rutin for Silk Langmuir

Freundlich 2

sample

KL (L/g)

S (mg/g)

R

quercetin rutin

0.684 0.268

212.77 72.46

0.9961 0.9998

KF (L/g)

n

R2

0.130 0.036

1.05 0.88

0.9911 0.9974

is clear that the Langmuir equation fit quite well with the experimental points (R2 = 0.9961 for quercetin, R2 = 0.9998 for rutin), whereas the Freundlich equation displayed slightly lower correlation coefficients (R2 = 0.9911 for quercetin, R2=0.9974 for rutin). This indicates that the Langmuir adsorption mechanism is more favorable than the Freundlich adsorption mechanium. On the other hand, the Freundlich exponent n was very close to 1, indicating that the reactive sites of silk fiber available for the adsorption of quercetin and rutin have a high degree of homogeneity. These results indicate the significant contribution of the chemisorption process in a monolayer followed by multilayer physisorption. Our previous work showed that silk fiber has an isoelectric point of 4.32.6 Therefore, silk fiber is positively charged at pH 2.75, which was used in this study, owing to the protonation of amino groups in its structure. The ion−ion interactions of the positively charged silk fiber with the deprotonated phenolic hydroxyl groups in quercetin and rutin can contribute to the Langmuir adsorption. The dissociation constants (pKa1) of quercetin and rutin reported in the literature are 5.87 and 7.1, respectively.23,30 At these pH values, the ionized fraction of phenolic hydroxyl groups is 50%. Thus, in the adsorption process, as a small quantity of hydroxyl groups in quercetin and rutin molecules are subjected to deprotonation at the pH used and adsorbed by the positively charged silk fiber, their dynamic ionization equilibrium is broken, which can promote the further disassociation and adsorption of quercetin and rutin. Additionally, quercetin and rutin have multiple hydrogen groups, and silk fiber bears a large amount of amide, amino, and carboxyl groups. Thus, hydrogen bonding can occur between silk fiber and quercetin and rutin. There also exist van der Waals forces between silk and quercetin and rutin, which contribute to the Freundlich adsorption. As far as the adsorption parameters were concerned, quercetin showed a higher Langmuir affinity constant (KL), Freundlich affinity constant (KF), and adsorption saturation (S) than rutin. The high KL and KF values reveal that quercetin has a higher affinity to silk fiber than rutin, which agrees well with the results of the adsorption kinetics mentioned above.

Figure 6. Exhaustion and adsorption quantity of quercetin and rutin on silk at various concentrations (a) and color characteristics of the treated silk fabrics (b).

continued to increase as its initial concentration increased, and the exhaustion percentage was still above 60% even at the initial concentration of 6% owf, indicating its good building-up capability and high utilization. However, rutin displayed much lower exhaustion and adsorption quantity than those of quercetin. The poor building-up ability of rutin would mean a high application cost. As quercetin and rutin are pale yellow in color, their treatment can exert certain impacts on the appearance of silk. As shown in Figure 6b, the treated silk fabrics displayed increasing b* values and color difference (DE in the inserted table) along with increasing concentrations of quercetin and rutin. Compared with the untreated silk, the treated samples showed a palely brilliant yellow appearance. Quite evidently, rutin had a smaller effect on the color of silk than quercetin. Functionalities. Antioxidant Activity. Previous studies have reported that the catechol moiety in the B-ring, the 3hydroxyl group in the C-ring, and the hydroxyl groups in the Aring contribute to the antioxidant action of flavonoids.31 Generally, quercetin exhibits higher antioxidant activity than rutin in vitro as it bears the free 3-hydroxyl group in the C-ring and a greater number of hydroxyl groups.17 For the treated silk fabrics, their antioxidant activity depends not only on the 10522


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ACS Sustainable Chemistry & Engineering molecular structures of flavonoids but also on the adsorption quantities of flavonoids. As seen in Figure 7a, the original silk exhibited poor antioxidant activity when compared to those of the quercetin-

Figure 8. Correlation of the antibacterial activity of the treated silk with the initial application concentration (a) and adsorption quantity (b) of quercetin and rutin.

antibacterial activity than quercetin although its adsorption amount (Cf 11.42 mg/g) was slightly lower than that of quercetin (Cf 15.33 mg/g). This is also an unexpected phenomenon, which is considered to originate from the high extent of the desorption of rutin from silk in the bacteria solution during the process of the antibacterial activity test. UV Protection Performance. It is common knowledge that overexposure to solar UV radiation may lead to increasing skin problems. Hence, developing UV protective clothes is a simple and effective measure to reduce or prevent skin risks. Because UVC (100−280 nm) is blocked by the earth’s atmosphere, UVA (315−400 nm) and UVB (280−315 nm) radiations exert considerable influence on the UV protection performance of textiles.33 Most silk fabrics have poor UV protection ability because of their lightweight character. The untreated fabric showed high UV transmittance in the UVA and UVB region ranging from 290 to 450 nm (Figure 9a and b) and accordingly had a very low UPF of 4.91 (Figure 9c). Both quercetin and rutin exhibited obvious absorption peaks in the UV light region as shown in Figure 2, suggesting their potential application as UV protection finishing agents. As depicted in Figure 9a, the silk fabrics treated with low concentration (2% owf) of quercetin and rutin were effective in preventing the transmittance of UVA and UVB. Moreover, quercetin showed higher capability than rutin for reducing the transmittance of UVA and UVB through silk fabric at the same initial concentration (Figure 9b), giving rise to its higher UPF values (Figure 9c). Figure 9d shows the relationships between the UPF of the treated silk and the adsorption amount of quercetin and rutin. Clearly, the UPF of silk fabric did not increase obviously with increasing adsorption quantity of quercetin, implying that the UV protection ability of silk fabric is also restricted by the aggregation density of fibers in fabric. At almost the same adsorption quantity, quercetin showed slightly higher UPF than rutin. For example, the UPF of the quercetintreated silk fabric was 26.39 at Cf = 8.46 mg/g quercetin, whereas that of the rutin-treated silk fabric was 23.05 at Cf = 8.81 mg/g. This is directly related to the fact that quercetin possesses higher UV absorption intensity than rutin, as shown in Figure 2. Durability of Functionalities. In this section, the functionalities of the quercetin- and rutin-treated silk fabrics subjected to repeated washing were explored to clarify their durabilities. The fabrics treated with 2 and 8% owf quercetin and rutin were employed to assess the durability of antioxidant

Figure 7. Correlation of the antioxidant activity of the treated silk with the initial application concentration (a) and adsorption quantity (b) of quercetin and rutin.

and rutin-treated silk. The silk samples treated with quercetin and rutin showed remarkable antioxidant activity. The color of ABTS•+ faded away in a few minutes after the contact with the treated samples, indicating that the treated silk possessed highefficiency radical scavenging ability. The antioxidant activity of silk treated with 2% owf quercetin and rutin reached 99 and 82%, respectively, suggesting that a small quantity of quercetin and rutin can endow silk with excellent antioxidant activity. At the same initial concentration, quercetin can endow silk with higher antioxidant activity than rutin, mainly due to its higher adsorption capability on silk as mentioned above. Figure 7b is a further plot of Figure 7a, which reflects the relationship between the antioxidant activity of the treated silk and the adsorption quantity of flavonoids on silk. Clearly, the antioxidant activity increased with increasing adsorption quantity of flavonoids. It is interesting to note that the rutintreated silk was more effective in free radical scavenging than the quercetin-treated silk at almost the same adsorption quantity. To be specific, rutin showed an antioxidant value of 99.21% at the adsorption quantity of 8.81 mg/g, whereas the antioxidant activity of quercetin was 93.21% at the adsorption quantity of 8.46 mg/g. This phenomenon can be attributable to the fact that rutin is more easily desorbed from the treated silk in the ABTS·+ solution than quercetin due to its low affinity to silk and relatively high hydrophilicity. Antibacterial Activity. The antibacterial activity of quercetin and rutin in vitro has been reported to be achieved via molecular actions by forming a complex with proteins through nonspecific forces.32 In the present work, the antibacterial activities of the silk samples treated with 2 and 8% owf quercetin and rutin against E. coli and S. aureus were checked, and the results are depicted in Figure 8. The original silk fabric had poor antibacterial activity, and its reduction rates against E. coli and S. aureus were of 15 and 17%, respectively, whereas the treated silk presented significantly enhanced antibacterial performance that increased with an increase in the initial concentration of quercetin and rutin (Figure 8a). Moreover, the quercetin-treated silk showed higher antibacterial activity than the rutin-treated silk at the same initial application concentration. In the frame diagram of Figure 8b, a further plot of Figure 8a, rutin showed slightly higher 10523


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Figure 9. UV transmittance curves (a), UVA and UVB transmittance (b), UPF (c), and UV protection efficiency (d) of silk fabrics treated with quercetin and rutin at various concentrations.

functional modification, are important for practical applications. Thus, the related changes were studied in the present study. The morphological structures of silk fabrics were observed by SEM and are shown in Figure S2. Obviously, the treated silk fiber showed a clean and smooth surface as the untreated sample did, revealing that the morphological structure of silk fiber is not affected by the quercetin and rutin treatment. Additionally, the aggregates of quercetin and rutin were not found on the silk surface, indicating that quercetin and rutin diffuse into the fiber interior in the adsorption process. The thermal stability of the untreated and treated silk was investigated by TG analyses. As depicted in Figure S3, the treatment processes involving quercetin and rutin had a marginal effect on the thermal stability of silk. The evaluation of tensile strength was implemented by measuring the maximum stress of the stress−strain plot at the beginning of the breaking of the fabric. The stress−strain plots, which represent the average values, are shown in Figure S4. The mean tensile strength and elongation of the untreated sample at break were 461.2 ± 5.3 N and 26.2 ± 1.5%, respectively. The quercetin- and rutin-treated samples had average tensile strengths of 428.0 ± 5.8 and 428.1 ± 6.3 N, respectively, and their average elongations were 35.3 ± 2.5% and 36.9 ± 1.7%, respectively. The tensile strength deterioration of the quercetin- and rutin-treated fabrics is caused by the hydrolysis of silk fiber at low pH and high temperature. For the wet processing of silk, a small decrease in tensile strength is permissible and may not have a great impact on the application of silk fabric. After the treatment, silk fabric had a slightly increased elongation, which is mainly attributed to the swelling of silk fiber, leading to the shrinkage of silk fabric.

activity and UV protection ability, and the 8% owf quercetin- or rutin-treated silk was used to explore the durability of antibacterial performance. As seen in Figure 10a, the antioxidant activity of the treated silk decreased with increasing washing cycle. However, the decline of antioxidant activity was greater for the rutin-treated silk than for the quercetin-treated silk. For the 8% owf quercetin-treated silk, its antibacterial activity values against E. coli and S. aureus decreased to 70.2 and 74.8%, respectively, after 10 washing cycles, but they were always higher than those of the rutin-treated silk (Figure 10b). The UPF of the quercetin-treated silk showed little variation after 10 washing cycles, whereas for the silk treated with 2 and 8% owf rutin, its UPF declined to 9.44 and 13.86, respectively (Figure 10c). Figure 10 reveals that the rutin-treated silk had an obvious reduction in functionalities after 10 washing cycles in comparison with the quercetin-treated silk. These results are in close relationship with the differences in the affinity of quercetin and rutin to silk fiber and the desorption performance (Figure S1) of quercetin and rutin from silk fiber in water. On the other hand, considering practical applications, the development of the multifunctional materials with distinctive washing durability is also the target to cater to different demands. For instance, in the case that the multifunctional silk has to be subjected to repeated washing cycles during its lifetime, the quercetin-treated silk is desirable. To manufacture the medical materials with sustained release of antioxidants during usage, rutin-treated silk is the better choice. In light of the tests on the functionality durability and flavonoid desorption of the treated silk, a low dosage (2% owf) of quercetin is sufficient for the manufacture of the washing resistant and functional silk materials, and a high concentration (8% owf) of rutin is suitable for the preparation of the medical materials with sustained release function. Changes in the Surface Morphology, Thermal Stability and Mechanical Performance of Silk. No or small changes in the morphological structure, thermal stability, and mechanical property of silk fiber, which is subjected to

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CONCLUSIONS In the present work, two flavonoids (quercetin and rutin) with similar structures were applied to prepare multifunctional silk materials by an adsorption technique. The adsorption kinetics of quercetin and rutin onto silk obeyed the pseudo-secondorder kinetic model, and the equilibrium adsorption isotherms fit well to the Langmuir and Freundlich adsorption models. 10524



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ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acssuschemeng.7b02513. Desorption rate of quercetin and rutin from the treated silk in water and SEM images, TG curves, and stress− strain curves of the untreated, quercetin-treated, and rutin-treated silk fabrics (PDF)

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. Fax: +86 512 6724 6786. Tel.: +86 512 6716 4993. ORCID

Ren-Cheng Tang: 0000-0001-7220-860X Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This study was funded by Jiangsu Provincial Key Research and Development Program of China (BE2015066), the Priority Academic Program Development (PAPD) of Jiangsu Higher Education Institutions (No. 2014-37), and the Research Innovation Program for College Graduates of Jiangsu Province (KYLX16_0137).

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REFERENCES

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Figure 10. Functionality changes of the quercetin and rutin treated silk after repeated washing: antioxidant activity (a), antibacterial activity (b) and UV protection performance (c).

Quercetin exhibited a higher adsorption capability toward silk than rutin because of its high affinity to silk and conferred better antibacterial, antioxidant, and UV protection performance to silk than rutin at the same initial application concentration. However, at almost the same adsorption quantity, rutin imparted slightly higher antibacterial and antioxidant activity to silk due to its higher extent of desorption from silk in aqueous solution caused by its low affinity to silk. Additionally, the functionalities of the quercetin-treated silk showed better washing resistance than those of the rutintreated silk. In conclusion, quercetin is favorable for the manufacture of the functional silk materials subjected to repeated washing, and rutin is suitable for the preparation of medical materials with sustained release of antioxidants during usage. 10525


Research Article

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Natural Flavonoid-Functionalized Silk Fiber Presenting Antibacterial

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